57 results on '"Eves-van den Akker S"'
Search Results
2. Shared transcriptional control and disparate gain and loss of aphid parasitism genes
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Thorpe, Peter, Carmen, Escudero-Martinez, Peter, Cock, Eves-van-den-Akker, S, Jorunn, Boss, and Apollo - University of Cambridge Repository
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aphids ,shared transcriptional control ,food and beverages ,horizontal gene transfer ,biochemical phenomena, metabolism, and nutrition ,genome evolution ,effectors - Abstract
Aphids are a diverse group of taxa that contain agronomically important species, which vary in their host range and ability to infest crop plants. The genome evolution underlying agriculturally important aphid traits is not well understood. We generated draft genome assemblies for two aphid species: Myzus cerasi (black cherry aphid), and the cereal specialist Rhopalosiphum padi. Using a de novo gene prediction pipeline on both these, and three additional aphid genome assemblies (Acyrthosiphon pisum, D. noxia and M. persicae), we show that aphid genomes consistently encode similar gene numbers. We compare gene content, gene duplication, synteny, and putative effector repertoires between these five species to understand the genome evolution of globally important plant parasites. Aphid genomes show signs of relatively distant gene duplication, and substantial, relatively recent, gene birth. Putative effector repertoires, originating from duplicated and other loci have an unusual genomic organisation and evolutionary history. We identify a highly conserved effector-pair that is tightly physically-linked in the genomes of all aphid species tested. In R. padi, this effector pair is tightly transcriptionally-linked, and shares an unknown transcriptional control mechanism with a subset of approximately 50 other putative effectors and secretory proteins. This study extends our current knowledge on the evolution of aphid genomes and reveals evidence for an as of yet unknown shared control mechanism, which underlies effector expression, and ultimately plant parasitism.
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- 2018
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3. The structure of a glutathione synthetase like-effector (GSS22) from Globodera pallida in apoform.
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Lilley, C.J., primary, Maqbool, A., additional, Wu, D., additional, Yusup, H.B., additional, Jones, L.M., additional, Birch, P.R.J., additional, Banfield, M.J., additional, Urwin, P.E., additional, and Eves-van den Akker, S., additional
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- 2018
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4. The structure of a glutathione synthetase like-effector (GSS22) from Globodera pallida in ADP-bound closed conformation.
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Lilley, C.J., primary, Maqbool, A., additional, Wu, D., additional, Yusup, H.B., additional, Jones, L.M., additional, Birch, P.R.J., additional, Banfield, M.J., additional, Urwin, P.E., additional, and Eves-van den Akker, S., additional
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- 2018
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5. The structure of a glutathione synthetase (StGSS1) from Solanum tuberosum in ADP and y-EC bound closed conformation.
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Lilley, C.J., primary, Maqbool, A., additional, Wu, D., additional, Yusup, H.B., additional, Jones, L.M., additional, Birch, P.R.J., additional, Banfield, M.J., additional, Urwin, P.E., additional, and Eves-van den Akker, S., additional
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- 2018
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6. Foundational and translational research opportunities to improve plant health
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Michelmore, R., Coaker, G., Bart, R., Beattie, G., Bent, A., Bruce, T., Cameron, D., Dangl, J., Dinesh-Kumar, S., Edwards, R., Eves-van den Akker, S., Gassmann, W., Greenberg, J., Harrison, R., He, P., Harvey, J., Huffaker, A., Hulbert, S., Innes, R., Jones, J., Kaloshian, I., Kamoun, S., Katagiri, F., Leach, J., Ma, W., McDowell, J., Medford, J., Meyers, B., Nelson, R., Oliver, Richard, Qi, Y., Saunders, D., Shaw, M., Subudhi, P., Torrance, L., Tyler, B., Walsh, J., Michelmore, R., Coaker, G., Bart, R., Beattie, G., Bent, A., Bruce, T., Cameron, D., Dangl, J., Dinesh-Kumar, S., Edwards, R., Eves-van den Akker, S., Gassmann, W., Greenberg, J., Harrison, R., He, P., Harvey, J., Huffaker, A., Hulbert, S., Innes, R., Jones, J., Kaloshian, I., Kamoun, S., Katagiri, F., Leach, J., Ma, W., McDowell, J., Medford, J., Meyers, B., Nelson, R., Oliver, Richard, Qi, Y., Saunders, D., Shaw, M., Subudhi, P., Torrance, L., Tyler, B., and Walsh, J.
- Abstract
This white paper reports the deliberations of a wo rkshop focused on biotic challenges to plant health held in Washington, D.C. in September 2016. Ensuring health of food plants is critical to maintaining the quality and productivity of crops and for sustenance of the rapidly growing human population. There is a close linkage between food security and societal stabil ity; however, global food security is threatened by the vulnerability of our agricultural systems to numerous pests, pathogens, weeds, and environmental stresses. These threats are aggravated by climate ch ange, the globalization of agriculture, and an over- reliance on non-sustainable inputs. New analytical and computational technologies are providing unprecedented resolution at a variety of molecular, cellular, organismal, and population scales for crop plants as well as pathogens, pests, beneficial microbes, and weeds. It is now possible to both characterize useful or deleterious variation as well as precisely manipulate it. Data-driven, informed decisions based on knowledge of the variation of biot ic challenges and of natural and synthetic variation in crop plants will enable deployment of durable in terventions throughout the world. These should be integral, dynamic components of agricultural strategies for sustainable agriculture.
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- 2017
7. Functional C-terminally encoded plant peptide (CEP) hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis
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Eves-van den Akker, S, Lilley, CJ, Yusup, HB, Jones, JT, and Urwin, PE
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Sedentary Plant-Parasitic Nematodes (PPNs) induce and maintain an intimate relationship with their host, stimulating cells adjacent to root vascular tissue to re-differentiate into unique and metabolically active “feeding sites”. The interaction between PPNs and their host is mediated by nematode effectors. We describe the discovery of a large and diverse family of effector genes, encoding C-terminally Encoded Peptide (CEP) plant hormone mimics (RrCEPs), in the syncytia-forming plant-parasite Rotylenchulus reniformis. The particular attributes of RrCEPs distinguish them from all other CEPs, regardless of origin. Together with the distant phylogenetic relationship of R. reniformis to the only other CEP-encoding nematode genus identified to date (Meloidogyne), this suggests CEPs likely evolved de novo in R. reniformis. We have characterised the first member of this large gene family (RrCEP1), demonstrating its significant upregulation during the plant-nematode interaction and expression in the effector-producing pharyngeal gland cell. All internal CEP domains of multi-domain RrCEPs are followed by di-basic residues, suggesting a mechanism for cleavage. A synthetic peptide corresponding to RrCEP1 domain 1 is biologically active and capable of upregulating plant nitrate transporter (AtNRT2.1) expression, while simultaneously reducing primary root elongation. When a non-CEP containing, syncytia-forming PPN species (Heterodera schachtii) infects Arabidopsis in a CEP-rich environment a smaller feeding site is produced. We hypothesise that CEPs of R. reniformis represent a two-fold adaptation to sustained biotrophy in this species; 1) increasing host nitrate uptake while 2) limiting the size of the syncytial feeding site produced.
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- 2016
8. The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence
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Eves-van den Akker, S, Laetsch, DR, Thorpe, P, Lilley, CJ, Danchin, EGJ, Da Rocha, M, Rancurel, C, Holroyd, NE, Cotton, JA, Szitenberg, A, Grenier, E, Montarry, J, Mimee, B, Duceppe, MO, Boyes, I, Marvin, JMC, Jones, LM, Yusup, HB, Lafond-Lapalme, J, Esquibet, M, Sabeh, M, Rott, M, Overmars, H, Finkers-Tomczak, A, Smant, G, Koutsovoulos, G, Blok, V, Mantelin, S, Cock, PJA, Phillips, W, Henrissat, B, Urwin, PE, Blaxter, M, Jones, JT, Eves-Van Den Akker, Sebastian [0000-0002-8833-9679], Apollo - University of Cambridge Repository, Institut Sophia Agrobiotech (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Architecture et fonction des macromolécules biologiques (AFMB), Institut National de la Recherche Agronomique (INRA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), BB/F000642/1, Biotechnology and Biological Sciences Research Council, grant 098051, Wellcome Trust, FA 1208, European Cooperation in Science and Technology, CRTI09_462RD, Canadian Safety and Security Program, Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)-Institut National de la Recherche Agronomique (INRA), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), AGROCAMPUS OUEST-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de la Recherche Agronomique (INRA), University of St Andrews. School of Medicine, University of St Andrews. School of Biology, and University of St Andrews. Biomedical Sciences Research Complex
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Gene Transfer, Horizontal ,Genomic Islands ,QH301 Biology ,RNA Splicing ,globodera rostochiensis ,transfert horizontal de gène ,QH301 ,pomme de terre ,[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN] ,Animals ,Position-Specific Scoring Matrices ,[SDV.MP.PAR]Life Sciences [q-bio]/Microbiology and Parasitology/Parasitology ,Tylenchoidea ,Nucleotide Motifs ,Laboratorium voor Nematologie ,R2C ,Plant Diseases ,Solanum tuberosum ,Life Cycle Stages ,Virulence ,Gene Expression Profiling ,Research ,~DC~ ,High-Throughput Nucleotide Sequencing ,Genomics ,Horizontal gene transfer ,[SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM] ,Effectors ,[SDV.BV.PEP]Life Sciences [q-bio]/Vegetal Biology/Phytopathology and phytopharmacy ,séquence du génome ,Enhancer Elements, Genetic ,effector ,Genome sequence ,potato ,RNA Splice Sites ,EPS ,Laboratory of Nematology ,BDC ,Transcriptome ,Genome, Protozoan ,Plant-parasitic nematode - Abstract
SE-vdA is supported by BBSRC grant BB/M014207/1. Sequencing was funded by BBSRC grant BB/F000642/1 to the University of Leeds and grant BB/F00334X/1 to the Wellcome Trust Sanger Institute). DRL was supported by a fellowship from The James Hutton Institute and the School of Biological Sciences, University of Edinburgh. GK was supported by a BBSRC PhD studentship. The James Hutton Institute receives funding from the Scottish Government. JAC and NEH are supported by the Wellcome Trust through its core funding of the Wellcome Trust Sanger Institute (grant 098051). This work was also supported by funding from the Canadian Safety and Security Program, project number CRTI09_462RD. Background. The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes. Results. We generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative ‘effector islands’ in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking. Conclusions. These G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action. Publisher PDF
- Published
- 2016
9. Comparative genomics/transcriptomics to study effector gene birth in plant-parasitic nematodes
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Eves-van den Akker, S., Lilley, C. J., Danchin, Etienne, Rancurel, Corinne, Cock, P. J. A., Jones, L. M., Yusup, H. B., Jones, J. T., Urwin, P. E., Dundee Effector Consortium, The James Hutton Institute, Norwich Research Park, Centre for Plant Sciences, University of Leeds, Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), School of Biology, IE University, and Society of Nematologists. Marceline, Missouri, USA.
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[SDV]Life Sciences [q-bio] ,[SDE]Environmental Sciences ,ComputingMilieux_MISCELLANEOUS - Abstract
International audience
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- 2015
10. A genomic resource for the sedentary semi-endoparasitic reniform nematode, Rotylenchulus reniformis Linford & Oliveira
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Showmaker Kurt C., Sanders William S., Eves-van den Akker Sebastian, Martin Brigitte E., Platt Roy N., Stokes John V., Hsu Chuan-Yu, Bartlett Benjamin D., Peterson Daniel G., and Wubben Martin J.
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Biology (General) ,QH301-705.5 - Abstract
The reniform nematode (Rotylenchulus reniformis) is a sedentary semi-endoparasitic species that is pathogenic on many row crops, fruits, and vegetables. Here, the authors present a draft genome assembly of R. reniformis using small- and large-insert libraries sequenced on the Illumina GAIIx and MiSeq platforms.
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- 2019
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11. Transcriptional changes in the aphid species Myzus cerasi under different host and environmental conditions
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Thorpe, P, Escudero-Martinez, CM, Eves-Van Den Akker, S, and Bos, JIB
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Food Chain ,Gene Expression Profiling ,Adaptation, Biological ,food and beverages ,biochemical phenomena, metabolism, and nutrition ,15. Life on land ,Environment ,RNAseq ,laboratory environment ,aphid host adaptation ,Aphids ,Animals ,detoxification ,Transcriptome - Abstract
Aphids feature complex life cycles, which in the case of many agriculturally important species involve primary and secondary host plant species. Whilst host alternation between primary and secondary host can occur in the field depending on host availability and the environment, aphid populations maintained as laboratory stocks generally are kept under conditions that allow asexual reproduction by parthenogenesis on secondary hosts. We used Myzus cerasi (black cherry aphid) to assess aphid transcriptional differences between populations collected from primary hosts in the field and those adapted to secondary hosts under controlled environment conditions. Transfer of M. cerasi collected from local cherry trees to reported secondary host species resulted in low survival rates. Moreover, aphids were unable to survive on the secondary host land cress, unless first adapted to another secondary host, cleavers. Transcriptome analyses of the different aphid populations (field collected and adapted) revealed extensive transcriptional plasticity to a change in environment, with predominantly genes involved in redox reactions differentially regulated. Most of the differentially expressed genes were duplicated and we found evidence for differential exon usage. Our data suggest that aphid adaptation to different environments may pose a major hurdle and leads to extensive gene expression changes.
12. The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals in-sights into the bases of parasitism and virulence
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Eves-Van Den Akker, S., Laetsch, D. R., Thorpe, P., Lilley, C. J., Danchin, E. G. J., Darocha, M., Rancurel, C., Holroyd, N. E., Cotton, J. A., Szitenberg, A., Grenier, E., Montarry, J., Mimee, B., Duceppe, M., Boyes, I., Marvin, J. M. C., Jones, L. M., Yusup, H. B., Lafond-Lapalme, J., Esquibet, M., Sabeh, M., Rott, M., Overmars, H., Finkers-Tomczak, A., Smant, G., Koutsovoulos, G., Blok, V., Mantelin, S., Cock, P. J. A., Phillips, W., Henrissat, B., Urwin, P. E., Mark Blaxter, Jones, J. T., Division of Plant Sciences, College of Life Sciences, University of Dundee, Institute of Evolutionary Biology, Cell and Molecular Sciences Group, Dundee Effector Consortium, The James Hutton Institute, Centre for Plant Sciences, University of Leeds, Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Wellcome Trust Genome Campus, The Wellcome Trust Sanger Institute [Cambridge], School of Biological, Biomedical and Environmental Sciences, University of Hull, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Horticulture Research and Development Centre, Agriculture and Agri-Food [Ottawa] (AAFC), Sidney Laboratory, Canadian Food Inspection Agency (CFIA), Laboratory of Nematology, Department of Plant Sciences, Wageningen University and Research Center (WUR), Information and Computational Sciences Group, Horticultural Crops Research Laboratory, USDA-ARS : Agricultural Research Service, Architecture et fonction des macromolécules biologiques (AFMB), Institut National de la Recherche Agronomique (INRA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Department of Biological Sciences, The Open University [Milton Keynes] (OU), School of Biology, University of St Andrews, University of St Andrews [Scotland], Institut Sophia Agrobiotech (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Agriculture and Agri-Food (AAFC), Wageningen University and Research [Wageningen] (WUR), School of Biology [University of St Andrews], Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), and Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)-Institut National de la Recherche Agronomique (INRA)
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Vertebrate Zoology ,[SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology ,Zoologie des vertébrés - Abstract
The yellow potato cyst nematode Globodera rostochiensis is a devastating plant pathogen of global economic importance, classified into pathotypes of different plant resistance-breaking phenotypes. G. rostochiensis secretes effectors, some of which were acquired by horizontal gene transfer (HGT), from pharyngeal glands into the host to manipulate host processes and promote parasitism. We generated a high-quality genome assembly for G. rostochiensis pathotype Ro1 and identified putative effectors and HGT events, mapped gene expression through the life cycle focusing on key parasitic transitions, and sequenced the genomes of eight populations including three additional pathotypes.
13. Duplication of hsp-110 Is Implicated in Differential Success of Globodera Species under Climate Change
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Howard J. Atkinson, Peter E. Urwin, Laura M. Jones, Patricija van-Oosten Hawle, Sebastian Eves-van den Akker, Eves-van den Akker, S, van-Oosten Hawle, P, Atkinson, HJ, Eves-Van Den Akker, Sebastian [0000-0002-8833-9679], and Apollo - University of Cambridge Repository
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0106 biological sciences ,0301 basic medicine ,Hot Temperature ,Climate Change ,Zoology ,Climate change ,Biology ,01 natural sciences ,thermotolerance ,Crop ,03 medical and health sciences ,Rhabditida ,Species Specificity ,Gene duplication ,Genetics ,Animals ,Globodera ,Globodera pallida ,HSP110 Heat-Shock Proteins ,Caenorhabditis elegans ,Molecular Biology ,Gene ,Ecology, Evolution, Behavior and Systematics ,Discoveries ,Invertebrate ,gene duplication ,hsf-1 ,biology.organism_classification ,030104 developmental biology ,13. Climate action ,heat shock proteins ,Molecular mechanism ,Female ,PEST analysis ,Heat-Shock Response ,010606 plant biology & botany - Abstract
Managing the emergence and spread of crop pests and pathogens is essential for global food security. Understanding how organisms have adapted to their native climate is key to predicting the impact of climate change. The potato cyst nematodes Globodera pallida and G. rostochiensis are economically important plant pathogens that cause yield losses of up to 50% in potato. The two species have different thermal optima that may relate to differences in the altitude of their regions of origin in the Andes. Here, we demonstrate that juveniles of G. pallida are less able to recover from heat stress than those of G. rostochiensis. Genome-wide analysis revealed that while both Globodera species respond to heat stress by induction of various protective heat-inducible genes, G. pallida experiences heat stress at lower temperatures. We use C. elegans as a model to demonstrate the dependence of the heat stress response on expression of Heat Shock Factor-1 (HSF-1). Moreover, we show that hsp-110 is induced by heat stress in G. rostochiensis, but not in the less thermotolerant G. pallida. Sequence analysis revealed that this gene and its promoter was duplicated in G. rostochiensis and acquired thermoregulatory properties. We show that hsp-110 is required for recovery from acute thermal stress in both C. elegans and in G. rostochiensis. Our findings point towards an underlying molecular mechanism that allows the differential expansion of one species relative to another closely related species under current climate change scenarios. Similar mechanisms may be true of other invertebrate species with pest status.
- Published
- 2018
14. The origin, deployment, and evolution of a plant-parasitic nematode effectorome.
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Molloy B, Shin DS, Long J, Pellegrin C, Senatori B, Vieira P, Thorpe PJ, Damm A, Ahmad M, Vermeulen K, Derevnina L, Wei S, Sperling A, Reyes Estévez E, Bruty S, de Souza VHM, Kranse OP, Maier T, Baum T, and Eves-van den Akker S
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- Animals, Tylenchoidea genetics, Plants parasitology, Helminth Proteins genetics, Helminth Proteins metabolism, Nematoda genetics, Plant Diseases parasitology, Host-Parasite Interactions
- Abstract
Plant-parasitic nematodes constrain global food security. During parasitism, they secrete effectors into the host plant from two types of pharyngeal gland cells. These effectors elicit profound changes in host biology to suppress immunity and establish a unique feeding organ from which the nematode draws nutrition. Despite the importance of effectors in nematode parasitism, there has been no comprehensive identification and characterisation of the effector repertoire of any plant-parasitic nematode. To address this, we advance techniques for gland cell isolation and transcriptional analysis to define a stringent annotation of putative effectors for the cyst nematode Heterodera schachtii at three key life-stages. We define 717 effector gene loci: 269 "known" high-confidence homologs of plant-parasitic nematode effectors, and 448 "novel" effectors with high gland cell expression. In doing so we define the most comprehensive "effectorome" of a plant-parasitic nematode to date. Using this effector definition, we provide the first systems-level understanding of the origin, deployment and evolution of a plant-parasitic nematode effectorome. The robust identification of the effector repertoire of a plant-parasitic nematode will underpin our understanding of nematode pathology, and hence, inform strategies for crop protection., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2024 Molloy et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)
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- 2024
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15. A gene with a thousand alleles: The hyper-variable effectors of plant-parasitic nematodes.
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Sonawala U, Beasley H, Thorpe P, Varypatakis K, Senatori B, Jones JT, Derevnina L, and Eves-van den Akker S
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- Animals, Plants parasitology, Plants genetics, Nematoda genetics, Genetic Variation genetics, Plant Diseases parasitology, Alleles
- Abstract
Pathogens are engaged in a fierce evolutionary arms race with their host. The genes at the forefront of the engagement between kingdoms are often part of diverse and highly mutable gene families. Even in this context, we discovered unprecedented variation in the hyper-variable (HYP) effectors of plant-parasitic nematodes. HYP effectors are single-gene loci that potentially harbor thousands of alleles. Alleles vary in the organization, as well as the number, of motifs within a central hyper-variable domain (HVD). We dramatically expand the HYP repertoire of two plant-parasitic nematodes and define distinct species-specific "rules" underlying the apparently flawless genetic rearrangements. Finally, by analyzing the HYPs in 68 individual nematodes, we unexpectedly found that despite the huge number of alleles, most individuals are germline homozygous. These data support a mechanism of programmed genetic variation, termed HVD editing, where alterations are locus specific, strictly governed by rules, and theoretically produce thousands of variants without errors., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.)
- Published
- 2024
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16. A Critical Appraisal of DNA Transfer from Plants to Parasitic Cyst Nematodes.
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Ko I, Kranse OP, Senatori B, and Eves-van den Akker S
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- Animals, DNA, Genomics, Plant Diseases parasitology, Plants genetics, Tylenchoidea genetics
- Abstract
Plant-parasitic nematodes are one of the most economically important pests of crops. It is widely accepted that horizontal gene transfer-the natural acquisition of foreign genes in parasitic nematodes-contributes to parasitism. However, an apparent paradox has emerged from horizontal gene transfer analyses: On the one hand, distantly related organisms with very dissimilar genetic structures (i.e. bacteria), and only transient interactions with nematodes as far as we know, dominate the list of putative donors, while on the other hand, considerably more closely related organisms (i.e. the host plant), with similar genetic structure (i.e. introns) and documented long-term associations with nematodes, are rare among the list of putative donors. Given that these nematodes ingest cytoplasm from a living plant cell for several weeks, there seems to be a conspicuous absence of plant-derived cases. Here, we used comparative genomic approaches to evaluate possible plant-derived horizontal gene transfer events in plant parasitic nematodes. Our evidence supports a cautionary message for plant-derived horizontal gene transfer cases in the sugar beet cyst nematode, Heterodera schachtii. We propose a 4-step model for horizontal gene transfer from plant to parasite in order to evaluate why the absence of plant-derived horizontal gene transfer cases is observed. We find that the plant genome is mobilized by the nematode during infection, but that uptake of the said "mobilome" is the first major barrier to horizontal gene transfer from host to nematode. These results provide new insight into our understanding of the prevalence/role of nucleic acid exchange in the arms race between plants and plant parasites., (© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)
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- 2024
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17. Whole mount multiplexed visualization of DNA, mRNA, and protein in plant-parasitic nematodes.
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Sperling AL and Eves-van den Akker S
- Abstract
Background: Plant-parasitic nematodes compromise the agriculture of a wide variety of the most common crops worldwide. Obtaining information on the fundamental biology of these organisms and how they infect the plant has been restricted by the ability to visualize intact nematodes using small molecule stains, antibodies, or in situ hybridization. Consequently, there is limited information available about the internal composition of the nematodes or the biology of the effector molecules they use to reprogram their host plant., Results: We present the Sperling prep - a whole mount method for nematode preparation that enables staining with small molecules, antibodies, or in situ hybridization chain reaction. This method does not require specialized apparatus and utilizes typical laboratory equipment and materials. By dissociating the strong cuticle and interior muscle layers, we enabled entry of the small molecule stains into the tissue. After permeabilization, small molecule stains can be used to visualize the nuclei with the DNA stain DAPI and the internal structures of the digestive tract and longitudinal musculature with the filamentous actin stain phalloidin. The permeabilization even allows entry of larger antibodies, albeit with lower efficiency. Finally, this method works exceptionally well with in situ HCR. Using this method, we have visualized effector transcripts specific to the dorsal gland and the subventral grand of the sugar beet cyst nematode, Heterodera schachtii, multiplexed in the same nematode., Conclusion: We were able to visualize the internal structures of the nematode as well as key effector transcripts that are used during plant infection and parasitism. Therefore, this method provides an important toolkit for studying the biology of plant-parasitic nematodes., (© 2023. The Author(s).)
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- 2023
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18. Phosphate Recovery from Urine-Equivalent Solutions for Fertilizer Production for Plant Growth.
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Avena Maia M, Kranse OP, Eves-van den Akker S, and Torrente-Murciano L
- Abstract
This study presents a proof of concept for the recovery of phosphate from aqueous solutions with high phosphorus (PO
4 -P) initial contents to simulate the concentration of streams from decentralized wastewater systems. Solutions with ∼500 ppm phosphorus enable phosphate adsorption and recovery, in contrast to the highly diluted inlet streams (<10 ppm) from centralized wastewater treatment plants. In this work, Mg-Fe layered double hydroxide is used as a phosphate adsorbent, demonstrating its separation from aqueous streams, recovery, and use as a fertilizer following the principles of circular economy. We demonstrate that the mechanism of phosphate adsorption in this material is by a combination of surface complexation and electrostatic attraction. After the loss of crystallinity in the presence of water in the first cycle and its associated decrease in adsorption capacity, the Mg-Fe layered double hydroxide (LDH) is stable after consecutive adsorption/desorption cycles, where desorption solutions were reused to substantially increase the final phosphate concentration demonstrating the recyclability of the material in a semicontinuous process. Phosphate recovered in this way was used to complement phosphate-deficient plant growth medium, demonstrating its efficacy as a fertilizer and thereby promoting a circular and sustainable economy., Competing Interests: The authors declare no competing financial interest., (© 2023 The Authors. Published by American Chemical Society.)- Published
- 2023
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19. Integrated Nematode Management in a World in Transition: Constraints, Policy, Processes, and Technologies for the Future.
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Sikora RA, Helder J, Molendijk LPG, Desaeger J, Eves-van den Akker S, and Mahlein AK
- Subjects
- Humans, Animals, Agriculture, Policy, Soil, Technology, Tylenchida
- Abstract
Plant-parasitic nematodes are one of the most insidious pests limiting agricultural production, parasitizing mostly belowground and occasionally aboveground plant parts. They are an important and underestimated component of the estimated 30% yield loss inflicted on crops globally by biotic constraints. Nematode damage is intensified by interactions with biotic and abiotic factors constraints: soilborne pathogens, soil fertility degradation, reduced soil biodiversity, climate variability, and policies influencing the development of improved management options. This review focuses on the following topics: ( a ) biotic and abiotic constraints, ( b ) modification of production systems, ( c ) agricultural policies, ( d ) the microbiome, ( e ) genetic solutions, and ( f ) remote sensing. Improving integrated nematode management (INM) across all scales of agricultural production and along the Global North-Global South divide, where inequalities influence access to technology, is discussed. The importance of the integration of technological development in INM is critical to improving food security and human well-being in the future.
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- 2023
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20. Unlocking the development- and physiology-altering 'effector toolbox' of plant-parasitic nematodes.
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Molloy B, Baum T, and Eves-van den Akker S
- Subjects
- Animals, Host-Parasite Interactions physiology, Plants parasitology, Parasites, Nematoda physiology
- Abstract
Plant parasites take advantage of host developmental plasticity to elicit profound developmental and physiological changes. In the case of plant-parasitic nematodes (PPNs), these changes can result in the development of new plant organs. Despite the importance of the development- and physiology-altering abilities of these parasites in pathology, research has historically focused on their abilities to suppress immunity. We argue that, given the dramatic changes involved in feeding site establishment, it is entirely possible that development- and physiology-altering abilities of PPNs may, in fact, dominate effector repertoires - highlighting the need for novel high-throughput screens for development- and physiology-altering 'tools'. Uncovering this portion of the nematode 'toolbox' can enable biotechnology, enhance crop protection, and shed light on fundamental host biology itself., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 The Authors. Published by Elsevier Ltd.. All rights reserved.)
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- 2023
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21. A low-cost and open-source solution to automate imaging and analysis of cyst nematode infection assays for Arabidopsis thaliana.
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Kranse OP, Ko I, Healey R, Sonawala U, Wei S, Senatori B, De Batté F, Zhou J, and Eves-van den Akker S
- Abstract
Background: Cyst nematodes are one of the major groups of plant-parasitic nematode, responsible for considerable crop losses worldwide. Improving genetic resources, and therefore resistant cultivars, is an ongoing focus of many pest management strategies. One of the major bottlenecks in identifying the plant genes that impact the infection, and thus the yield, is phenotyping. The current available screening method is slow, has unidimensional quantification of infection limiting the range of scorable parameters, and does not account for phenotypic variation of the host. The ever-evolving field of computer vision may be the solution for both the above-mentioned issues. To utilise these tools, a specialised imaging platform is required to take consistent images of nematode infection in quick succession., Results: Here, we describe an open-source, easy to adopt, imaging hardware and trait analysis software method based on a pre-existing nematode infection screening method in axenic culture. A cost-effective, easy-to-build and -use, 3D-printed imaging device was developed to acquire images of the root system of Arabidopsis thaliana infected with the cyst nematode Heterodera schachtii, replacing costly microscopy equipment. Coupling the output of this device to simple analysis scripts allowed the measurement of some key traits such as nematode number and size from collected images, in a semi-automated manner. Additionally, we used this combined solution to quantify an additional trait, root area before infection, and showed both the confounding relationship of this trait on nematode infection and a method to account for it., Conclusion: Taken together, this manuscript provides a low-cost and open-source method for nematode phenotyping that includes the biologically relevant nematode size as a scorable parameter, and a method to account for phenotypic variation of the host. Together these tools highlight great potential in aiding our understanding of nematode parasitism., (© 2022. The Author(s).)
- Published
- 2022
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22. The DNA methylation landscape of the root-knot nematode-induced pseudo-organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism.
- Author
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Silva AC, Ruiz-Ferrer V, Müller SY, Pellegrin C, Abril-Urías P, Martínez-Gómez Á, Gómez-Rojas A, Berenguer E, Testillano PS, Andrés MF, Fenoll C, Eves-van den Akker S, and Escobar C
- Subjects
- Animals, Protein-Tyrosine Kinases genetics, Protein-Tyrosine Kinases metabolism, Gene Expression Regulation, Plant, DNA Methylation genetics, Plant Roots genetics, Plant Roots metabolism, Proto-Oncogene Proteins genetics, Proto-Oncogene Proteins metabolism, DNA (Cytosine-5-)-Methyltransferases genetics, DNA (Cytosine-5-)-Methyltransferases metabolism, Arabidopsis metabolism, Tylenchoidea physiology, Arabidopsis Proteins genetics, Arabidopsis Proteins metabolism
- Abstract
Root-knot nematodes (RKNs) induce giant cells (GCs) within galls which are characterized by large-scale gene repression at early stages. However, the epigenetic mechanism(s) underlying gene silencing is (are) still poorly characterized. DNA methylation in Arabidopsis galls induced by Meloidogyne javanica was studied at crucial infection stages (3 d post-infection (dpi) and 14 dpi) using enzymatic, cytological, and sequencing approaches. DNA methyltransferase mutants (met1, cmt2, cmt3, cmt2/3, drm1/2, ddc) and a DNA demethylase mutant (ros1), were analyzed for RKN resistance/tolerance, and galls were characterized by confocal microscopy and RNA-seq. Early galls were hypermethylated, and the GCs were found to be the major contributors to this hypermethylation, consistent with the very high degree of gene repression they exhibit. By contrast, medium/late galls showed no global increase in DNA methylation compared to uninfected roots, but exhibited large-scale redistribution of differentially methylated regions (DMRs). In line with these findings, it was also shown that DNA methylation and demethylation mutants showed impaired nematode reproduction and gall/GC-development. Moreover, siRNAs that were exclusively present in early galls accumulated at hypermethylated DMRs, overlapping mostly with retrotransposons in the CHG/CG contexts that might be involved in their repression, contributing to their stability/genome integrity. Promoter/gene methylation correlated with differentially expressed genes encoding proteins with basic cell functions. Both mechanisms are consistent with reprogramming host tissues for gall/GC formation. In conclusion, RNA-directed DNA methylation (RdDM; DRM2/1) pathways, maintenance methyltransferases (MET1/CMT3) and demethylation (ROS1) appear to be prominent mechanisms driving a dynamic regulation of the epigenetic landscape during RKN infection., (© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.)
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- 2022
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23. The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5.
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Siddique S, Radakovic ZS, Hiltl C, Pellegrin C, Baum TJ, Beasley H, Bent AF, Chitambo O, Chopra D, Danchin EGJ, Grenier E, Habash SS, Hasan MS, Helder J, Hewezi T, Holbein J, Holterman M, Janakowski S, Koutsovoulos GD, Kranse OP, Lozano-Torres JL, Maier TR, Masonbrink RE, Mendy B, Riemer E, Sobczak M, Sonawala U, Sterken MG, Thorpe P, van Steenbrugge JJM, Zahid N, Grundler F, and Eves-van den Akker S
- Subjects
- Animals, Pantothenic Acid, Transcriptome, Parasites, Tylenchida, Cysts
- Abstract
Plant-parasitic nematodes are a major threat to crop production in all agricultural systems. The scarcity of classical resistance genes highlights a pressing need to find new ways to develop nematode-resistant germplasm. Here, we sequence and assemble a high-quality phased genome of the model cyst nematode Heterodera schachtii to provide a platform for the first system-wide dual analysis of host and parasite gene expression over time, covering all major parasitism stages. Analysis of the hologenome of the plant-nematode infection site identified metabolic pathways that were incomplete in the parasite but complemented by the host. Using a combination of bioinformatic, genetic, and biochemical approaches, we show that a highly atypical completion of vitamin B5 biosynthesis by the parasitic animal, putatively enabled by a horizontal gene transfer from a bacterium, is required for full pathogenicity. Knockout of either plant-encoded or now nematode-encoded steps in the pathway significantly reduces parasitic success. Our experiments establish a reference for cyst nematodes, further our understanding of the evolution of plant-parasitism by nematodes, and show that congruent differential expression of metabolic pathways in the infection hologenome represents a new way to find nematode susceptibility genes. The approach identifies genome-editing-amenable targets for future development of nematode-resistant crops., (© 2022. The Author(s).)
- Published
- 2022
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24. Targeted transcriptomics reveals signatures of large-scale independent origins and concerted regulation of effector genes in Radopholus similis.
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Vieira P, Myers RY, Pellegrin C, Wram C, Hesse C, Maier TR, Shao J, Koutsovoulos GD, Zasada I, Matsumoto T, Danchin EGJ, Baum TJ, Eves-van den Akker S, and Nemchinov LG
- Subjects
- Animals, Helminth Proteins genetics, Phylogeny, Nicotiana growth & development, Gene Expression Regulation, Helminth Proteins metabolism, Plant Diseases parasitology, Nicotiana parasitology, Transcriptome, Tylenchida physiology
- Abstract
The burrowing nematode, Radopholus similis, is an economically important plant-parasitic nematode that inflicts damage and yield loss to a wide range of crops. This migratory endoparasite is widely distributed in warmer regions and causes extensive destruction to the root systems of important food crops (e.g., citrus, banana). Despite the economic importance of this nematode, little is known about the repertoire of effectors owned by this species. Here we combined spatially and temporally resolved next-generation sequencing datasets of R. similis to select a list of candidates for the identification of effector genes for this species. We confirmed spatial expression of transcripts of 30 new candidate effectors within the esophageal glands of R. similis by in situ hybridization, revealing a large number of pioneer genes specific to this nematode. We identify a gland promoter motif specifically associated with the subventral glands (named Rs-SUG box), a putative hallmark of spatial and concerted regulation of these effectors. Nematode transcriptome analyses confirmed the expression of these effectors during the interaction with the host, with a large number of pioneer genes being especially abundant. Our data revealed that R. similis holds a diverse and emergent repertoire of effectors, which has been shaped by various evolutionary events, including neofunctionalization, horizontal gene transfer, and possibly by de novo gene birth. In addition, we also report the first GH62 gene so far discovered for any metazoan and putatively acquired by lateral gene transfer from a bacterial donor. Considering the economic damage caused by R. similis, this information provides valuable data to elucidate the mode of parasitism of this nematode., Competing Interests: The authors have declared that no competing interests exist.
- Published
- 2021
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25. Plant-nematode interactions.
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Eves-van den Akker S
- Subjects
- Animals, Host-Parasite Interactions, Plants, Nematoda, Plant Diseases
- Abstract
Plant-parasitic nematodes threaten food security in the developed and developing world. This review looks at the field through a wide lens, aiming to capture a breadth of recent landmark achievements that have changed our understanding of plant-nematode interactions in particular, and plant pathology in general. It recognises the importance of expanding existing paradigms in plant-pathology to encompass plant-nematode interactions and, at the same time, celebrates achievements that build on the uniqueness of the system. It highlights emerging areas of plant nematology. Finally, it argues that the accelerated progress of recent years is prophetic, and that cumulative advances in our understanding, coupled with technological advances in genetic engineering of plants and nematodes, promise to lift perennial constraints on the field and thereby further expedite progress., (Copyright © 2021 Elsevier Ltd. All rights reserved.)
- Published
- 2021
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26. Recent applications of biotechnological approaches to elucidate the biology of plant-nematode interactions.
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Eves-van den Akker S, Stojilković B, and Gheysen G
- Subjects
- Animals, Biology, Biotechnology, Plants genetics, Nematoda genetics, Plant Diseases
- Abstract
Plant-parasitic nematodes are a major threat to food security. The most economically important species have remarkable abilities to manipulate host physiology and immunity. This review highlights recent applications of biotechnological approaches to elucidate the underlying biology on both sides of the interaction. Their obligate biotrophic nature has hindered the development of simple nematode transformation protocols. Instead, transient or stable expression of the effector (native or tagged) in planta has been instrumental in elucidating the biology of plant-nematode interactions. Recent progress in the development of functional genetics tools 'in nematoda' promises further advances. Finally, we discuss how effector research has uncovered novel protein translocation routes in plant cells and may reveal additional unknown biological processes in the future., (Copyright © 2021 Elsevier Ltd. All rights reserved.)
- Published
- 2021
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27. How Do Pathogens Evolve Novel Virulence Activities?
- Author
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Sacristán S, Goss EM, and Eves-van den Akker S
- Subjects
- Phenotype, Virulence, Adaptation, Physiological, Host-Pathogen Interactions
- Abstract
This article is part of the Top 10 Unanswered Questions in MPMI invited review series.We consider the state of knowledge on pathogen evolution of novel virulence activities, broadly defined as anything that increases pathogen fitness with the consequence of causing disease in either the qualitative or quantitative senses, including adaptation of pathogens to host immunity and physiology, host species, genotypes, or tissues, or the environment. The evolution of novel virulence activities as an adaptive trait is based on the selection exerted by hosts on variants that have been generated de novo or arrived from elsewhere. In addition, the biotic and abiotic environment a pathogen experiences beyond the host may influence pathogen virulence activities. We consider host-pathogen evolution, host range expansion, and external factors that can mediate pathogen evolution. We then discuss the mechanisms by which pathogens generate and recombine the genetic variation that leads to novel virulence activities, including DNA point mutation, transposable element activity, gene duplication and neofunctionalization, and genetic exchange. In summary, if there is an (epi)genetic mechanism that can create variation in the genome, it will be used by pathogens to evolve virulence factors. Our knowledge of virulence evolution has been biased by pathogen evolution in response to major gene resistance, leaving other virulence activities underexplored. Understanding the key driving forces that give rise to novel virulence activities and the integration of evolutionary concepts and methods with mechanistic research on plant-microbe interactions can help inform crop protection.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
- Published
- 2021
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28. Genome Expression Dynamics Reveal the Parasitism Regulatory Landscape of the Root-Knot Nematode Meloidogyne incognita and a Promoter Motif Associated with Effector Genes.
- Author
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Da Rocha M, Bournaud C, Dazenière J, Thorpe P, Bailly-Bechet M, Pellegrin C, Péré A, Grynberg P, Perfus-Barbeoch L, Eves-van den Akker S, and Danchin EGJ
- Subjects
- Animals, Life Cycle Stages genetics, Secernentea Infections parasitology, Transcription, Genetic genetics, Transcriptome genetics, Gene Expression genetics, Plant Diseases parasitology, Plant Roots parasitology, Promoter Regions, Genetic genetics, Tylenchoidea genetics
- Abstract
Root-knot nematodes (genus Meloidogyne ) are the major contributor to crop losses caused by nematodes. These nematodes secrete effector proteins into the plant, derived from two sets of pharyngeal gland cells, to manipulate host physiology and immunity. Successful completion of the life cycle, involving successive molts from egg to adult, covers morphologically and functionally distinct stages and will require precise control of gene expression, including effector genes. The details of how root-knot nematodes regulate transcription remain sparse. Here, we report a life stage-specific transcriptome of Meloidogyne incognita . Combined with an available annotated genome, we explore the spatio-temporal regulation of gene expression. We reveal gene expression clusters and predicted functions that accompany the major developmental transitions. Focusing on effectors, we identify a putative cis-regulatory motif associated with expression in the dorsal glands, providing an insight into effector regulation. We combine the presence of this motif with several other criteria to predict a novel set of putative dorsal gland effectors. Finally, we show this motif, and thereby its utility, is broadly conserved across the Meloidogyne genus, and we name it Mel-DOG. Taken together, we provide the first genome-wide analysis of spatio-temporal gene expression in a root-knot nematode and identify a new set of candidate effector genes that will guide future functional analyses.
- Published
- 2021
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29. Toward genetic modification of plant-parasitic nematodes: delivery of macromolecules to adults and expression of exogenous mRNA in second stage juveniles.
- Author
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Kranse O, Beasley H, Adams S, Pires-daSilva A, Bell C, Lilley CJ, Urwin PE, Bird D, Miska E, Smant G, Gheysen G, Jones J, Viney M, Abad P, Maier TR, Baum TJ, Siddique S, Williamson V, Akay A, and Eves-van den Akker S
- Subjects
- Animals, Male, Plant Diseases, RNA Interference, RNA, Messenger, Arabidopsis genetics, Tylenchoidea genetics
- Abstract
Plant-parasitic nematodes are a continuing threat to food security, causing an estimated 100 billion USD in crop losses each year. The most problematic are the obligate sedentary endoparasites (primarily root knot nematodes and cyst nematodes). Progress in understanding their biology is held back by a lack of tools for functional genetics: forward genetics is largely restricted to studies of natural variation in populations and reverse genetics is entirely reliant on RNA interference. There is an expectation that the development of functional genetic tools would accelerate the progress of research on plant-parasitic nematodes, and hence the development of novel control solutions. Here, we develop some of the foundational biology required to deliver a functional genetic tool kit in plant-parasitic nematodes. We characterize the gonads of male Heterodera schachtii and Meloidogyne hapla in the context of spermatogenesis. We test and optimize various methods for the delivery, expression, and/or detection of exogenous nucleic acids in plant-parasitic nematodes. We demonstrate that delivery of macromolecules to cyst and root knot nematode male germlines is difficult, but possible. Similarly, we demonstrate the delivery of oligonucleotides to root knot nematode gametes. Finally, we develop a transient expression system in plant-parasitic nematodes by demonstrating the delivery and expression of exogenous mRNA encoding various reporter genes throughout the body of H. schachtii juveniles using lipofectamine-based transfection. We anticipate these developments to be independently useful, will expedite the development of genetic modification tools for plant-parasitic nematodes, and ultimately catalyze research on a group of nematodes that threaten global food security., (© The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America.)
- Published
- 2021
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30. A new esophageal gland transcriptome reveals signatures of large scale de novo effector birth in the root lesion nematode Pratylenchus penetrans.
- Author
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Vieira P, Shao J, Vijayapalani P, Maier TR, Pellegrin C, Eves-van den Akker S, Baum TJ, and Nemchinov LG
- Subjects
- Animals, Helminth Proteins genetics, Phylogeny, Plant Diseases, Transcriptome, Tylenchoidea genetics
- Abstract
Background: The root lesion nematode Pratylenchus penetrans is a migratory plant-parasitic nematode responsible for economically important losses in a wide number of crops. Despite the importance of P. penetrans, the molecular mechanisms employed by this nematode to promote virulence remain largely unknown., Results: Here we generated a new and comprehensive esophageal glands-specific transcriptome library for P. penetrans. In-depth analysis of this transcriptome enabled a robust identification of a catalogue of 30 new candidate effector genes, which were experimentally validated in the esophageal glands by in situ hybridization. We further validated the expression of a multifaceted network of candidate effectors during the interaction with different plants. To advance our understanding of the "effectorome" of P. penetrans, we adopted a phylogenetic approach and compared the expanded effector repertoire of P. penetrans to the genome/transcriptome of other nematode species with similar or contrasting parasitism strategies. Our data allowed us to infer plausible evolutionary histories that shaped the effector repertoire of P. penetrans, as well as other close and distant plant-parasitic nematodes. Two remarkable trends were apparent: 1) large scale effector birth in the Pratylenchidae in general and P. penetrans in particular, and 2) large scale effector death in sedentary (endo) plant-parasitic nematodes., Conclusions: Our study doubles the number of validated Pratylenchus penetrans effectors reported in the literature. The dramatic effector gene gain in P. penetrans could be related to the remarkable ability of this nematode to parasitize a large number of plants. Our data provide valuable insights into nematode parasitism and contribute towards basic understating of the adaptation of P. penetrans and other root lesion nematodes to specific host plants.
- Published
- 2020
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31. Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari.
- Author
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Pokhare SS, Thorpe P, Hedley P, Morris J, Habash SS, Elashry A, Eves-van den Akker S, Grundler FMW, and Jones JT
- Subjects
- Animals, Helminth Proteins genetics, Helminth Proteins metabolism, Host-Parasite Interactions, Peptide Hormones genetics, Peptide Hormones metabolism, Transcriptome genetics, Tylenchoidea genetics, Plant Diseases parasitology, Tylenchoidea metabolism, Tylenchoidea pathogenicity
- Abstract
Interactions between plant-parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari, a cyst nematode parasite of rice (Oryza sativa) and sugarcane (Saccharum officinarum). A multi-gene phylogenetic analysis showed that H. sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot-parasitic ancestor. We compared the effector repertoires of H. sacchari with those of the dicot parasites Heterodera glycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non-effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non-effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H. sacchari effectors are adapted to monocots. This is exemplified by the plant-peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION-like (CLE) effectors. Peptide hormones encoded by H. sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant-parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H. sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co-occurred with the transition from a dicot-parasitic to a monocot-parasitic lifestyle., (© 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.)
- Published
- 2020
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32. Transcriptional changes in the aphid species Myzus cerasi under different host and environmental conditions.
- Author
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Thorpe P, Escudero-Martinez CM, Eves-van den Akker S, and Bos JIB
- Subjects
- Animals, Aphids genetics, Gene Expression Profiling, Adaptation, Biological, Aphids physiology, Environment, Food Chain, Transcriptome
- Abstract
Aphids feature complex life cycles, which in the case of many agriculturally important species involve primary and secondary host plant species. Whilst host alternation between primary and secondary host can occur in the field depending on host availability and the environment, aphid populations maintained as laboratory stocks generally are kept under conditions that allow asexual reproduction by parthenogenesis on secondary hosts. We used Myzus cerasi (black cherry aphid) to assess aphid transcriptional differences between populations collected from primary hosts in the field and those adapted to secondary hosts under controlled environment conditions. Transfer of M. cerasi collected from local cherry trees to reported secondary host species resulted in low survival rates. Moreover, aphids were unable to survive on the secondary host land cress, unless first adapted to another secondary host, cleavers. Transcriptome analyses of the different aphid populations (field collected and adapted) revealed extensive transcriptional plasticity to a change in environment, with predominantly genes involved in redox reactions differentially regulated. Most of the differentially expressed genes were duplicated and we found evidence for differential exon usage. Our data suggest that aphid adaptation to different environments may pose a major hurdle and leads to extensive gene expression changes., (© 2019 The Authors. Insect Molecular Biology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society.)
- Published
- 2020
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33. Duplication of hsp-110 Is Implicated in Differential Success of Globodera Species under Climate Change.
- Author
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Jones LM, Eves-van den Akker S, van-Oosten Hawle P, Atkinson HJ, and Urwin PE
- Subjects
- Animals, Female, HSP110 Heat-Shock Proteins metabolism, Hot Temperature, Rhabditida metabolism, Species Specificity, Climate Change, Gene Duplication, HSP110 Heat-Shock Proteins genetics, Heat-Shock Response, Rhabditida genetics
- Abstract
Managing the emergence and spread of crop pests and pathogens is essential for global food security. Understanding how organisms have adapted to their native climate is key to predicting the impact of climate change. The potato cyst nematodes Globodera pallida and G. rostochiensis are economically important plant pathogens that cause yield losses of up to 50% in potato. The two species have different thermal optima that may relate to differences in the altitude of their regions of origin in the Andes. Here, we demonstrate that juveniles of G. pallida are less able to recover from heat stress than those of G. rostochiensis. Genome-wide analysis revealed that while both Globodera species respond to heat stress by induction of various protective heat-inducible genes, G. pallida experiences heat stress at lower temperatures. We use C. elegans as a model to demonstrate the dependence of the heat stress response on expression of Heat Shock Factor-1 (HSF-1). Moreover, we show that hsp-110 is induced by heat stress in G. rostochiensis, but not in the less thermotolerant G. pallida. Sequence analysis revealed that this gene and its promoter was duplicated in G. rostochiensis and acquired thermoregulatory properties. We show that hsp-110 is required for recovery from acute thermal stress in both C. elegans and in G. rostochiensis. Our findings point towards an underlying molecular mechanism that allows the differential expansion of one species relative to another closely related species under current climate change scenarios. Similar mechanisms may be true of other invertebrate species with pest status.
- Published
- 2018
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34. Shared Transcriptional Control and Disparate Gain and Loss of Aphid Parasitism Genes.
- Author
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Thorpe P, Escudero-Martinez CM, Cock PJA, Eves-van den Akker S, and Bos JIB
- Subjects
- Animals, Biological Evolution, Gene Duplication, Gene Transfer, Horizontal, Aphids genetics, Gene Expression Regulation, Genome, Insect, Herbivory genetics
- Abstract
Aphids are a diverse group of taxa that contain agronomically important species, which vary in their host range and ability to infest crop plants. The genome evolution underlying agriculturally important aphid traits is not well understood. We generated draft genome assemblies for two aphid species: Myzus cerasi (black cherry aphid) and the cereal specialist Rhopalosiphum padi. Using a de novo gene prediction pipeline on both these, and three additional aphid genome assemblies (Acyrthosiphon pisum, Diuraphis noxia, and Myzus persicae), we show that aphid genomes consistently encode similar gene numbers. We compare gene content, gene duplication, synteny, and putative effector repertoires between these five species to understand the genome evolution of globally important plant parasites. Aphid genomes show signs of relatively distant gene duplication, and substantial, relatively recent, gene birth. Putative effector repertoires, originating from duplicated and other loci, have an unusual genomic organization and evolutionary history. We identify a highly conserved effector pair that is tightly physically linked in the genomes of all aphid species tested. In R. padi, this effector pair is tightly transcriptionally linked and shares an unknown transcriptional control mechanism with a subset of ∼50 other putative effectors and secretory proteins. This study extends our current knowledge on the evolution of aphid genomes and reveals evidence for an as-of-yet unknown shared control mechanism, which underlies effector expression, and ultimately plant parasitism.
- Published
- 2018
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35. STATAWAARS: a promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilus.
- Author
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Espada M, Eves-van den Akker S, Maier T, Vijayapalani P, Baum T, Mota M, and Jones JT
- Subjects
- Animals, Nucleotide Motifs, Pharynx metabolism, Transcriptome, Tylenchida metabolism, Promoter Regions, Genetic, Tylenchida genetics
- Abstract
Background: Plant-parasitic nematodes cause severe damage to a wide range of crop and forest species worldwide. The migratory endoparasitic nematode, Bursaphelenchus xylophilus, (pinewood nematode) is a quarantine pathogen that infects pine trees and has a hugely detrimental economic impact on the forestry industry. Under certain environmental conditions large areas of infected trees can be destroyed, leading to damage on an ecological scale. The interactions of B. xylophilus with plants are mediated by secreted effector proteins produced in the pharyngeal gland cells. Identification of effectors is important to understand mechanisms of parasitism and to develop new control measures for the pathogens., Results: Using an approach pioneered in cyst nematodes, we have analysed the promoter regions of a small panel of previously validated pharyngeal gland cell effectors from B. xylophilus to identify an associated putative regulatory promoter motif: STATAWAARS. The presence of STATAWAARS in the promoter region of an uncharacterized gene is a predictor that the corresponding gene encodes a putatively secreted protein, consistent with effector function. Furthermore, we are able to experimentally validate that a subset of STATAWAARS-containing genes are specifically expressed in the pharyngeal glands. Finally, we independently validate the association of STATAWAARS with tissue-specific expression by directly sequencing the mRNA of pharyngeal gland cells. We combine a series of criteria, including STATAWAARS predictions and abundance in the gland cell transcriptome, to generate a comprehensive effector repertoire for B. xylophilus. The genes highlighted by this approach include many previously described effectors and a series of novel "pioneer" effectors., Conclusions: We provide a major scientific advance in the area of effector regulation. We identify a novel promoter motif (STATAWAARS) associated with expression in the pharyngeal gland cells. Our data, coupled with those from previous studies, suggest that lineage-specific promoter motifs are a theme of effector regulation in the phylum Nematoda.
- Published
- 2018
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36. Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene.
- Author
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Lilley CJ, Maqbool A, Wu D, Yusup HB, Jones LM, Birch PRJ, Banfield MJ, Urwin PE, and Eves-van den Akker S
- Subjects
- Animals, Gene Expression Regulation, Enzymologic, Host-Parasite Interactions, Crops, Agricultural parasitology, Genes, Essential, Genes, Helminth, Glutathione Synthase genetics, Tylenchida genetics
- Abstract
Plant pathogens and parasites are a major threat to global food security. Plant parasitism has arisen four times independently within the phylum Nematoda, resulting in at least one parasite of every major food crop in the world. Some species within the most economically important order (Tylenchida) secrete proteins termed effectors into their host during infection to re-programme host development and immunity. The precise detail of how nematodes evolve new effectors is not clear. Here we reconstruct the evolutionary history of a novel effector gene family. We show that during the evolution of plant parasitism in the Tylenchida, the housekeeping glutathione synthetase (GS) gene was extensively replicated. New GS paralogues acquired multiple dorsal gland promoter elements, altered spatial expression to the secretory dorsal gland, altered temporal expression to primarily parasitic stages, and gained a signal peptide for secretion. The gene products are delivered into the host plant cell during infection, giving rise to "GS-like effectors". Remarkably, by solving the structure of GS-like effectors we show that during this process they have also diversified in biochemical activity, and likely represent the founding members of a novel class of GS-like enzyme. Our results demonstrate the re-purposing of an endogenous housekeeping gene to form a family of effectors with modified functions. We anticipate that our discovery will be a blueprint to understand the evolution of other plant-parasitic nematode effectors, and the foundation to uncover a novel enzymatic function.
- Published
- 2018
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37. Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background.
- Author
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Mróz TL, Eves-van den Akker S, Bernat A, Skarzyńska A, Pryszcz L, Olberg M, Havey MJ, and Bartoszewski G
- Subjects
- Cell Nucleus genetics, Cell Nucleus metabolism, Computational Biology methods, Cucumis sativus metabolism, Gene Expression Profiling, Gene Library, Genome, Mitochondrial, High-Throughput Nucleotide Sequencing, Mitochondria genetics, Mitochondria metabolism, Molecular Sequence Annotation, Phenotype, Signal Transduction, Cucumis sativus genetics, DNA, Mitochondrial, Gene Expression Regulation, Plant, Inbreeding, Mosaicism, Mutation, Transcriptome
- Abstract
Cucumber ( Cucumis sativus L.) has a large, paternally transmitted mitochondrial genome. Cucumber plants regenerated from cell cultures occasionally show paternally transmitted mosaic (MSC) phenotypes, characterized by slower growth, chlorotic patterns on the leaves and fruit, lower fertility, and rearrangements in their mitochondrial DNAs (mtDNAs). MSC lines 3, 12, and 16 originated from different cell cultures all established using the highly inbred, wild-type line B. These MSC lines possess different rearrangements and under-represented regions in their mtDNAs. We completed RNA-seq on normalized and non-normalized cDNA libraries from MSC3, MSC12, and MSC16 to study their nuclear gene-expression profiles relative to inbred B. Results from both libraries indicated that gene expression in MSC12 and MSC16 were more similar to each other than MSC3. Forty-one differentially expressed genes (DEGs) were upregulated and one downregulated in the MSC lines relative to B. Gene functional classifications revealed that more than half of these DEGs are associated with stress-response pathways. Consistent with this observation, we detected elevated levels of hydrogen peroxide throughout leaf tissue in all MSC lines compared to wild-type line B. These results demonstrate that independently produced MSC lines with different mitochondrial polymorphisms show unique and shared nuclear responses. This study revealed genes associated with stress response that could become selection targets to develop cucumber cultivars with increased stress tolerance, and further support of cucumber as a model plant to study nuclear-mitochondrial interactions., (Copyright © 2018 Mroz et al.)
- Published
- 2018
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38. Sex: Not all that it's cracked up to be?
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Eves-van den Akker S and Jones JT
- Published
- 2018
- Full Text
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39. Identification of candidate effector genes of Pratylenchus penetrans.
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Vieira P, Maier TR, Eves-van den Akker S, Howe DK, Zasada I, Baum TJ, Eisenback JD, and Kamo K
- Abstract
Pratylenchus penetrans is one of the most important species of root lesion nematodes (RLNs) because of its detrimental and economic impact in a wide range of crops. Similar to other plant-parasitic nematodes (PPNs), P. penetrans harbours a significant number of secreted proteins that play key roles during parasitism. Here, we combined spatially and temporally resolved next-generation sequencing datasets of P. penetrans to select a list of candidate genes aimed at the identification of a panel of effector genes for this species. We determined the spatial expression of transcripts of 22 candidate effectors within the oesophageal glands of P. penetrans by in situ hybridization. These comprised homologues of known effectors of other PPNs with diverse putative functions, as well as novel pioneer effectors specific to RLNs. It is noteworthy that five of the pioneer effectors encode extremely proline-rich proteins. We then combined in situ localization of effectors with available genomic data to identify a non-coding motif enriched in promoter regions of a subset of P. penetrans effectors, and thus a putative hallmark of spatial expression. Expression profiling analyses of a subset of candidate effectors confirmed their expression during plant infection. Our current results provide the most comprehensive panel of effectors found for RLNs. Considering the damage caused by P. penetrans, this information provides valuable data to elucidate the mode of parasitism of this nematode and offers useful suggestions regarding the potential use of P. penetrans-specific target effector genes to control this important pathogen., (© 2018 BSPP AND JOHN WILEY & SONS LTD.)
- Published
- 2018
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40. Genome Evolution of Plant-Parasitic Nematodes.
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Kikuchi T, Eves-van den Akker S, and Jones JT
- Subjects
- Animals, Gene Transfer, Horizontal, Multigene Family, Evolution, Molecular, Genome, Helminth, Nematoda genetics, Plant Diseases parasitology, Plants parasitology
- Abstract
Plant parasitism has evolved independently on at least four separate occasions in the phylum Nematoda. The application of next-generation sequencing (NGS) to plant-parasitic nematodes has allowed a wide range of genome- or transcriptome-level comparisons, and these have identified genome adaptations that enable parasitism of plants. Current genome data suggest that horizontal gene transfer, gene family expansions, evolution of new genes that mediate interactions with the host, and parasitism-specific gene regulation are important adaptations that allow nematodes to parasitize plants. Sequencing of a larger number of nematode genomes, including plant parasites that show different modes of parasitism or that have evolved in currently unsampled clades, and using free-living taxa as comparators would allow more detailed analysis and a better understanding of the organization of key genes within the genomes. This would facilitate a more complete understanding of the way in which parasitism has shaped the genomes of plant-parasitic nematodes.
- Published
- 2017
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41. Foundational and Translational Research Opportunities to Improve Plant Health.
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Michelmore R, Coaker G, Bart R, Beattie G, Bent A, Bruce T, Cameron D, Dangl J, Dinesh-Kumar S, Edwards R, Eves-van den Akker S, Gassmann W, Greenberg JT, Hanley-Bowdoin L, Harrison RJ, Harvey J, He P, Huffaker A, Hulbert S, Innes R, Jones JDG, Kaloshian I, Kamoun S, Katagiri F, Leach J, Ma W, McDowell J, Medford J, Meyers B, Nelson R, Oliver R, Qi Y, Saunders D, Shaw M, Smart C, Subudhi P, Torrance L, Tyler B, Valent B, and Walsh J
- Subjects
- Biotechnology methods, Climate Change, Crops, Agricultural microbiology, Crops, Agricultural parasitology, Humans, Plant Diseases microbiology, Plant Diseases parasitology, Agriculture methods, Crops, Agricultural growth & development, Food Supply, Translational Research, Biomedical methods
- Abstract
Reader Comments | Submit a Comment The white paper reports the deliberations of a workshop focused on biotic challenges to plant health held in Washington, D.C. in September 2016. Ensuring health of food plants is critical to maintaining the quality and productivity of crops and for sustenance of the rapidly growing human population. There is a close linkage between food security and societal stability; however, global food security is threatened by the vulnerability of our agricultural systems to numerous pests, pathogens, weeds, and environmental stresses. These threats are aggravated by climate change, the globalization of agriculture, and an over-reliance on nonsustainable inputs. New analytical and computational technologies are providing unprecedented resolution at a variety of molecular, cellular, organismal, and population scales for crop plants as well as pathogens, pests, beneficial microbes, and weeds. It is now possible to both characterize useful or deleterious variation as well as precisely manipulate it. Data-driven, informed decisions based on knowledge of the variation of biotic challenges and of natural and synthetic variation in crop plants will enable deployment of durable interventions throughout the world. These should be integral, dynamic components of agricultural strategies for sustainable agriculture.
- Published
- 2017
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42. Draft Transcriptome of Globodera ellingtonae .
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Phillips WS, Eves-van den Akker S, and Zasada IA
- Abstract
Globodera ellingtonae is a newly described cyst nematode found in Idaho, Oregon, and Argentina. Here we present the first transcriptome assembly of G. ellingtonae , providing a valuable resource for comparing the evolution of expressed genes between potato cyst nematode species.
- Published
- 2017
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43. The Draft Genome of Globodera ellingtonae .
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Phillips WS, Howe DK, Brown AMV, Eves-van den Akker S, Dettwyler L, Peetz AB, Denver DR, and Zasada IA
- Abstract
Globodera ellingtonae is a newly described potato cyst nematode (PCN) found in Idaho, Oregon, and Argentina. Here, we present a genome assembly for G. ellingtonae , a relative of the quarantine nematodes G. pallida and G. rostochiensis , produced using data from Illumina and Pacific Biosciences DNA sequencing technologies.
- Published
- 2017
- Full Text
- View/download PDF
44. Opening the Effector Protein Toolbox for Plant-Parasitic Cyst Nematode Interactions.
- Author
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Eves-van den Akker S and Birch PR
- Subjects
- Animals, Host-Parasite Interactions, Nematoda physiology, Plant Proteins metabolism, Plants metabolism, Plants parasitology
- Published
- 2016
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45. Functional C-TERMINALLY ENCODED PEPTIDE (CEP) plant hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis.
- Author
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Eves-Van Den Akker S, Lilley CJ, Yusup HB, Jones JT, and Urwin PE
- Subjects
- Amino Acid Sequence, Amino Acids metabolism, Animals, Arabidopsis parasitology, Genes, Helminth, Host-Parasite Interactions, Multigene Family, Parasites genetics, Peptides metabolism, Pharynx cytology, Phylogeny, Protein Domains, Sequence Alignment, Tylenchoidea genetics, Parasites metabolism, Peptides chemistry, Plant Growth Regulators chemistry, Tylenchoidea metabolism
- Abstract
Sedentary plant-parasitic nematodes (PPNs) induce and maintain an intimate relationship with their host, stimulating cells adjacent to root vascular tissue to re-differentiate into unique and metabolically active 'feeding sites'. The interaction between PPNs and their host is mediated by nematode effectors. We describe the discovery of a large and diverse family of effector genes, encoding C-TERMINALLY ENCODED PEPTIDE (CEP) plant hormone mimics (RrCEPs), in the syncytia-forming plant parasite Rotylenchulus reniformis. The particular attributes of RrCEPs distinguish them from all other CEPs, regardless of origin. Together with the distant phylogenetic relationship of R. reniformis to the only other CEP-encoding nematode genus identified to date (Meloidogyne), this suggests that CEPs probably evolved de novo in R. reniformis. We have characterized the first member of this large gene family (RrCEP1), demonstrating its significant up-regulation during the plant-nematode interaction and expression in the effector-producing pharyngeal gland cell. All internal CEP domains of multi-domain RrCEPs are followed by di-basic residues, suggesting a mechanism for cleavage. A synthetic peptide corresponding to RrCEP1 domain 1 is biologically active and capable of up-regulating plant nitrate transporter (AtNRT2.1) expression, whilst simultaneously reducing primary root elongation. When a non-CEP-containing, syncytia-forming PPN species (Heterodera schachtii) infects Arabidopsis in a CEP-rich environment, a smaller feeding site is produced. We hypothesize that CEPs of R. reniformis represent a two-fold adaptation to sustained biotrophy in this species: (i) increasing host nitrate uptake, whilst (ii) limiting the size of the syncytial feeding site produced., (© 2016 The Authors. Molecular Plant Pathology Published by British Society for Plant Pathology and John Wiley & Sons Ltd.)
- Published
- 2016
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46. A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity.
- Author
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Noon JB, Qi M, Sill DN, Muppirala U, Eves-van den Akker S, Maier TR, Dobbs D, Mitchum MG, Hewezi T, and Baum TJ
- Subjects
- Amino Acid Sequence, Animals, Genetic Complementation Test, Mutation genetics, Plant Proteins chemistry, Plant Roots parasitology, Polymorphism, Genetic, Protein Domains, RNA Interference, Repetitive Sequences, Nucleic Acid genetics, Tylenchoidea pathogenicity, Virulence, Immunity, Innate, Plant Immunity, Plasmodium physiology, Glycine max immunology, Glycine max parasitology, Tylenchoidea physiology, Virulence Factors metabolism
- Abstract
Heterodera glycines, the soybean cyst nematode, delivers effector proteins into soybean roots to initiate and maintain an obligate parasitic relationship. HgGLAND18 encodes a candidate H. glycines effector and is expressed throughout the infection process. We used a combination of molecular, genetic, bioinformatic and phylogenetic analyses to determine the role of HgGLAND18 during H. glycines infection. HgGLAND18 is necessary for pathogenicity in compatible interactions with soybean. The encoded effector strongly suppresses both basal and hypersensitive cell death innate immune responses, and immunosuppression requires the presence and coordination between multiple protein domains. The N-terminal domain in HgGLAND18 contains unique sequence similarity to domains of an immunosuppressive effector of Plasmodium spp., the malaria parasites. The Plasmodium effector domains functionally complement the loss of the N-terminal domain from HgGLAND18. In-depth sequence searches and phylogenetic analyses demonstrate convergent evolution between effectors from divergent parasites of plants and animals as the cause of sequence and functional similarity., (© 2016 The Authors. New Phytologist © 2016 New Phytologist Trust.)
- Published
- 2016
- Full Text
- View/download PDF
47. The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence.
- Author
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Eves-van den Akker S, Laetsch DR, Thorpe P, Lilley CJ, Danchin EG, Da Rocha M, Rancurel C, Holroyd NE, Cotton JA, Szitenberg A, Grenier E, Montarry J, Mimee B, Duceppe MO, Boyes I, Marvin JM, Jones LM, Yusup HB, Lafond-Lapalme J, Esquibet M, Sabeh M, Rott M, Overmars H, Finkers-Tomczak A, Smant G, Koutsovoulos G, Blok V, Mantelin S, Cock PJ, Phillips W, Henrissat B, Urwin PE, Blaxter M, and Jones JT
- Subjects
- Animals, Enhancer Elements, Genetic, Gene Expression Profiling, Gene Transfer, Horizontal, Genomic Islands, Genomics methods, High-Throughput Nucleotide Sequencing, Life Cycle Stages, Nucleotide Motifs, Position-Specific Scoring Matrices, RNA Splice Sites, RNA Splicing, Transcriptome, Tylenchoidea growth & development, Virulence genetics, Genome, Protozoan, Plant Diseases parasitology, Solanum tuberosum parasitology, Tylenchoidea genetics, Tylenchoidea pathogenicity
- Abstract
Background: The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes., Results: We generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative 'effector islands' in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking., Conclusions: These G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action.
- Published
- 2016
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48. Identification and characterization of parasitism genes from the pinewood nematode Bursaphelenchus xylophilus reveals a multilayered detoxification strategy.
- Author
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Espada M, Silva AC, Eves van den Akker S, Cock PJ, Mota M, and Jones JT
- Subjects
- Animals, Computational Biology, Gene Expression Regulation, Genetic Association Studies, Helminth Proteins metabolism, Pharynx cytology, Reproducibility of Results, Genes, Helminth, Inactivation, Metabolic genetics, Parasites genetics, Pinus parasitology, Tylenchida genetics
- Abstract
The migratory endoparasitic nematode Bursaphelenchus xylophilus, which is the causal agent of pine wilt disease, has phytophagous and mycetophagous phases during its life cycle. This highly unusual feature distinguishes it from other plant-parasitic nematodes and requires profound changes in biology between modes. During the phytophagous stage, the nematode migrates within pine trees, feeding on the contents of parenchymal cells. Like other plant pathogens, B. xylophilus secretes effectors from pharyngeal gland cells into the host during infection. We provide the first description of changes in the morphology of these gland cells between juvenile and adult life stages. Using a comparative transcriptomics approach and an effector identification pipeline, we identify numerous novel parasitism genes which may be important for the mediation of interactions of B. xylophilus with its host. In-depth characterization of all parasitism genes using in situ hybridization reveals two major categories of detoxification proteins, those specifically expressed in either the pharyngeal gland cells or the digestive system. These data suggest that B. xylophilus incorporates effectors in a multilayer detoxification strategy in order to protect itself from host defence responses during phytophagy., (© 2015 BSPP AND JOHN WILEY & SONS LTD.)
- Published
- 2016
- Full Text
- View/download PDF
49. The Pratylenchus penetrans Transcriptome as a Source for the Development of Alternative Control Strategies: Mining for Putative Genes Involved in Parasitism and Evaluation of in planta RNAi.
- Author
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Vieira P, Eves-van den Akker S, Verma R, Wantoch S, Eisenback JD, and Kamo K
- Subjects
- Animals, Gene Expression Regulation, Gene Silencing, Helminth Proteins chemistry, Helminth Proteins genetics, High-Throughput Nucleotide Sequencing, Host-Parasite Interactions, Molecular Sequence Annotation, Plant Roots parasitology, RNA, Helminth antagonists & inhibitors, RNA, Messenger antagonists & inhibitors, RNA, Small Interfering genetics, Sequence Homology, Nucleic Acid, Tylenchoidea pathogenicity, Plant Diseases parasitology, RNA, Helminth genetics, RNA, Messenger genetics, Glycine max parasitology, Transcriptome, Tylenchoidea genetics
- Abstract
The root lesion nematode Pratylenchus penetrans is considered one of the most economically important species within the genus. Host range studies have shown that nearly 400 plant species can be parasitized by this species. To obtain insight into the transcriptome of this migratory plant-parasitic nematode, we used Illumina mRNA sequencing analysis of a mixed population, as well as nematode reads detected in infected soybean roots 3 and 7 days after nematode infection. Over 140 million paired end reads were obtained for this species, and de novo assembly resulted in a total of 23,715 transcripts. Homology searches showed significant hit matches to 58% of the total number of transcripts using different protein and EST databases. In general, the transcriptome of P. penetrans follows common features reported for other root lesion nematode species. We also explored the efficacy of RNAi, delivered from the host, as a strategy to control P. penetrans, by targeted knock-down of selected nematode genes. Different comparisons were performed to identify putative nematode genes with a role in parasitism, resulting in the identification of transcripts with similarities to other nematode parasitism genes. Focusing on the predicted nematode secreted proteins found in this transcriptome, we observed specific members to be up-regulated at the early time points of infection. In the present study, we observed an enrichment of predicted secreted proteins along the early time points of parasitism by this species, with a significant number being pioneer candidate genes. A representative set of genes examined using RT-PCR confirms their expression during the host infection. The expression patterns of the different candidate genes raise the possibility that they might be involved in critical steps of P. penetrans parasitism. This analysis sheds light on the transcriptional changes that accompany plant infection by P. penetrans, and will aid in identifying potential gene targets for selection and use to design effective control strategies against root lesion nematodes.
- Published
- 2015
- Full Text
- View/download PDF
50. A metagenetic approach to determine the diversity and distribution of cyst nematodes at the level of the country, the field and the individual.
- Author
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Eves-van den Akker S, Lilley CJ, Reid A, Pickup J, Anderson E, Cock PJ, Blaxter M, Urwin PE, Jones JT, and Blok VC
- Subjects
- Animals, DNA Barcoding, Taxonomic, DNA, Helminth genetics, DNA, Mitochondrial genetics, Molecular Sequence Data, Plant Diseases parasitology, Scotland, Soil, Genetic Variation, Genetics, Population, Solanum tuberosum parasitology, Tylenchoidea genetics
- Abstract
Distinct populations of the potato cyst nematode (PCN) Globodera pallida exist in the UK that differ in their ability to overcome various sources of resistance. An efficient method for distinguishing between populations would enable pathogen-informed cultivar choice in the field. Science and Advice for Scottish Agriculture (SASA) annually undertake national DNA diagnostic tests to determine the presence of PCN in potato seed and ware land by extracting DNA from soil floats. These DNA samples provide a unique resource for monitoring the distribution of PCN and further interrogation of the diversity within species. We identify a region of mitochondrial DNA descriptive of three main groups of G. pallida present in the UK and adopt a metagenetic approach to the sequencing and analysis of all SASA samples simultaneously. Using this approach, we describe the distribution of G. pallida mitotypes across Scotland with field-scale resolution. Most fields contain a single mitotype, one-fifth contain a mix of mitotypes, and less than 3% contain all three mitotypes. Within mixed fields, we were able to quantify the relative abundance of each mitotype across an order of magnitude. Local areas within mixed fields are dominated by certain mitotypes and indicate towards a complex underlying 'pathoscape'. Finally, we assess mitotype distribution at the level of the individual cyst and provide evidence of 'hybrids'. This study provides a method for accurate, quantitative and high-throughput typing of up to one thousand fields simultaneously, while revealing novel insights into the national genetic variability of an economically important plant parasite., (© 2015 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd.)
- Published
- 2015
- Full Text
- View/download PDF
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