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1. Fast-track transformation and genome editing in Brachypodium distachyon

Author

Camille Soulhat, Houssein Wehbi, Yannick Fierlej, Patrick Berquin, Thomas Girin, Pierre Hilson, and Oumaya Bouchabké-Coussa

Subjects
Brachypodium distachyon, Genetic transformation, Genome editing, CRISPR/Cas9, Nitrate reductase (NR) mutants, Somatic embryogenesis, Plant culture, SB1-1110, Biology (General), QH301-705.5
Abstract

Abstract Background Even for easy-to-transform species or genotypes, the creation of transgenic or edited plant lines remains a significant bottleneck. Thus, any technical advance that accelerates the regeneration and transformation process is welcome. So far, methods to produce Brachypodium distachyon (Bd) transgenics span at least 14 weeks from the start of tissue culture to the recovery of regenerated plantlets. Results We have previously shown that embryogenic somatic tissues grow in the scutellum of immature zygotic Bd embryos within 3 days of in vitro induction with exogenous auxin and that the development of secondary embryos can be initiated immediately thereafter. Here, we further demonstrate that such pluripotent reactive tissues can be genetically transformed with Agrobacterium tumefaciens right after the onset of somatic embryogenesis. In brief, immature zygotic embryos are induced for callogenesis for one week, co-cultured with Agrobacterium for three days, then incubated on callogenesis selective medium for three weeks, and finally transferred on selective regeneration medium for up to three weeks to obtain plantlets ready for rooting. This 7-to-8-week procedure requires only three subcultures. Its validation includes the molecular and phenotype characterization of Bd lines carrying transgenic cassettes and novel CRISPR/Cas9-generated mutations in two independent loci coding for nitrate reductase enzymes (BdNR1 and BdNR2). Conclusions With a short callogenesis stage and streamlined in vitro regeneration following co-cultivation with Agrobacterium, transgenic and edited T0 Bd plantlets can be produced in about 8 weeks, a gain of one to two months compared to previously published methods, with no reduction in transformation efficiency and at lower costs.

Published
2023
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2. One-Week Scutellar Somatic Embryogenesis in the Monocot Brachypodium distachyon

Author

Houssein Wehbi, Camille Soulhat, Halima Morin, Abdelhafid Bendahmane, Pierre Hilson, and Oumaya Bouchabké-Coussa

Subjects
Brachypodium distachyon, development, monocot, regeneration, somatic embryogenesis, zygotic embryogenesis, Botany, QK1-989
Abstract

Plant somatic embryogenesis (SE) is a natural process of vegetative propagation. It can be induced in tissue cultures to investigate developmental transitions, to create transgenic or edited lines, or to multiply valuable crops. We studied the induction of SE in the scutellum of monocots with Brachypodium distachyon as a model system. Towards the in-depth analysis of SE initiation, we determined the earliest stages at which somatic scutellar cells acquired an embryogenic fate, then switched to a morphogenetic mode in a regeneration sequence involving treatments with exogenous hormones: first an auxin (2,4-D) then a cytokinin (kinetin). Our observations indicated that secondary somatic embryos could already develop in the proliferative calli derived from immature zygotic embryo tissues within one week from the start of in vitro culture. Cell states and tissue identity were deduced from detailed histological examination, and in situ hybridization was performed to map the expression of key developmental genes. The fast SE induction method we describe here facilitates the mechanistic study of the processes involved and may significantly shorten the production of transgenic or gene-edited plants.

Published
2022
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3. A Brachypodium UDP-Glycosyltransferase Confers Root Tolerance to Deoxynivalenol and Resistance to Fusarium Infection

Author

Vessela Atanasova-Pénichon, Marion Dalmais, Oumaya Bouchabke-Coussa, Edouard Boex-Fontvieille, Abdelhafid Bendahmane, Jean-Claude Pasquet, Marie Dufresne, Valentin Changenet, Catherine Macadre, Camille Soulhat, Patrick Saindrenan, Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Université Jean Monnet [Saint-Étienne] (UJM), Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Unité de recherche Mycologie et Sécurité des Aliments (MycSA), Institut National de la Recherche Agronomique (INRA), and Université Jean Monnet - Saint-Étienne (UJM)

Subjects
0106 biological sciences, 0301 basic medicine, Physiology, [SDV]Life Sciences [q-bio], Plant Science, medicine.disease_cause, Plant Roots, 01 natural sciences, chemistry.chemical_compound, Fusarium, Glucosides, Gene Expression Regulation, Plant, [SDV.IDA]Life Sciences [q-bio]/Food engineering, polycyclic compounds, Disease Resistance, Plant Proteins, 2. Zero hunger, Genetics, Mutation, biology, Reverse Transcriptase Polymerase Chain Reaction, food and beverages, Articles, Plants, Genetically Modified, Genetically modified organism, [SDE]Environmental Sciences, Host-Pathogen Interactions, Brachypodium, Brachypodium distachyon, Gene Expression Regulation, Enzymologic, Uridine Diphosphate, 03 medical and health sciences, Botany, medicine, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, [SPI.GPROC]Engineering Sciences [physics]/Chemical and Process Engineering, Amino Acid Sequence, Secondary metabolism, Mycotoxin, Gene, Plant Diseases, Base Sequence, Glycosyltransferases, biology.organism_classification, Kinetics, 030104 developmental biology, chemistry, Trichothecenes, 010606 plant biology & botany
Abstract

International audience; Fusarium head blight (FHB) is a cereal disease caused by Fusarium graminearum, a fungus able to produce type B trichothecenes on cereals, including deoxynivalenol (DON), which is harmful for humans and animals. Resistance to FHB is quantitative, and the mechanisms underlying resistance are poorly understood. Resistance has been related to the ability to conjugate DON into a glucosylated form, deoxynivalenol-3-O-glucose (D3G), by secondary metabolism UDP-glucosyltransferases (UGTs). However, functional analyses have never been performed within a single host species. Here, using the model cereal species Brachypodium distachyon, we show that the Bradi5g03300 UGT converts DON into D3G in planta. We present evidence that a mutation in Bradi5g03300 increases root sensitivity to DON and the susceptibility of spikes to F. graminearum, while overexpression confers increased root tolerance to the mycotoxin and spike resistance to the fungus. The dynamics of expression and conjugation suggest that the speed of DON conjugation rather than the increase of D3G per se is a critical factor explaining the higher resistance of the overexpressing lines. A detached glumes assay showed that overexpression but not mutation of the Bradi5g03300 gene alters primary infection by F. graminearum, highlighting the involvement of DON in early steps of infection. Together, these results indicate that early and efficient UGT-mediated conjugation of DON is necessary and sufficient to establish resistance to primary infection by F. graminearum and highlight a novel strategy to promote FHB resistance in cereals.

Published
2016

4. Expression atlas and comparative coexpression network analyses reveal important genes involved in the formation of lignified cell wall in Brachypodium distachyon

Author

Sebastian Proost, Staffan Persson, David Roujol, Philippe Le Bris, Laurent Cézart, Richard Sibout, Asher Pasha, Herman Höfte, Frédéric Legée, Federico M. Giorgi, Catherine Lapierre, Bjoern Oest Hansen, Neha Vaid, Oumaya Bouchabke-Coussa, Marek Mutwil, Camille Soulhat, Elisabeth Jamet, Séverine Ho-Yue-Kuang, Nicholas J. Provart, Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Université Paris-Saclay, Max Planck Institute of Molecular Plant Physiology (MPI-MP), Max-Planck-Gesellschaft, Centre for Cancer Genetic Epidemiology [Cambridge], Department of Oncology-University of Cambridge [UK] (CAM), University of Toronto, Laboratoire de Recherche en Sciences Végétales (LRSV), Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, University of Melbourne, University of Cambridge [UK] (CAM)-Department of Oncology, Dynamique et Evolution des Parois cellulaires végétales, Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Sibout, Richard, Proost, Sebastian, Hansen, Bjoern Oest, Vaid, Neha, Giorgi, Federico M., Ho-Yue-Kuang, Severine, Legée, Frédéric, Cézart, Laurent, Bouchabké-Coussa, Oumaya, Soulhat, Camille, Provart, Nichola, Pasha, Asher, Le Bris, Philippe, Roujol, David, Hofte, Herman, Jamet, Elisabeth, Lapierre, Catherine, Persson, Staffan, and Mutwil, Marek

Subjects
0106 biological sciences, 0301 basic medicine, Physiology, [SDV]Life Sciences [q-bio], Arabidopsis, Gene regulatory network, functional module, lignin, Plant Science, Computational biology, Genes, Plant, 01 natural sciences, Genome, Plant Stem, Transcriptome, 03 medical and health sciences, Cell Wall, Gene Expression Regulation, Plant, comparative coexpression, Databases, Genetic, Botany, Gene Regulatory Networks, Gene, 2. Zero hunger, Regulation of gene expression, Brachypodium distachyon, Gene Regulatory Network, Plant Stems, biology, coexpression, food and beverages, Oryza, 15. Life on land, Plants, Genetically Modified, biology.organism_classification, 030104 developmental biology, gene function, expression atla, Brachypodium, expression atlas, Arabidopsi, functional modules, 010606 plant biology & botany
Abstract

While Brachypodium distachyon (Brachypodium) is an emerging model for grasses, no expression atlas or gene coexpression network is available. Such tools are of high importance to provide insights into the function of Brachypodium genes. We present a detailed Brachypodium expression atlas, capturing gene expression in its major organs at different developmental stages. The data were integrated into a large-scale coexpression database ( www.gene2function.de), enabling identification of duplicated pathways and conserved processes across 10 plant species, thus allowing genome-wide inference of gene function. We highlight the importance of the atlas and the platform through the identification of duplicated cell wall modules, and show that a lignin biosynthesis module is conserved across angiosperms. We identified and functionally characterised a putative ferulate 5-hydroxylase gene through overexpression of it in Brachypodium, which resulted in an increase in lignin syringyl units and reduced lignin content of mature stems, and led to improved saccharification of the stem biomass. Our Brachypodium expression atlas thus provides a powerful resource to reveal functionally related genes, which may advance our understanding of important biological processes in grasses.

Published
2017

5. LACCASE5 Is Required for Lignification of the Brachypodium distachyon Culm

Author

Oumaya Bouchabke-Coussa, Camille Soulhat, Grégory Mouille, Catherine Lapierre, Halima Morin, Frédéric Legée, Sébastien Antelme, Yin Wang, Laurent Cézard, Marion Dalmais, Philippe Lebris, Emilie Gineau, Abdelafid Bendahmane, Richard Sibout, Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, unité mixte CNRS, Centre National de la Recherche Scientifique (CNRS), Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Université d'Évry-Val-d'Essonne (UEVE)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut National de la Recherche Agronomique program Amelioration de la Ligno-Cellulose, European Commission’s Seventh Framework Programme project RENEWALL (grant no. 211982), the Knowledge-Based Bio Economy project CELLWALL, and BRAVO (grant no. ANR–14–CE19–0012–01), China Scholarship Council, ANR-14-CE19-0012,BRAVO,Ontogénie des tissus vasculaires chez les graminées(2014), Unité de recherche en génomique végétale (URGV), Institut National de la Recherche Agronomique (INRA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Université d'Évry-Val-d'Essonne (UEVE), and Université d'Évry-Val-d'Essonne (UEVE)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
2. Zero hunger, Laccase, Messenger RNA, biology, Physiology, [SDV]Life Sciences [q-bio], Mutant, food and beverages, Plant Science, biology.organism_classification, Ferulic acid, chemistry.chemical_compound, Hydrolysis, Biochemistry, chemistry, Botany, [SDV.IDA]Life Sciences [q-bio]/Food engineering, Genetics, biology.protein, Lignin, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, [SPI.GPROC]Engineering Sciences [physics]/Chemical and Process Engineering, Brachypodium distachyon, Peroxidase
Abstract

The oxidation of monolignols is a required step for lignin polymerization and deposition in cell walls. In dicots, both peroxidases and laccases are known to participate in this process. Here, we provide evidence that laccases are also involved in the lignification of Brachypodium distachyon, a model plant for temperate grasses. Transcript quantification data as well as in situ and immunolocalization experiments demonstrated that at least two laccases (LACCASE5 and LACCASE6) are present in lignifying tissues. A mutant with a misspliced LACCASE5 messenger RNA was identified in a targeting-induced local lesion in genome mutant collection. This mutant shows 10% decreased Klason lignin content and modification of the syringyl-to-guaiacyl units ratio. The amount of ferulic acid units ester linked to the mutant cell walls is increased by 40% when compared with control plants, while the amount of ferulic acid units ether linked to lignins is decreased. In addition, the mutant shows a higher saccharification efficiency. These results provide clear evidence that laccases are required for B. distachyon lignification and are promising targets to alleviate the recalcitrance of grass lignocelluloses.

Published
2015

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