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1. Phylogenomics and the rise of the angiosperms

Author

Zuntini, Alexandre R., Carruthers, Tom, Maurin, Olivier, Bailey, Paul C., Leempoel, Kevin, Brewer, Grace E., Epitawalage, Niroshini, Françoso, Elaine, Gallego-Paramo, Berta, McGinnie, Catherine, Negrão, Raquel, Roy, Shyamali R., Simpson, Lalita, Toledo Romero, Eduardo, Barber, Vanessa M. A., Botigué, Laura, Clarkson, James J., Cowan, Robyn S., Dodsworth, Steven, Johnson, Matthew G., Kim, Jan T., Pokorny, Lisa, Wickett, Norman J., Antar, Guilherme M., DeBolt, Lucinda, Gutierrez, Karime, Hendriks, Kasper P., Hoewener, Alina, Hu, Ai-Qun, Joyce, Elizabeth M., Kikuchi, Izai A. B. S., Larridon, Isabel, Larson, Drew A., de Lírio, Elton John, Liu, Jing-Xia, Malakasi, Panagiota, Przelomska, Natalia A. S., Shah, Toral, Viruel, Juan, Allnutt, Theodore R., Ameka, Gabriel K., Andrew, Rose L., Appelhans, Marc S., Arista, Montserrat, Ariza, María Jesús, Arroyo, Juan, Arthan, Watchara, Bachelier, Julien B., Bailey, C. Donovan, Barnes, Helen F., Barrett, Matthew D., Barrett, Russell L., Bayer, Randall J., Bayly, Michael J., Biffin, Ed, Biggs, Nicky, Birch, Joanne L., Bogarín, Diego, Borosova, Renata, Bowles, Alexander M. C., Boyce, Peter C., Bramley, Gemma L. C., Briggs, Marie, Broadhurst, Linda, Brown, Gillian K., Bruhl, Jeremy J., Bruneau, Anne, Buerki, Sven, Burns, Edie, Byrne, Margaret, Cable, Stuart, Calladine, Ainsley, Callmander, Martin W., Cano, Ángela, Cantrill, David J., Cardinal-McTeague, Warren M., Carlsen, Mónica M., Carruthers, Abigail J. A., de Castro Mateo, Alejandra, Chase, Mark W., Chatrou, Lars W., Cheek, Martin, Chen, Shilin, Christenhusz, Maarten J. M., Christin, Pascal-Antoine, Clements, Mark A., Coffey, Skye C., Conran, John G., Cornejo, Xavier, Couvreur, Thomas L. P., Cowie, Ian D., Csiba, Laszlo, Darbyshire, Iain, Davidse, Gerrit, Davies, Nina M. J., Davis, Aaron P., van Dijk, Kor-jent, Downie, Stephen R., Duretto, Marco F., Duvall, Melvin R., Edwards, Sara L., Eggli, Urs, Erkens, Roy H. J., Escudero, Marcial, de la Estrella, Manuel, Fabriani, Federico, Fay, Michael F., Ferreira, Paola de L., Ficinski, Sarah Z., Fowler, Rachael M., Frisby, Sue, Fu, Lin, Fulcher, Tim, Galbany-Casals, Mercè, Gardner, Elliot M., German, Dmitry A., Giaretta, Augusto, Gibernau, Marc, Gillespie, Lynn J., González, Cynthia C., Goyder, David J., Graham, Sean W., Grall, Aurélie, Green, Laura, Gunn, Bee F., Gutiérrez, Diego G., Hackel, Jan, Haevermans, Thomas, Haigh, Anna, Hall, Jocelyn C., Hall, Tony, Harrison, Melissa J., Hatt, Sebastian A., Hidalgo, Oriane, Hodkinson, Trevor R., Holmes, Gareth D., Hopkins, Helen C. F., Jackson, Christopher J., James, Shelley A., Jobson, Richard W., Kadereit, Gudrun, Kahandawala, Imalka M., Kainulainen, Kent, Kato, Masahiro, Kellogg, Elizabeth A., King, Graham J., Klejevskaja, Beata, Klitgaard, Bente B., Klopper, Ronell R., Knapp, Sandra, Koch, Marcus A., Leebens-Mack, James H., Lens, Frederic, Leon, Christine J., Léveillé-Bourret, Étienne, Lewis, Gwilym P., Li, De-Zhu, Li, Lan, Liede-Schumann, Sigrid, Livshultz, Tatyana, Lorence, David, Lu, Meng, Lu-Irving, Patricia, Luber, Jaquelini, Lucas, Eve J., Luján, Manuel, Lum, Mabel, Macfarlane, Terry D., Magdalena, Carlos, Mansano, Vidal F., Masters, Lizo E., Mayo, Simon J., McColl, Kristina, McDonnell, Angela J., McDougall, Andrew E., McLay, Todd G. B., McPherson, Hannah, Meneses, Rosa I., Merckx, Vincent S. F. T., Michelangeli, Fabián A., Mitchell, John D., Monro, Alexandre K., Moore, Michael J., Mueller, Taryn L., Mummenhoff, Klaus, Munzinger, Jérôme, Muriel, Priscilla, Murphy, Daniel J., Nargar, Katharina, Nauheimer, Lars, Nge, Francis J., Nyffeler, Reto, Orejuela, Andrés, Ortiz, Edgardo M., Palazzesi, Luis, Peixoto, Ariane Luna, Pell, Susan K., Pellicer, Jaume, Penneys, Darin S., Perez-Escobar, Oscar A., Persson, Claes, Pignal, Marc, Pillon, Yohan, Pirani, José R., Plunkett, Gregory M., Powell, Robyn F., Prance, Ghillean T., Puglisi, Carmen, Qin, Ming, Rabeler, Richard K., Rees, Paul E. J., Renner, Matthew, Roalson, Eric H., Rodda, Michele, Rogers, Zachary S., Rokni, Saba, Rutishauser, Rolf, de Salas, Miguel F., Schaefer, Hanno, Schley, Rowan J., Schmidt-Lebuhn, Alexander, Shapcott, Alison, Al-Shehbaz, Ihsan, Shepherd, Kelly A., Simmons, Mark P., Simões, André O., Simões, Ana Rita G., Siros, Michelle, Smidt, Eric C., Smith, James F., Snow, Neil, Soltis, Douglas E., Soltis, Pamela S., Soreng, Robert J., Sothers, Cynthia A., Starr, Julian R., Stevens, Peter F., Straub, Shannon C. K., Struwe, Lena, Taylor, Jennifer M., Telford, Ian R. H., Thornhill, Andrew H., Tooth, Ifeanna, Trias-Blasi, Anna, Udovicic, Frank, Utteridge, Timothy M. A., Del Valle, Jose C., Verboom, G. Anthony, Vonow, Helen P., Vorontsova, Maria S., de Vos, Jurriaan M., Al-Wattar, Noor, Waycott, Michelle, Welker, Cassiano A. D., White, Adam J., Wieringa, Jan J., Williamson, Luis T., Wilson, Trevor C., Wong, Sin Yeng, Woods, Lisa A., Woods, Roseina, Worboys, Stuart, Xanthos, Martin, Yang, Ya, Zhang, Yu-Xiao, Zhou, Meng-Yuan, Zmarzty, Sue, Zuloaga, Fernando O., Antonelli, Alexandre, Bellot, Sidonie, Crayn, Darren M., Grace, Olwen M., Kersey, Paul J., Leitch, Ilia J., Sauquet, Hervé, Smith, Stephen A., Eiserhardt, Wolf L., Forest, Félix, and Baker, William J.

Published
2024
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2. Identifying genomic regions associated with C4 photosynthetic activity and leaf anatomy in Alloteropsis semialata.

Author

Alenazi, Ahmed S., Pereira, Lara, Christin, Pascal‐Antoine, Osborne, Colin P., and Dunning, Luke T.

Subjects
LEAF anatomy, CARBON 4 photosynthesis, LEAF development, ANATOMY, MERISTEMS
Abstract

Summary: C4 photosynthesis is a complex trait requiring multiple developmental and metabolic alterations. Despite this complexity, it has independently evolved over 60 times. However, our understanding of the transition to C4 is complicated by the fact that variation in photosynthetic type is usually segregated between species that diverged a long time ago.Here, we perform a genome‐wide association study (GWAS) using the grass Alloteropsis semialata, the only known species to have C3, intermediate, and C4 accessions that recently diverged. We aimed to identify genomic regions associated with the strength of the C4 cycle (measured using δ13C), and the development of C4 leaf anatomy.Genomic regions correlated with δ13C include regulators of C4 decarboxylation enzymes (RIPK), nonphotochemical quenching (SOQ1), and the development of Kranz anatomy (SCARECROW‐LIKE). Regions associated with the development of C4 leaf anatomy in the intermediate individuals contain additional leaf anatomy regulators, including those responsible for vein patterning (GSL8) and meristem determinacy (GIF1).The parallel recruitment of paralogous leaf anatomy regulators between A. semialata and other C4 lineages implies the co‐option of these genes is context‐dependent, which likely has implications for the engineering of the C4 trait into C3 species. [ABSTRACT FROM AUTHOR]

Published
2024
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7. C4 photosynthesis provided an immediate demographic advantage to populations of the grass Alloteropsis semialata.

Author

Sotelo, Graciela, Gamboa, Sara, Dunning, Luke T., Christin, Pascal‐Antoine, and Varela, Sara

Subjects
CARBON 4 photosynthesis, PLANT evolution, PALEOCLIMATOLOGY
Abstract

Summary: C4 photosynthesis is a key innovation in land plant evolution, but its immediate effects on population demography are unclear. We explore the early impact of the C4 trait on the trajectories of C4 and non‐C4 populations of the grass Alloteropsis semialata.We combine niche models projected into paleoclimate layers for the last 5 million years with demographic models based on genomic data.The initial split between C4 and non‐C4 populations was followed by a larger expansion of the ancestral C4 population, and further diversification led to the unparalleled expansion of descendant C4 populations. Overall, C4 populations spread over three continents and achieved the highest population growth, in agreement with a broader climatic niche that rendered a large potential range over time. The C4 populations that remained in the region of origin, however, experienced lower population growth, rather consistent with local geographic constraints. Moreover, the posterior transfer of some C4‐related characters to non‐C4 counterparts might have facilitated the recent expansion of non‐C4 populations in the region of origin.Altogether, our findings support that C4 photosynthesis provided an immediate demographic advantage to A. semialata populations, but its effect might be masked by geographic contingencies. [ABSTRACT FROM AUTHOR]

Published
2024
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15. Lateral gene transfer generates accessory genes that accumulate at different rates within a grass lineage.

Author

Raimondeau, Pauline, Bianconi, Matheus E., Pereira, Lara, Parisod, Christian, Christin, Pascal‐Antoine, and Dunning, Luke T.

Subjects
HORIZONTAL gene transfer, PAN-genome, GENES, GRASSES
Abstract

Summary: Lateral gene transfer (LGT) is the movement of DNA between organisms without sexual reproduction. The acquired genes represent genetic novelties that have independently evolved in the donor's genome. Phylogenetic methods have shown that LGT is widespread across the entire grass family, although we know little about the underlying dynamics.We identify laterally acquired genes in five de novo reference genomes from the same grass genus (four Alloteropsis semialata and one Alloteropsis angusta). Using additional resequencing data for a further 40 Alloteropsis individuals, we place the acquisition of each gene onto a phylogeny using stochastic character mapping, and then infer rates of gains and losses.We detect 168 laterally acquired genes in the five reference genomes (32–100 per genome). Exponential decay models indicate that the rate of LGT acquisitions (6–28 per Ma) and subsequent losses (11–24% per Ma) varied significantly among lineages. Laterally acquired genes were lost at a higher rate than vertically inherited loci (0.02–0.8% per Ma).This high turnover creates intraspecific gene content variation, with a preponderance of them occurring as accessory genes in the Alloteropsis pangenome. This rapid turnover generates standing variation that can ultimately fuel local adaptation. [ABSTRACT FROM AUTHOR]

Published
2023
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17. The mechanisms underpinning lateral gene transfer between grasses.

Author

Pereira, Lara, Christin, Pascal‐Antoine, and Dunning, Luke T.

Subjects
*HORIZONTAL gene transfer, *PLANT genetic transformation, *GENETIC engineering, *POLLINATORS, *GRASSES, *POLLEN tube, *PROKARYOTES, *AGROBACTERIUM tumefaciens
Abstract

Societal Impact Statement: Lateral gene transfer (LGT) refers to the transmission of genetic material without sexual reproduction. LGT is widespread in a number of plant species, including grasses. But how these genes of foreign origin got there is presently unknown. In this review, we show that transformation techniques used to genetically modify organisms could occur in the wild and be responsible for the frequently observed grass‐to‐grass LGTs. The distinction between natural evolutionary processes and genetic engineering might be arbitrary, and its validity will be further debated as agricultural biotechnology becomes more widely used and examples of "natural genetic engineering" through LGT increase. Summary: Lateral gene transfer (LGT) is the transmission of genetic material among species without sexual reproduction. LGT was initially thought to be restricted to prokaryotes, but it has since been reported in a wide range of eukaryotes, including plants. Grasses seem to be particularly prone to LGT and frequently exchange genes among species. However, the mechanism(s) facilitating these transfers in this economically and ecologically important group of plants are debated. Here, we review vector‐mediated, direct tissue‐to‐tissue contact, wide‐crossing and reproductive contamination LGT mechanisms and discuss the likelihood of each in light of recent studies. Of particular relevance are transformation approaches that require minimal human intervention to transfer DNA among grasses in the lab that could mimic the mechanisms facilitating grass‐to‐grass LGT in the wild. These approaches include relatively simple techniques, such as pollen tube pathway‐mediated transformation, that take advantage of the permeability of the reproductive process to introduce alien genetic material from a third individual into an embryo. This process could be easily mirrored in the wild where pollen from one species lands on the stigma of another, acting as a source of alien DNA that can ultimately contaminate the reproductive process. This contamination is likely to be prevalent in wind pollinated species such as grasses, where the rates of illegitimate pollination will be high. In conclusion, plant transformation methods requiring minimal intervention are likely paralleled in the wild where they act as the mechanism underpinning LGT between distantly related grass species. [ABSTRACT FROM AUTHOR]

Published
2023
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25. Alloteropsis semialata as a study system for C4 evolution in grasses.

Author

Pereira, Lara, Bianconi, Matheus E, Osborne, Colin P, Christin, Pascal-Antoine, and Dunning, Luke T

Subjects
COMPARATIVE genomics, TROPICAL conditions, CHROMOSOME duplication, PHENOTYPIC plasticity, GENETIC variation, BIOCHEMISTRY
Abstract

Background Numerous groups of plants have adapted to CO2 limitations by independently evolving C4 photosynthesis. This trait relies on concerted changes in anatomy and biochemistry to concentrate CO2 within the leaf and thereby boost productivity in tropical conditions. The ecological and economic importance of C4 photosynthesis has motivated intense research, often relying on comparisons between distantly related C4 and non-C4 plants. The photosynthetic type is fixed in most species, with the notable exception of the grass Alloteropsis semialata. This species includes populations exhibiting the ancestral C3 state in southern Africa, intermediate populations in the Zambezian region and C4 populations spread around the palaeotropics. Scope We compile here the knowledge on the distribution and evolutionary history of the Alloteropsis genus as a whole and discuss how this has furthered our understanding of C4 evolution. We then present a chromosome-level reference genome for a C3 individual and compare the genomic architecture with that of a C4 accession of A. semialata. Conclusions Alloteropsis semialata is one of the best systems in which to investigate the evolution of C4 photosynthesis because the genetic and phenotypic variation provides a fertile ground for comparative and population-level studies. Preliminary comparative genomic investigations show that the C3 and C4 genomes are highly syntenic and have undergone a modest amount of gene duplication and translocation since the different photosynthetic groups diverged. The background knowledge and publicly available genomic resources make A. semialata a great model for further comparative analyses of photosynthetic diversification. [ABSTRACT FROM AUTHOR]

Published
2023
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44. Low dispersal and ploidy differences in a grass maintain photosynthetic diversity despite gene flow and habitat overlap

Author

European Research Council, Natural Environment Research Council (UK), Royal Society (UK), Olofsson, Jill K., Curran, Emma V., Nyirenda, Florence, Bianconi, Matheus E., Dunning, Luke T., Milenkovic, Vanja, Sotelo, Graciela, Hidalgo, Oriane, Powell, Robyn F., Lundgren, Marjorie R., Leitch, Ilia J., Nosil, Patrik, Osborne, Colin P., Christin, Pascal-Antoine, European Research Council, Natural Environment Research Council (UK), Royal Society (UK), Olofsson, Jill K., Curran, Emma V., Nyirenda, Florence, Bianconi, Matheus E., Dunning, Luke T., Milenkovic, Vanja, Sotelo, Graciela, Hidalgo, Oriane, Powell, Robyn F., Lundgren, Marjorie R., Leitch, Ilia J., Nosil, Patrik, Osborne, Colin P., and Christin, Pascal-Antoine

Abstract

Geographical isolation facilitates the emergence of distinct phenotypes within a single species, but reproductive barriers or selection are needed to maintain the polymorphism after secondary contact. Here, we explore the processes that maintain intraspecific variation of C4 photosynthesis, a complex trait that results from the combined action of multiple genes. The grass Alloteropsis semialata includes C4 and non-C4 populations, which have coexisted as a polyploid series for more than 1 million years in the miombo woodlands of Africa. Using population genomics, we show that there is genome-wide divergence for the photosynthetic types, but the current geographical distribution does not reflect a simple habitat displacement scenario as the genetic clusters overlap, being occasionally mixed within a given habitat. Despite evidence of recurrent introgression between non-C4 and C4 groups, in both diploids and polyploids, the distinct genetic lineages retain their identity, potentially because of selection against hybrids. Coupled with strong isolation by distance within each genetic group, this selection created a geographical mosaic of photosynthetic types. Diploid C4 and non-C4 types never grew together, and the C4 type from mixed populations constantly belonged to the hexaploid lineage. By limiting reproductive interactions between photosynthetic types, the ploidy difference probably allows their co-occurrence, reinforcing the functional diversity within this species. Together, these factors enabled the persistence of divergent physiological traits of ecological importance within a single species despite gene flow and habitat overlap.

Published
2021

49. Contrasted histories of organelle and nuclear genomes underlying physiological diversification in a grass species: Intraspecific dispersal of C4 physiology

Author

Bianconi, Matheus E., Dunning, Luke T., Curran, Emma V., Hidalgo, Oriane, Powell, Robyn F., Mian, Sahr, Leitch, Ilia J., Lundgren, Marjorie R., Manzi, Sophie, Vorontsova, Maria S., Besnard, Guillaume, Osborne, Colin P., Olofsson, Jill K., Christin, Pascal-Antoine, European Research Council, Royal Society (UK), Agence Nationale de la Recherche (France), and Labex TULIP

Abstract

C 4 photosynthesis evolved multiple times independently in angiosperms, but most origins are relatively old so that the early events linked to photosynthetic diversification are blurred. The grass Alloteropsis semialata is an exception, as this species encompasses C 4 and non-C 4 populations. Using phylogenomics and population genomics, we infer the history of dispersal and secondary gene flow before, during and after photosynthetic divergence in A. semialata. We further analyse the genome composition of individuals with varied ploidy levels to establish the origins of polyploids in this species. Detailed organelle phylogenies indicate limited seed dispersal within the mountainous region of origin and the emergence of a C 4 lineage after dispersal to warmer areas of lower elevation. Nuclear genome analyses highlight repeated secondary gene flow. In particular, the nuclear genome associated with the C 4 phenotype was swept into a distantly related maternal lineage probably via unidirectional pollen flow. Multiple intraspecific allopolyploidy events mediated additional secondary genetic exchanges between photosynthetic types. Overall, our results show that limited dispersal and isolation allowed lineage divergence, with photosynthetic innovation happening after migration to new environments, and pollen-mediated gene flow led to the rapid spread of the derived C 4 physiology away from its region of origin., This study was funded by the European Research Council (grant no. ERC-2014-STG-638333), the Royal Society (grant no. RGF\EA\181050) and has benefited from ‘Investissements d'Avenir' grants managed by the Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01 and TULIP, ref. ANR-10-LABX-41). Edinburgh Genomics, which contributed to the sequencing, is partly supported through core grants from the NERC (grant no. R8/H10/ 56), MRC (grant no. MR/K001744/1) and BBSRC (grant no. BB/ J004243/1). P.A.C. is funded by a Royal Society University Research Fellowship (grant no. URF\R\180022)., 1. Introduction 2. Materials and methods (a) Sampling, sequencing and data filtering (b) Genome sizing and carbon isotope analyses (c) Assembly of organelle genomes and molecular dating (d) Phylogenetic analyses of the nuclear genome (e) Genetic structure (f) Genome composition 3. Results (a) Genome sizes (b) Time-calibrated organelle phylogenies (c) Nuclear phylogeny (d) Population structure and genome composition 4. Discussion (a) Limited seed dispersal in the region of origin (b) Widespread pollen flow and sweep of the C4 nuclear genome (c) Recurrent hybridization and polyploidization 5. Concluding remarks Data accessibility Authors' contributions Competing interests Funding Acknowledgements Footnotes

Published
2020

50. Phylogenetic relatedness, co-occurrence, and rhizomes increase lateral gene transfer among grasses

Author

Hibdige, Samuel G. S., Raimondeau, Pauline, Christin, Pascal-Antoine, and Dunning, Luke T.

Subjects
food and beverages
Abstract

Background Lateral gene transfer (LGT) has been documented in a broad range of eukaryotes, where it can promote adaptation. In plants, LGT of functional nuclear genes has been repeatedly reported in parasitic plants, ferns and grasses, but the exact extent of the phenomenon remains unknown. Systematic studies are now needed to identify the factors that govern the frequency of LGT among plants. Results Here we scan the genomes of a diverse set of grass species that span more than 50 million years of divergence and include major crops. We identify protein coding LGT in a majority of them (13 out of 17). There is variation among species in the amount of LGT received, with rhizomatous species receiving more genes. In addition, the amount of LGT increases with phylogenetic relatedness, which might reflect genomic compatibility among close relatives facilitating successful transfers. However, we also observe genetic exchanges among distantly related species that diverged shortly after the origin of the grass family when they co-occur in the wild, pointing to a role of biogeography. The dynamics of successful LGT in grasses therefore appear to be dependent on both opportunity (co-occurrence and rhizomes) and compatibility (phylogenetic distance). Conclusion Overall, we show that LGT is a widespread phenomenon in grasses, which is boosted by repeated contact among related lineages. The process has moved functional genes across the entire grass family into domesticated and wild species alike.

Published
2020
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