The Gynandropsis gynandra genome provides insights into whole-genome duplications and the evolution of C4 photosynthesis in Cleomaceae

Abstract Gynandropsis gynandra (Cleomaceae) is a cosmopolitan leafy vegetable and medicinal plant, which has also been used as a model to study C4 photosynthesis due to its evolutionary proximity to C3 Arabidopsis (Arabidopsis thaliana). Here, we present the genome sequence of G. gynandra, anchored...

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Published inThe Plant cell Vol. 35; no. 5; pp. 1334 - 1359
Main Authors Hoang, Nam V, Sogbohossou, E O Deedi, Xiong, Wei, Simpson, Conor J C, Singh, Pallavi, Walden, Nora, van den Bergh, Erik, Becker, Frank F M, Li, Zheng, Zhu, Xin-Guang, Brautigam, Andrea, Weber, Andreas P M, van Haarst, Jan C, Schijlen, Elio G W M, Hendre, Prasad S, Van Deynze, Allen, Achigan-Dako, Enoch G, Hibberd, Julian M, Schranz, M Eric
Format Journal Article
LanguageEnglish
Published US Oxford University Press 20.04.2023
Subjects
Arabidopsis - genetics
Brassicaceae - genetics
Evolution, Molecular
Gene Duplication
Large-Scale Biology
Magnoliopsida - genetics
Photosynthesis - genetics
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Summary:Abstract Gynandropsis gynandra (Cleomaceae) is a cosmopolitan leafy vegetable and medicinal plant, which has also been used as a model to study C4 photosynthesis due to its evolutionary proximity to C3 Arabidopsis (Arabidopsis thaliana). Here, we present the genome sequence of G. gynandra, anchored onto 17 main pseudomolecules with a total length of 740 Mb, an N50 of 42 Mb and 30,933 well-supported gene models. The G. gynandra genome and previously released genomes of C3 relatives in the Cleomaceae and Brassicaceae make an excellent model for studying the role of genome evolution in the transition from C3 to C4 photosynthesis. Our analyses revealed that G. gynandra and its C3 relative Tarenaya hassleriana shared a whole-genome duplication event (Gg-α), then an addition of a third genome (Th-α, +1×) took place in T. hassleriana but not in G. gynandra. Analysis of syntenic copy number of C4 photosynthesis-related gene families indicates that G. gynandra generally retained more duplicated copies of these genes than C3T. hassleriana, and also that the G. gynandra C4 genes might have been under positive selection pressure. Both whole-genome and single-gene duplication were found to contribute to the expansion of the aforementioned gene families in G. gynandra. Collectively, this study enhances our understanding of the polyploidy history, gene duplication and retention, as well as their impact on the evolution of C4 photosynthesis in Cleomaceae. The Gynandropsis gynandra genome sequence facilitates comparative phylogenomics and sheds light on the whole-genome duplication history and evolution of C4 photosynthesis in Cleomaceae.
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The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (https://academic.oup.com/plcell) is: M. Eric Schranz (eric.schranz@wur.nl).
These authors contributed equally to this work
M.E.S., J.M.H., E.G.A.-D., A.P.M.W., and X.Z. conceived the project and coordinated the genome assembly and annotation; M.E.S. supervised the data analysis and manuscript preparation; N.V.H., E.O.D.S., and M.E.S. performed experiments and analyzed the data; N.V.H. prepared the first draft of the paper and figures with the inputs from other authors; E.v.d.B. and A.B. contributed to initial genome annotation; W.X. produced the final genome annotation; N.W. contributed to phylogenetic analyses of subgenomes; F.F.M.B. helped with sample collection, DNA extraction, and sequencing; Z.L. contributed to analyses of gene-tree reconciliation and gene duplication mapping; C.J.C.S. and P.S. contributed to the analysis of C4-related genes; J.C.v.H. and E.G.W.M.S. contributed to 10× genomic sequencing and assembly; P.S.H. and A.V.D. contributed to genome analysis and editing manuscript; E.G.A.-D. contributed to funding acquisition, project administration, supervision, and editing; J.M.H. contributed to experiment design, data interpretation, and editing manuscript. All authors read, edited, and approved the final manuscript.
Conflict of interest statement. The authors declare no conflict of interest.
ISSN:1040-4651
1532-298X
DOI:10.1093/plcell/koad018