The genome of Gynandropsis gynandra 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 Arabidopsis. Here, we present a high-quality genome sequence of G. gynandra, anchored onto 17 main super-scaffolds 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. We 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, +1x) 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 impact of gene duplication and gene retention on the evolution of C4 photosynthesis in Cleomaceae.

Integrated global analysis in spider-flowers illuminates features underlying the evolution and maintenance of C4 photosynthesis

“…Moreover, the Gg-α in G. gynandra contributed to the expansion of some gene families shared with the C 4 monocot Z. mays , which function in various C 4 metabolism-associated processes from signaling pathways to photosynthetic performance and stress resistance (Figure 4). This is supportive of recent studies showing that WGD led to multiple aspects of the evolution of C 4 photosynthesis in G. gynandra and grasses (Huang et al, 2021, 2022). Almost all of the well-documented vein development-associated genes in G. gynandra have retained their WGD-derived duplicates (Supplemental Data Set S20) (Ohashi-Ito and Fukuda, 2010; Huang et al, 2021; Liu et al, 2022).…”

“…G. gynandra has been an instrumental organism for addressing evolutionary questions, often as a pair with T. hassleriana (Hoang et al, 2022). This plant is valuable for the study of its nutritional and health-promoting properties, as well as molecular mechanisms absent in C 3 model organisms such as the dicot Arabidopsis and the monocot rice, and represents an emerging model plant to extensively investigate C 4 biology (Brown et al, 2005; Külahoglu et al, 2014; Bayat et al, 2018).…”

“…G. gynandra belongs to family of Cleomaceae, the sister clade to Brassicaceae, and is phylogenetically closest to the dicot C 3 model plant Arabidopsis thaliana , enabling the utilization of molecular resources and tools developed for Arabidopsis in G. gynandra and facilitating knowledge transfer (Marshall et al, 2007; Koteyeva et al, 2011; Patchell et al, 2014; Hoang et al, 2022). Moreover, G. gynandra , together with the congeneric C 3 species Tarenaya hassleriana (common names: spider-flower, pinkqueen and grandfather’s-whiskers), provides an invaluable genetic platform for comparative studies of many intriguing biological phenomena including the evolutionary trajectory and developmental progression from C 3 to C 4 (Bräutigam et al, 2011; Külahoglu et al, 2014; Bayat et al, 2018; Hüdig et al, 2022).…”

Transposable elements contribute to the establishment of the glycine shuttle in Brassicaceae species

“…Next, we analyzed the proportion of TEs in the individual genomes. Our estimation of TE proportions is consistent with previously analyzed Brassicacae genomes (Liu et al 2020, Mirouze & Vitte 2014 and the Gynandropsis gynandra genome (Hoang et al 2022). We found a significant correlation between the photosynthesis phenotype and the proportion of the genome occupied by TEs in the respective species.…”

Leaf elemental composition analysis in spider plant [Gynandropsis gynandra L. (Briq.)] differentiates three nutritional groups

“…These populations could be developed using the genotypes from clusters 1 and 2. Several methods could be used, including genome-wide association studies (GWAS) and QTL mapping, which will be easier with ongoing efforts to release the genome of G. gynandra (Hoang et al, 2022).…”