Gene and genome duplications and the origin of C4 photosynthesis: Birth of a trait in the Cleomaceae

Abstract

a b s t r a c t C 4 photosynthesis is a trait that has evolved in 66 independent plant lineages and increases the efficiency of carbon fixation. The shift from C 3 to C 4 photosynthesis requires substantial changes to genes and gene functions effecting phenotypic, physiological and enzymatic changes. We investigate the role of ancient whole genome duplications (WGD) as a source of new genes in the development of this trait and compare expression between paralog copies. We compare Gynandropsis gynandra, the closest relative of Arabidopsis that uses C 4 photosynthesis, with its C 3 relative Tarenaya hassleriana that underwent a WGD named Th-␣. We establish through comparison of paralog synonymous substitution rate that both species share this paleohexaploidy. Homologous clusters of photosynthetic gene families show that gene copy numbers are similar to what would be expected given their duplication history and that no significant difference between the C 3 and C 4 species exists in terms of gene copy number. This is further confirmed by syntenic analysis of T. hassleriana, Arabidopsis thaliana and Aethionema arabicum, where syntenic region copy number ratios lie close to what could be theoretically expected. Expression levels of C 4 photosynthesis orthologs show that regulation of transcript abundance in T. hassleriana is much less strictly controlled than in G. gynandra, where orthologs have extremely similar expression patterns in different organs, seedlings and seeds. We conclude that the Th-␣ and older paleopolyploidy events have had a significant influence on the specific genetic makeup of Cleomaceae versus Brassicaceae. Because the copy number of various essential genes involved in C 4 photosynthesis is not significantly influenced by polyploidy combined with the fact that transcript abundance in G. gynandra is more strictly controlled, we also conclude that recruitment of existing genes through regulatory changes is more likely to have played a role in the shift to C 4 than the neofunctionalization of duplicated genes. DATA: The data deposited at NCBI represents raw RNA reads for each data series mentioned: 5 leaf stages, root, stem, stamen, petal, carpel, sepal, 3 seedling stages and 3 seed stages of Tarenaya hassleriana and Gynandropsis gynandra. The assembled reads were used for all analyses of this paper where RNA was used. http://www.ncbi.nlm.nih.gov/Traces/sra/?study=SRP036637, http://www.ncbi.nlm.nih.gov/ Traces/sra/?study=SRP036837 den Bergh), canan.kuelahoglu@uni-duesseldorf.de (C. Külahoglu), andrea.braeutigam@uni-duesseldorf.de (A. Bräutigam), jmh65@cam.ac.uk (J.M. Hibberd), andreas.weber@uni-duesseldorf.de (A.P.M. Weber), zhuxinguang@picb.ac.cn (X.-G. Zhu), eric.schranz@wur.nl (M. Eric Schranz).

Association between vitamin content, plant morphology and geographical origin in a worldwide collection of the orphan crop Gynandropsis gynandra (Cleomaceae)

“…Previous studies have demonstrated that individual accessions of Gynandropsis gynandra leaves are rich in nutrients including carotenoids, vitamin C and minerals (Neugart et al 2017;Odhav et al 2007;Omondi et al 2017;Schönfeldt and Pretorius 2011;Uusiku et al 2010;van Jaarsveld et al 2014). Variation between accessions of G. gynandra originating from East and Southern Africa showed variations in mineral levels and various health-related compounds including vitamin C, flavonoids, phenolics and glucosinolates, as well as in morphological traits (Jiménez-Aguilar and Grusak 2015; Omondi et al 2017).…”

Evolution of Portulacineae marked by gene tree conflict and gene family expansion associated with adaptation to harsh environments

“…Lineage-specific selection analyses on these two genes revealed that 10-13 internal branches are likely under positive selection, with the most occurred within Cactaceae. The role of gene duplication in the evolution of C 4 photosynthesis has been contentious, and some authors have proposed that neo-functionalization of genes following duplication has not played a major role in the evolution of C 4 photosynthesis (e.g., Williams et al 2012; van den Bergh et al 2014). However, recent analyses provide evidence that duplication and subsequent retention of genes are associated with the evolution of C 4 photosynthesis (Emms et al 2016), specifically including the NADP-dependent malic enzyme.…”

Comparative genomics and trait evolution in Cleomaceae, a model family for ancient polyploidy

“…In contrast, crown Brassicaceae are especially abundant in colder temperate climates (Stevens, 2001a). Some Cleomaceae are capable of C4 photosynthesis and, because of their phylogenetic relationship to Brassicaceae, they have been suggested as a new and emerging framework for analysis of gene and genomic structural and functional evolution (Marshall et al, 2007;Marquard and Steinback, 2009;van den Bergh et al, 2014). Moreover, Cleomaceae do not share the At-α duplication event of Brassicaceae, but have undergone a different, lineage-specific polyploidy event.…”

“…Moreover, Cleomaceae do not share the At-α duplication event of Brassicaceae, but have undergone a different, lineage-specific polyploidy event. This genome triplication event is termed Th-α and occurred approximately 24-13 Ma (Barker et al, 2009;van den Bergh et al, 2014). Because of the recent Th-α and At-α events in both families, these polyploidy events form an ideal comparison to study the effects of ancient genome multiplication.…”

“…Cleomaceae have been identified as a model genus for studying the transition from C3 to C4 photosynthesis (Brown et al, 2005) as it contains a number of C4 species, as well as a C3 / C4 intermediate (Feodorova et al, 2010). Cleomaceae are also studied as a model outgroup for Brassicaceae regarding polyploidy, and after sequencing of the T. hassleriana genome (Cheng et al, 2013), a model framework has rapidly emerged (van den Bergh et al, 2014Bergh et al, , 2016.…”