Multiple Arabidopsis genes primed for recruitment into C₄ photosynthesis

Abstract

SUMMARYC 4 photosynthesis occurs in the most productive crops and vegetation on the planet, and has become widespread because it allows increased rates of photosynthesis compared with the ancestral C 3 pathway. Leaves of C 4 plants typically possess complicated alterations to photosynthesis, such that its reactions are compartmented between mesophyll and bundle sheath cells. Despite its complexity, the C 4 pathway has arisen independently in 62 separate lineages of land plants, and so represents one of the most striking examples of convergent evolution known. We demonstrate that elements in untranslated regions (UTRs) of multiple genes important for C 4 photosynthesis contribute to the metabolic compartmentalization characteristic of a C 4 leaf. Either the 5¢ or the 3¢ UTR is sufficient for cell specificity, indicating that functional redundancy underlies this key aspect of C 4 gene expression. Furthermore, we show that orthologous PPDK and CA genes from the C 3 plant Arabidopsis thaliana are primed for recruitment into the C 4 pathway. Elements sufficient for M-cell specificity in C 4 leaves are also present in both the 5¢ and 3¢ UTRs of these C 3 A. thaliana genes. These data indicate functional latency within the UTRs of genes from C 3 species that have been recruited into the C 4 pathway. The repeated recruitment of pre-existing cis-elements in C 3 genes may have facilitated the evolution of C 4 photosynthesis. These data also highlight the importance of alterations in trans in producing a functional C 4 leaf, and so provide insight into both the evolution and molecular basis of this important type of photosynthesis.

Recruitment of pre-existing networks during the evolution of C 4 photosynthesis

“…A similar situation has been found with PPDK and CA genes. Here, cis-regulatory elements located in untranslated regions generate preferential expression in M cells of C 4 G. gynandra [75,76]. Orthologous CA and PPDK genes from C 3 A. thaliana contain the same elements, and although they are silent in terms of cell specificity in C 3 leaves, when placed into C 4 G. gynandra, they lead to expression in the BS.…”

An Untranslated cis-Element Regulates the Accumulation of Multiple C4 Enzymes in Gynandropsis gynandra Mesophyll Cells

“…As these studies focused on a number of genes isolated from phylogenetically distinct C 4 species, they suggest that the mechanisms regulating genes of the C 4 pathway vary both within and between independent C 4 lineages. In the majority of cases, different sequences generate increased abundance and cell specificity for the same gene (Marshall et al, 1997;Akyildiz et al, 2007;Kajala et al, 2012;Wiludda et al, 2012), suggesting that the evolution of these two traits is not coordinated. Most mechanisms identified to date are also unique to each C 4 lineage studied, although a homologous mechanism has been co-opted to generate BS specificity for multiple genes encoding malic enzyme within maize (Zea mays) and Gynandropsis gynandra (formerly designated as Cleome gynandra; Brown et al, 2011).…”

“…Despite this, only individual CA genes have been studied to date. For example, in Flaveria, loss of a transit peptide repositions a highly abundant chloroplastic CA into the cytosol , while in G. gynandra, M specificity of CA4 is mediated by the UTRs (Kajala et al, 2012). To better understand the precise alterations required to recruit CA genes into C 4 photosynthesis, we examined GgCA4, which is preferentially expressed in M cells of the C 4 model species G. gynandra (Kajala et al, 2012).…”

“…For example, the increased abundance of C 4 enzymes can be conferred by elements within the promoter (Matsuoka et al, 1994;Gowik et al, 2004;Kajala et al, 2012;Wiludda et al, 2012), intron (Nomura et al, 2005b), or untranslated regions (UTRs) (Ali and Taylor, 2001;Wiludda et al, 2012). Similarly, cell specificity can be generated by the promoter (Matsuoka et al, 1994;Gowik et al, 2004), exon , or UTRs (Patel et al, 2004;Kajala et al, 2012). As these studies focused on a number of genes isolated from phylogenetically distinct C 4 species, they suggest that the mechanisms regulating genes of the C 4 pathway vary both within and between independent C 4 lineages.…”

Evolutionary transition from C3 to C4 photosynthesis and the route to C4 rice

“…By comparing ten gene families of known C 4 pathway components from three C 3 and three C 4 species whose genomes were completely sequenced, none of the C 4 plants shows a clear increase in gene copy number . Combining the facts that multiple C 3 genes possess elements to direct M or BS specificity in C 4 plants (Brown et al 2011;Kajala et al 2012), it implies that C 3 othologues of C 4 genes had already been predisposed for C 4 evolution before they were recruited into the C 4 cycle and gene duplication seems not to be necessary for the evolution of C 4 pathway . Earlier emergence of increased venation than that of high BS:M ratio during C 4 evolution is also in debate as proliferation of BS cells was observed to be more advanced than any increase in vein density in C 3 species of PACMAD lineages, to which all grasses with the C 4 pathway are restricted (Griffiths et al 2012).…”