Parallel Recruitment of Multiple Genes into C4 Photosynthesis

Abstract

During the diversification of living organisms, novel adaptive traits usually evolve through the co-option of preexisting genes. However, most enzymes are encoded by gene families, whose members vary in their expression and catalytic properties. Each may therefore differ in its suitability for recruitment into a novel function. In this work, we test for the presence of such a gene recruitment bias using the example of C4 photosynthesis, a complex trait that evolved recurrently in flowering plants as a response to atmospheric CO2 depletion. We combined the analysis of complete nuclear genomes and high-throughput transcriptome data for three grass species that evolved the C4 trait independently. For five of the seven enzymes analyzed, the same gene lineage was recruited across the independent C4 origins, despite the existence of multiple copies. The analysis of a closely related C3 grass confirmed that C4 expression patterns were not present in the C3 ancestors but were acquired during the evolutionary transition to C4 photosynthesis. The significant bias in gene recruitment indicates that some genes are more suitable for a novel function, probably because the mutations they accumulated brought them closer to the characteristics required for the new function.

Evolutionary Convergence of Cell-Specific Gene Expression in Independent Lineages of C4 Grasses

“…For example, all 10 structural genes of the C 4 cycle and half of the metabolite transporters that are up-regulated in either M or BS cells of maize and S. viridis are syntenic. Our analysis supports the proposals of Christin et al (2013), but we also find that syntenic homologs from the OMT1 and Rubisco Activase gene families have been recruited into C 4 photosynthesis. We excluded genes encoding Ala aminotransferase and pyrophosphorylase from our analysis because the former is not associated with the NADP-ME pathway used by maize and S. viridis (Furbank et al, 2011) and the latter was not differentially expressed between M and BS cells.…”

“…Phylogenetic reconstructions have led to the inference that specific members of multigene families have repeatedly been coopted into the C 4 cycle and, therefore, that parallel evolution underlies their recruitment into the C 4 pathway (Christin et al, 2013). Using information on the relative abundance of transcripts in M and BS cells, which is a hallmark of C 4 photosynthesis, as well as synteny (Schnable et al, 2012), we show that a high proportion of genes recruited into the C 4 pathway are syntenic.…”

“…As genes are recruited into the C 4 cycle they are up-regulated, but their expression is also restricted to M or BS cells (Hibberd and Covshoff, 2010). The extent to which parallel evolution underlies both of these alterations in gene expression (Christin et al, 2013) may differ for each gene. The ancestral localization of each protein in M and BS cells of C 3 species will need to be determined to provide insight into this phenomenon.…”

Introgression and repeated co-option facilitated the recurrent emergence of C4photosynthesis among close relatives

“…The C 4 cycle is realized using the same set of genes in A. angusta and A. semialata , which can be explained by convergent evolution (e.g., as indicated for other C 4 grasses; Christin et al. 2013b) or a single origin of a weak C 4 cycle (C 3 +C 4 ), followed by a reversal to expression levels that resemble the ancestral condition in the C 3 accessions (Fig. 2).…”

“…In short, the reference datasets, composed of Arabidopsis thaliana coding sequences annotated as encoding C 4 ‐related enzymes, and homolog sequences from other completely sequenced plants including five grasses, were retrieved from Christin et al. (2013b; 2015), or generated following the same approach for additional C 4 ‐related enzymes identified in more recent studies (Mallmann et al. 2014; Li et al.…”