Abstract
Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants. We hypothesize that convergent evolution of protein sequence and temporal gene expression underpins the independent emergences of CAM from C3 photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalanchoë fedtschenkoi, an obligate CAM species within the core eudicots with a relatively small genome (~260 Mb). Our comparative analyses identify signatures of convergence in protein sequence and re-scheduling of diel transcript expression of genes involved in nocturnal CO2 fixation, stomatal movement, heat tolerance, circadian clock, and carbohydrate metabolism in K. fedtschenkoi and other CAM species in comparison with non-CAM species. These findings provide new insights into molecular convergence and building blocks of CAM and will facilitate CAM-into-C3 photosynthesis engineering to enhance water-use efficiency in crops.
Highlights
Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants
We sought to investigate whether changes in protein sequence and/or gene expression contribute to the evolutionary convergence of CAM through genome-wide screening for signatures of convergent changes in protein sequences and diel mRNA expression patterns that meet the following criteria: the signatures are (1) isomorphic in the CAM genomes of distant groups, such as eudicots and monocots, which diverged ~135 million years ago[17], and (2) dimorphic in related C3 photosynthesis genomes
The major lineages of core eudicots are thought to have diversified rapidly following their first appearance, making resolution of the relationships among these clades challenging[17,25] and implicating incomplete lineage sorting (ILS) as a potentially important process that would result in discordance among gene histories[26]
Summary
A sudden drop in syntenic depth occurred after a depth of 4× (Fig. 2a), indicating that each grape genome region has up to four K. fedtschenkoi blocks and providing strong evidence for two distinct wholegenome duplications (WGDs) events in K. fedtschenkoi. Despite two apparent WGDs in the K. fedtschenkoi lineage, synonymous substitutions per synonymous site (Ks) between duplicate gene pairs showed only one prominent peak ~0.35 (Supplementary Fig. 8). Grape-Kalanchoë gene pairs show a prominent peak around Ks = 1.5 (Supplementary Fig. 8), indicating that the WGDs in the K. fedtschenkoi lineage occurred well after its divergence from grape early in the history of the rosid lineage. Our analysis identified 25 co-expression modules, among which one module
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