Phenotypic landscape inference reveals multiple evolutionary paths to C4 photosynthesis

Abstract

C4 photosynthesis has independently evolved from the ancestral C3 pathway in at least 60 plant lineages, but, as with other complex traits, how it evolved is unclear. Here we show that the polyphyletic appearance of C4 photosynthesis is associated with diverse and flexible evolutionary paths that group into four major trajectories. We conducted a meta-analysis of 18 lineages containing species that use C3, C4, or intermediate C3–C4 forms of photosynthesis to parameterise a 16-dimensional phenotypic landscape. We then developed and experimentally verified a novel Bayesian approach based on a hidden Markov model that predicts how the C4 phenotype evolved. The alternative evolutionary histories underlying the appearance of C4 photosynthesis were determined by ancestral lineage and initial phenotypic alterations unrelated to photosynthesis. We conclude that the order of C4 trait acquisition is flexible and driven by non-photosynthetic drivers. This flexibility will have facilitated the convergent evolution of this complex trait.DOI: http://dx.doi.org/10.7554/eLife.00961.001

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

“…This promoter sequence is unlikely to be important in generating M specificity, as Gg-CA4 transcripts are equally abundant between M and BS cells (Supplemental Table 2). Computational modeling of the convergent evolutionary events generating C 4 photosynthesis in a wide variety of lineages predicts that increased abundance and cell specificity also evolved independently for at least five additional C 4 pathway enzymes (Williams et al, 2013). It therefore appears that the decoupling of changes to enzyme abundance and cell type localization may be a general trend in C 4 evolution, occurring in multiple lineages and in the evolution of both enzymes localized to either BS or M cells.…”

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

“…Furthermore, all the enzymes of the C 4 pathway identified to date operate in C 3 species [18]. Indeed, a number of models depicting evolutionary trajectories from C 3 to C 4 photosynthesis have been developed in recent years [2,16,[39][40][41]. Although these models take contrasting approaches and focus on slightly different aspects of the C 4 system, overall they support the notion that anatomical modifications tended to precede a series of modular changes to metabolic networks that led to evolution of the full C 4 pathway.…”

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

“…This preferential accumulation of proteins is underpinned by transcriptional and posttranscriptional regulation of gene expression as well as posttranslational modification (Hibberd and Covshoff, 2010). While there is considerable diversity in the mechanisms responsible for cell-specific gene expression in C 4 leaves, and modeling predicts that the evolution of C 4 photosynthesis has occurred via distinct routes in various taxa (Williams et al, 2013), it is now clear that there are also examples where the same mechanism has been used by independent C 4 lineages to generate expression in either M or BS cells. For example, the accumulation of NAD-dependent malic enzyme in Cleome gynandra and NADP-ME in maize (Zea mays) is mediated by a conserved element found within the coding sequence of these genes .…”