Anatomical enablers and the evolution of C ₄ photosynthesis in grasses

Abstract

C 4 photosynthesis is a series of anatomical and biochemical modifications to the typical C 3 pathway that increases the productivity of plants in warm, sunny, and dry conditions. Despite its complexity, it evolved more than 62 times independently in flowering plants. However, C 4 origins are absent from most plant lineages and clustered in others, suggesting that some characteristics increase C 4 evolvability in certain phylogenetic groups. The C 4 trait has evolved 22-24 times in grasses, and all origins occurred within the PACMAD clade, whereas the similarly sized BEP clade contains only C 3 taxa. Here, multiple foliar anatomy traits of 157 species from both BEP and PACMAD clades are quantified and analyzed in a phylogenetic framework. Statistical modeling indicates that C 4 evolvability strongly increases when the proportion of vascular bundle sheath (BS) tissue is higher than 15%, which results from a combination of short distance between BS and large BS cells. A reduction in the distance between BS occurred before the split of the BEP and PACMAD clades, but a decrease in BS cell size later occurred in BEP taxa. Therefore, when environmental changes promoted C 4 evolution, suitable anatomy was present only in members of the PACMAD clade, explaining the clustering of C 4 origins in this lineage. These results show that key alterations of foliar anatomy occurring in a C 3 context and preceding the emergence of the C 4 syndrome by millions of years facilitated the repeated evolution of one of the most successful physiological innovations in angiosperm history.precursor | preadaptation | phylogeny | Poaceae

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

“…We also recorded the presence of minor veins, and measured the following traits on one cross‐sectional image per accession, as described in Christin et al. (2013a), using ImageJ software (Schneider et al. 2012): the interveinal distance (IVD; the average distance between centers of consecutive veins), the number of mediolateral mesophyll cells between veins, the average width of all outer and inner bundle sheath cells within a leaf segment, and the ratio of outer to inner bundle sheath cell widths (OS:IS).…”

“…1) may have evolved relatively few times, and have then been recurrently used for independent transitions to C 3 +C 4 or C 4 photosynthesis (Christin et al. 2011, 2013a). …”

Occupation of bare habitats, an evolutionary precursor to soil specialization in plants

“…[22][23][24][25]. Experiments with an explicit phylogenetic framework can address aspects of trait evolution, niche conservatism, adaptation, historical contingency, exaptations, phylogenetic lag, and genetic constraints (20,(26)(27)(28)(29)(30). Here, we expand on these approaches by also incorporating extensive ecological data collections taken across field sites occupied by members of a whole clade, and integrating them with common garden greenhouse experiments and phylogenetic hypotheses.…”

Multiple origins of serpentine-soil endemism explained by preexisting tolerance of open habitats

“…Thus, there seems to be growing support for the idea that major adaptive transitions in evolution often, or even usually, occur through the prior establishment by chance of one or more preaptations (19)(20)(21). Once these preaptations are in place, it becomes much more likely that multiple independent parallel shifts (parallelisms) will occur, hence explaining the commonness of parallel evolution as is often observed in adaptive traits (15,18,21). Additional detailed phylogenetic comparative studies, such as this one (10), may show evolution by exaptation (preaptations acquiring new functions) to be the dominant theme wherever parallel evolution is observed in groups of related species.…”

“…The answer in both cases may be that critical preexisting features that enable an ecological shift are already in place. A recent study by Christin et al (18) found evidence for multiple parallel origins of C4 photosynthesis in grasses and that these shifts were contingent on appropriate preexisting leaf anatomy (exaptation). The parallels to the present study (10) are striking.…”