Dataset Information

Anatomical enablers and the evolution of C4 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.

SUBMITTER: Christin PA

PROVIDER: S-EPMC3557070 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Anatomical enablers and the evolution of C4 photosynthesis in grasses.

Christin Pascal-Antoine PA Osborne Colin P CP Chatelet David S DS Columbus J Travis JT Besnard Guillaume G Hodkinson Trevor R TR Garrison Laura M LM Vorontsova Maria S MS Edwards Erika J EJ

Proceedings of the National Academy of Sciences of the United States of America 20121224 4

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, ...[more]

PMID: 23267116

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Project description:C₄ is one of three known photosynthetic processes of carbon fixation in flowering plants. It evolved independently more than 61 times in multiple angiosperm lineages and consists of a series of anatomical and biochemical modifications to the ancestral C3 pathway increasing plant productivity under warm and light-rich conditions. The C4 lineages of eudicots belong to seven orders and 15 families, are phylogenetically less constrained than those of monocots and entail an enormous structural and ecological diversity. Eudicot C4 lineages likely evolved the C4 syndrome along different evolutionary paths. Therefore, a better understanding of this diversity is key to understanding the evolution of this complex trait as a whole. By compiling 1207 recognised C4 eudicots species described in the literature and presenting trait data among these species, we identify global centres of species richness and of high phylogenetic diversity. Furthermore, we discuss climatic preferences in the context of plant functional traits. We identify two hotspots of C4 eudicot diversity: arid regions of Mexico/Southern United States and Australia, which show a similarly high number of different C4 eudicot genera but differ in the number of C4 lineages that evolved in situ. Further eudicot C4 hotspots with many different families and genera are in South Africa, West Africa, Patagonia, Central Asia and the Mediterranean. In general, C4 eudicots are diverse in deserts and xeric shrublands, tropical and subtropical grasslands, savannas and shrublands. We found C4 eudicots to occur in areas with less annual precipitation than C4 grasses which can be explained by frequently associated adaptations to drought stress such as among others succulence and salt tolerance. The data indicate that C4 eudicot lineages utilising the NAD-ME decarboxylating enzyme grow in drier areas than those using the NADP-ME decarboxylating enzyme indicating biochemical restrictions of the later system in higher temperatures. We conclude that in most eudicot lineages, C4 evolved in ancestrally already drought-adapted clades and enabled these to further spread in these habitats and colonise even drier areas.

Dataset Information

Anatomical enablers and the evolution of C4 photosynthesis in grasses.

Publications

Anatomical enablers and the evolution of C4 photosynthesis in grasses.

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