Global distribution, climatic preferences and photosynthesis‐related traits of C 4 eudicots and how they differ from those of C 4 grasses

Berasategui, Jessica A.; Žerdoner Čalasan, Anže; Zizka, Alexander; Kadereit, Gudrun (2023): Global distribution, climatic preferences and photosynthesis‐related traits of C 4 eudicots and how they differ from those of C 4 grasses. Ecology and Evolution, 13 (11). ISSN 2045-7758

Abstract

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.

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 C 3 pathway increasing plant productivity under warm and light‐rich conditions. The C 4 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 C 4 lineages likely evolved the C 4 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 C 4 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 C 4 eudicot diversity: arid regions of Mexico/Southern United States and Australia, which show a similarly high number of different C 4 eudicot genera but differ in the number of C 4 lineages that evolved in situ. Further eudicot C 4 hotspots with many different families and genera are in South Africa, West Africa, Patagonia, Central Asia and the Mediterranean. In general, C 4 eudicots are diverse in deserts and xeric shrublands, tropical and subtropical grasslands, savannas and shrublands. We found C 4 eudicots to occur in areas with less annual precipitation than C 4 grasses which can be explained by frequently associated adaptations to drought stress such as among others succulence and salt tolerance. The data indicate that C 4 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, C 4 evolved in ancestrally already drought‐adapted clades and enabled these to further spread in these habitats and colonise even drier areas.
11 12 2023 11 2023 e10720 10.1002/ece3.10720 2 10.1002/crossmark_policy onlinelibrary.wiley.com true 2023-05-02 2023-10-30 2023-11-12 Deutsche Forschungsgemeinschaft https://doi.org/10.13039/501100001659 KA1816‐7/3 http://creativecommons.org/licenses/by/4.0/ 10.1002/ece3.10720 https://onlinelibrary.wiley.com/doi/10.1002/ece3.10720 https://onlinelibrary.wiley.com/doi/pdf/10.1002/ece3.10720 10.1600/0363644054223684 10.1080/11263504.2012.662921 10.1086/518263 10.6084/m9.figshare.14544207 10.1111/nph.19282 10.1002/jqs.876 10.1111/j.1365‐2486.2004.00833.x 10.1126/sciadv.abb8227 10.2172/910351 10.1600/036364412x656608 10.3732/ajb.1300279 10.1016/j.ppees.2014.12.003 10.1146/annurev.ecolsys.39.110707.173411 10.1111/jeb.12320 10.1111/nph.18919 10.1146/annurev.pp.08.060157.001423 10.1016/j.sajb.2019.05.032 10.3732/ajb.0800224 10.1038/38229 Chamberlain S. Barve V. Mcglinn D. Oldoni D. Desmet P. Geffert L. &Ram K.(2020).rgbif: Interface to the global biodiversity information facility API. 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• Dokumententyp: Artikel (LMU)
• Organisationseinheit (Fakultäten): 19 Biologie > Department Biologie I
• DFG-Fachsystematik der Wissenschaftsbereiche: Lebenswissenschaften
• DFG: Gefördert durch die Deutsche Forschungsgemeinschaft (DFG) - 491502892