C₄ photosynthesis evolved in warm climates but promoted migration to cooler ones

Abstract

C photosynthesis is considered an adaptation to warm climates, where its functional benefits are greatest and C plants achieve their highest diversity and dominance. However, whether inherent physiological barriers impede the persistence of C species in cool environments remains debated. Here, we use large grass phylogenetic and geographical distribution data sets to test whether (1) temperature influences the rate of C origins, (2) photosynthetic types affect the rate of migration among climatic zones, and (3) C evolution changes the breadth of the temperature niche. Our analyses show that C photosynthesis in grasses originated in tropical climates, and that C grasses were more likely to colonise cold climates. However, migration rates among tropical and temperate climates were higher in C grasses. Therefore, while the origins of C photosynthesis were concentrated in tropical climates, its physiological benefits across a broad temperature range expanded the niche into warmer climates and enabled diversification into cooler environments.

C4 anatomy can evolve via a single developmental change

“…Different traits may be involved in the initial transition to a C 4 phenotype and the subsequent adaptation and diversification of that phenotype (Christin & Osborne ; Watcharamongkol et al . ). Within the grass Alloteropsis semialata , we have shown that the only gross leaf property distinguishing all C 4 from all non‐C 4 phenotypes is the development of frequent minor veins.…”

SMRT sequencing of a full-length transcriptome reveals transcript variants involved in C18 unsaturated fatty acid biosynthesis and metabolism pathways at chilling temperature in Pennisetum giganteum

“…C 4 plants play a key role in world agriculture, crops such as maize and sorghum are major contributors to world food production in both developed and developing nations, and C 4 grasses are the major plant sources of bioenergy [23]. However, most C 4 plants are chilling sensitive [12]. It is important to develop an effective strategy for the genetic breeding of chilling tolerance in P. giganteum.…”

“…C 4 grasses dominate most open biomes in tropical and subtropical areas, where they achieve greater biomass and higher growth rates [11]. However, in cooler environments, the peak yields of most C 4 plants are markedly reduced [12]. As a result, the present global distribution of C 4 grasses is largely limited to warmer climate regions, and strong positive relationships between C 4 grass abundance and growing season temperature have been documented at continental scales and along elevational gradients on tropical mountains across the globe [13].…”

Widespread lateral gene transfer among grasses

“…Life history, distribution, growth form and the domestication status were retrieved from GrassBase (Clayton et al 2016). 1C Genome sizes were obtained from the Plant DNA C-values database (Bennett and Leitch 2005), and climatic information from Watcharamongkol et al (2018). The climate data for Oropetium thomaeum was not included in Watcharamongkol et al (2018), and was therefore retrieved from GBIF and expected frequencies for chi-squared tests based on the number of genes tested within each species (Table 1).…”

“…1C Genome sizes were obtained from the Plant DNA C-values database (Bennett and Leitch 2005), and climatic information from Watcharamongkol et al (2018). The climate data for Oropetium thomaeum was not included in Watcharamongkol et al (2018), and was therefore retrieved from GBIF and expected frequencies for chi-squared tests based on the number of genes tested within each species (Table 1). The Kruskal-Wallis tests performed used absolute LGT numbers, which were divided into donor groups when determining if some clades were more frequent donors than others.…”