The evolutionary ecology of C₄plants

Abstract

765I.765II.767III.768IV.768V.770VI.771VII.773VIII.777777References777 Summary C4 photosynthesis is a physiological syndrome resulting from multiple anatomical and biochemical components, which function together to increase the CO2 concentration around Rubisco and reduce photorespiration. It evolved independently multiple times and C4 plants now dominate many biomes, especially in the tropics and subtropics. The C4 syndrome comes in many flavours, with numerous phenotypic realizations of C4 physiology and diverse ecological strategies. In this work, we analyse the events that happened in a C3 context and enabled C4 physiology in the descendants, those that generated the C4 physiology, and those that happened in a C4 background and opened novel ecological niches. Throughout the manuscript, we evaluate the biochemical and physiological evidence in a phylogenetic context, which demonstrates the importance of contingency in evolutionary trajectories and shows how these constrained the realized phenotype. We then discuss the physiological innovations that allowed C4 plants to escape these constraints for two important dimensions of the ecological niche – growth rates and distribution along climatic gradients. This review shows that a comprehensive understanding of C4 plant ecology can be achieved by accounting for evolutionary processes spread over millions of years, including the ancestral condition, functional convergence via independent evolutionary trajectories, and physiological diversification.

Grass diversification in Madagascar: In situ radiation of two large C3 shade clades and support for a Miocene to Pliocene origin of C4 grassy biomes

“…C 4 photosynthesis, although generally an adaptation to open and warm habitats, covers a large ecological spectrum (Christin & Osborne, ), and C 4 grassland communities in South Africa have been shown to cluster phylogenetically depending on humidity, fire regime and grazer disturbance (Visser, Woodward, Freckleton, & Osborne, ). In Madagascar, Andropogoneae and Chloridoideae also tend to dominate in more mesic versus more dry habitats, respectively (Bond et al., ).…”

Rubisco is not really so bad

“…In C 3 plants, where the photorespiratory pathway has evolved to carry large fluxes, its suppression could also destabilize plant cell metabolism due to perturbations in flux control properties of photosynthates production and consequences for N and S assimilation (Cornish‐Bowden, , Abadie, Boex‐Fontvieille, Carroll, & Tcherkez, , Eisenhut et al, , Busch, Sage, & Farquhar, , see also below). In other words, the cost/benefit ratio for photorespiration is probably not as large as often assumed and depends on a complex combination of environmental drivers (temperature, CO 2 concentration, and precipitation), as recent insights in the ecology of C 4 plants suggest (Christin & Osborne, ; Urban, Nelson, Street‐Perrott, Verschuren, & Hu, ). Benefits for crops from an oxygenase‐free Rubisco are thus difficult to anticipate considering potential consequences for the metabolic network associated with the oxygenase activity and photorespiratory recovery.…”

Determinants of woody encroachment and cover in African savannas

“…Photorespiration, which reduces the efficiency of photosynthesis, is more likely to occur in C 3 plants during periods of high temperatures and low atmospheric CO 2 (Sage 2004; Edwards et al 2010). In contrast, C 4 plants increase their carbon-fixation efficiency by saturating the Rubisco enzyme with CO 2 (Ehleringer 1978; Edwards et al 2010; Christin and Osborne 2014). Thus lower CO 2 is competitively advantageous to C 4 plants (Ehleringer et al 1997; Edwards et al 2010) and in eras of high atmospheric CO 2 , C 4 plant have less of a competitive advantage over C 3 plants offering a plausible reason for woody encroachment (Idso 1992).…”