Evolutionary implications of C-3-C-4 intermediates in the grass Alloteropsis semialata

Lundgren, Marjorie R. and Christin, Pascal-Antoine and Ripley, Brad S. and Escobar, Emmanuel Gonzalez and Besnard, Guillaume and Long, Christine M. and Hattersley, Paul W. and Ellis, Roger P. and Leegood, Richard C. and Osborne, Colin P. (2016) Evolutionary implications of C-3-C-4 intermediates in the grass Alloteropsis semialata. Plant, Cell and Environment, 39 (9). pp. 1874-1885. ISSN 0140-7791

Abstract

C-4 photosynthesis is a complex trait resulting from a series of anatomical and biochemical modifications to the ancestral C-3 pathway. It is thought to evolve in a stepwise manner, creating intermediates with different combinations of C-4-like components. Determining the adaptive value of these components is key to understanding how C-4 photosynthesis can gradually assemble through natural selection. Here, we decompose the photosynthetic phenotypes of numerous individuals of the grass Alloteropsis semialata, the only species known to include both C-3 and C-4 genotypes. Analyses of C-13, physiology and leaf anatomy demonstrate for the first time the existence of physiological C-3-C-4 intermediate individuals in the species. Based on previous phylogenetic analyses, the C-3-C-4 individuals are not hybrids between the C-3 and C-4 genotypes analysed, but instead belong to a distinct genetic lineage, and might have given rise to C-4 descendants. C(3)A. semialata, present in colder climates, likely represents a reversal from a C-3-C-4 intermediate state, indicating that, unlike C-4 photosynthesis, evolution of the C-3-C-4 phenotype is not irreversible.