Parallel recruitment of multiple genes into c4 photosynthesis.

Pascal-Antoine Christin,Colin P Osborne,Susanna F Boxall,Richard Gregory,James Hartwell,Erika J Edwards

doi:10.1093/gbe/evt168

Abstract

During the diversification of living organisms, novel adaptive traits usually evolve through the co-option of preexisting genes. However, most enzymes are encoded by gene families, whose members vary in their expression and catalytic properties. Each may therefore differ in its suitability for recruitment into a novel function. In this work, we test for the presence of such a gene recruitment bias using the example of C4 photosynthesis, a complex trait that evolved recurrently in flowering plants as a response to atmospheric CO2 depletion. We combined the analysis of complete nuclear genomes and high-throughput transcriptome data for three grass species that evolved the C4 trait independently. For five of the seven enzymes analyzed, the same gene lineage was recruited across the independent C4 origins, despite the existence of multiple copies. The analysis of a closely related C3 grass confirmed that C4 expression patterns were not present in the C3 ancestors but were acquired during the evolutionary transition to C4 photosynthesis. The significant bias in gene recruitment indicates that some genes are more suitable for a novel function, probably because the mutations they accumulated brought them closer to the characteristics required for the new function.

Highlights

The adaptation of organisms to changing environmental conditions often requires the evolution of novel traits, sometimes of impressive complexity
Using phylogenetic analyses of whole nuclear genomes available for five grass species, we evaluate the size of C4-related gene families as well as the diversification of gene lineages in different subcellular compartments
Exceptions included the putative C4 aspartate aminotransferase (ASP-AT) of Setaria and the putative C4 alanine aminotransferase (ALAAT) of Setaria, Zea, and Alloteropsis, which were predicted to be chloroplast targeted, whereas the enzyme is reported in some literature to act in the cytosol or the mitochondria of C4 plants (e.g., Kanai and Edwards 1999; Furbank 2011)

Summary

Introduction

The adaptation of organisms to changing environmental conditions often requires the evolution of novel traits, sometimes of impressive complexity. Most enzymes are encoded by multigene families (Nei and Rooney 2005), whose members have evolved independently, in some cases for a long time. As a consequence, they have accumulated different mutations, which can affect the expression and catalytic properties of the encoded enzymes (Xu et al 2009; Hoffmann et al 2010; Storz et al 2013). As gene members are recurrently lost during the course of evolution (Nei and Rooney 2005), they might not be present in all species of a specific group, and their distribution might affect the evolvability of a complex trait

Methods

Results

Discussion

Conclusion