Independent and Parallel Evolution of New Genes by Gene Duplication in Two Origins of C4 Photosynthesis Provides New Insight into the Mechanism of Phloem Loading in C4 Species.

David M Emms,Julian M Hibberd,Sarah Covshoff,Steven Kelly

doi:10.1093/molbev/msw057

David M Emms, Julian M Hibberd + Show 2 more

Open Access

https://doi.org/10.1093/molbev/msw057

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Abstract

C4 photosynthesis is considered one of the most remarkable examples of evolutionary convergence in eukaryotes. However, it is unknown whether the evolution of C4 photosynthesis required the evolution of new genes. Genome-wide gene-tree species-tree reconciliation of seven monocot species that span two origins of C4 photosynthesis revealed that there was significant parallelism in the duplication and retention of genes coincident with the evolution of C4 photosynthesis in these lineages. Specifically, 21 orthologous genes were duplicated and retained independently in parallel at both C4 origins. Analysis of this gene cohort revealed that the set of parallel duplicated and retained genes is enriched for genes that are preferentially expressed in bundle sheath cells, the cell type in which photosynthesis was activated during C4 evolution. Furthermore, functional analysis of the cohort of parallel duplicated genes identified SWEET-13 as a potential key transporter in the evolution of C4 photosynthesis in grasses, and provides new insight into the mechanism of phloem loading in these C4 species.Key words: C4 photosynthesis, gene duplication, gene families, parallel evolution.

Highlights

The evolution of C4 photosynthesis from ancestral C3 photosynthesis involved multiple changes to biochemistry, subcellular compartmentalization, and leaf anatomy such that most modern-day C4 species partition the entire photosynthetic process between two discrete cell types—bundle sheath (BS) and mesophyll (M) cells
To identify retained gene duplication events the following two filtration criteria were applied: 1) A gene duplication event must have supporting evidence for its occurrence from at least two species and 2) all genes resulting from a gene duplication event must be retained in the genomes of all species that diverged after the duplication event
A significant body of knowledge has amassed concerning genes that are differentially expressed between C4 and C3 species, it is unknown whether the evolution of C4 photosynthesis was concomitant with the evolution of new genes

Summary

Introduction

The evolution of C4 photosynthesis from ancestral C3 photosynthesis involved multiple changes to biochemistry, subcellular compartmentalization, and leaf anatomy such that most modern-day C4 species partition the entire photosynthetic process between two discrete cell types—bundle sheath (BS) and mesophyll (M) cells. This partitioning of the photosynthesis reactions between two cells facilitates an increase in CO2 concentration around Rubisco leading to a reduction in photorespiration and a concomitant increase in photosynthetic efficiency (Hatch et al 1967). Our understanding of gene expression changes associated with C4 biology is rapidly increasing, almost nothing is known about the gene content differences that distinguish C4 species from their C3 relatives

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