Abstract
C4 photosynthesis is a remarkable complex trait, elucidations of the evolutionary trajectory of C4 photosynthesis from its ancestral C3 pathway can help us better understand the generic principles of the evolution of complex traits and guide the engineering of C3 crops for higher yields. Here, we used the genus Flaveria that contains C3, C3–C4, C4-like and C4 species as a system to study the evolution of C4 photosynthesis. We first mapped transcript abundance, protein sequence and morphological features onto the phylogenetic tree of the genus Flaveria, and calculated the evolutionary correlation of different features; we then predicted the relative changes of ancestral nodes of those features to illustrate the major events during the evolution of C4 photosynthesis. We found that gene expression and protein sequence showed consistent modification patterns in the phylogenetic tree. High correlation coefficients ranging from 0.46 to 0.9 among gene expression, protein sequence and morphology were observed. The greatest modification of those different features consistently occurred at the transition between C3-C4 species and C4-like species. Our results show highly coordinated changes in gene expression, protein sequence and morphological features, which support evolutionary major events during the evolution of C4 metabolism.
Highlights
C4 photosynthesis is a remarkable complex trait, elucidations of the evolutionary trajectory of C4 photosynthesis from its ancestral C3 pathway can help us better understand the generic principles of the evolution of complex traits and guide the engineering of C3 crops for higher yields
RNA-Seq data of 31 samples of 16 Flaveria species were obtained from the public database Sequence Read Achieve (SRA) of the National Center for Biotechnology Information (NCBI) (Table S1)
Considering the large evolutionary divergence between Arabidopsis and Flaveria, which was estimated to be 120 million years, we estimated the accuracy of annotation by examining whether the transcripts annotated to be the same genes were from same orthologous groups
Summary
C4 photosynthesis is a remarkable complex trait, elucidations of the evolutionary trajectory of C4 photosynthesis from its ancestral C3 pathway can help us better understand the generic principles of the evolution of complex traits and guide the engineering of C3 crops for higher yields. We first mapped transcript abundance, protein sequence and morphological features onto the phylogenetic tree of the genus Flaveria, and calculated the evolutionary correlation of different features; we predicted the relative changes of ancestral nodes of those features to illustrate the major events during the evolution of C4 photosynthesis. We found that gene expression and protein sequence showed consistent modification patterns in the phylogenetic tree. Our results show highly coordinated changes in gene expression, protein sequence and morphological features, which support evolutionary major events during the evolution of C4 metabolism. In C 3 photosynthesis, CO2 is fixed by ribulose1,5-bisphosphate carboxylase/oxygenase (Rubisco), whereas in dual-cell C 4 photosynthesis, CO2 is initially fixed into a four-carbon organic acid in mesophyll cells (MCs) by phosphoenolpyruvate carboxylase (PEPC)[8]. Compared with C3 leaf anatomy, Kranz anatomy requires a spatial rearrangement of MCs and BSCs, cell size adjustment for increased numbers of organelles, larger organelles and metabolite transfer between the two cell types, and a reduction in distance between leaf veins
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