Evidence for the role of transposons in the recruitment of cis-regulatory motifs during the evolution of C4 photosynthesis.

Chensi Cao,Guangyong Zheng,Jiajia Xu,Xin-Guang Zhu

doi:10.1186/s12864-016-2519-3

Abstract

BackgroundC4 photosynthesis evolved from C3 photosynthesis and has higher light, water, and nitrogen use efficiencies. Several C4 photosynthesis genes show cell-specific expression patterns, which are required for these high resource-use efficiencies. However, the mechanisms underlying the evolution of cis-regulatory elements that control these cell-specific expression patterns remain elusive.ResultsIn the present study, we tested the hypothesis that the cis-regulatory motifs related to C4 photosynthesis genes were recruited from non-photosynthetic genes and further examined potential mechanisms facilitating this recruitment. We examined 65 predicted bundle sheath cell-specific motifs, 17 experimentally validated cell-specific cis-regulatory elements, and 1,034 motifs derived from gene regulatory networks. Approximately 7, 5, and 1,000 of these three categories of motifs, respectively, were apparently recruited during the evolution of C4 photosynthesis. In addition, we checked 1) the distance between the acceptors and the donors of potentially recruited motifs in a chromosome, and 2) whether the potentially recruited motifs reside within the overlapping region of transposable elements and the promoter of donor genes. The results showed that 7, 4, and 658 of the potentially recruited motifs might have moved via the transposable elements. Furthermore, the potentially recruited motifs showed higher binding affinity to transcription factors compared to randomly generated sequences of the same length as the motifs.ConclusionsThis study provides molecular evidence supporting the hypothesis that transposon-driven recruitment of pre-existing cis-regulatory elements from non-photosynthetic genes into photosynthetic genes plays an important role during C4 evolution. The findings of the present study coincide with the observed repetitive emergence of C4 during evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2519-3) contains supplementary material, which is available to authorized users.

Highlights

C4 photosynthesis evolved from C3 photosynthesis and has higher light, water, and nitrogen use efficiencies
We identified seven motifs that might have been potentially recruited during C4 evolution based on the following criteria: a) these are differentially distributed in C4 and C3 orthologs; b) these existed in the neighboring genes of the C3 orthologs (Table 1)
Identification of cis-regulatory elements that were potentially recruited during C4 evolution Based on the strategy shown in Fig. 1, 40 pairs of orthologs of the C4 genes in maize and rice, including its Occurrence of transposable elements (TEs)-driven motif recruitment in the experimentally validated motifs To test whether TE-driven motif recruitment is a general phenomenon, we further examined whether TEs are involved in the recruitment of motifs that were

Summary

Introduction

C4 photosynthesis evolved from C3 photosynthesis and has higher light, water, and nitrogen use efficiencies. The mechanisms underlying the evolution of cis-regulatory elements that control these cell-specific expression patterns remain elusive. C4 photosynthesis differs from C3 photosynthesis by possessing a CO2 concentrating mechanism, which enables C4 plants to achieve higher light, water, and nitrogen use efficiencies [1, 2]. One underlying assumption of this approach is that genes within the same cluster are potentially regulated by common cis-regulatory elements. Genes A and B are regulated by the same cis-regulatory elements, whereas C is regulated by B and shows the same expression pattern as that of B. If the expression pattern is used as the sole criterion in clustering these genes, these three genes will be misclassified into the same gene cluster, which in turn can lead to the inaccurate detection of cis-regulatory elements. Gene regulatory networks constructed based on conditional mutual information can solve the issue of misclassifying genes into the same cluster because this algorithm only detects genes with direct regulatory relationships [12]

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Discussion

Conclusion