title: Evidence for the role of transposons in the recruitment of cis-regulatory motifs during the evolution of C4 photosynthesis.
abstract: BACKGROUND
  C4 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.
  
  
  RESULTS
  In 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.
  
  
  CONCLUSIONS
  This 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.
authors.affiliation: CAS Key Laboratory for Computational Biology, CAS-MPG Partner Institute for Computational Biology, Chinese Academy of Sciences, Room 102, Physiology Building, 320 Yueyang Road, Shanghai, 200031, China. chensicao@capitalbio.com.
authors.forename: Chensi
authors.initials: C
authors.lastname: Cao
authors.affiliation: CAS Key Laboratory for Computational Biology, CAS-MPG Partner Institute for Computational Biology, Chinese Academy of Sciences, Room 102, Physiology Building, 320 Yueyang Road, Shanghai, 200031, China. xu.mercedes@gmail.com.
authors.forename: Jiajia
authors.initials: J
authors.lastname: Xu
authors.affiliation: CAS Key Laboratory for Computational Biology, CAS-MPG Partner Institute for Computational Biology, Chinese Academy of Sciences, Room 102, Physiology Building, 320 Yueyang Road, Shanghai, 200031, China. zhengguangyong@picb.ac.cn.
authors.forename: Guangyong
authors.initials: G
authors.lastname: Zheng
authors.affiliation: CAS Key Laboratory for Computational Biology, CAS-MPG Partner Institute for Computational Biology, Chinese Academy of Sciences, Room 102, Physiology Building, 320 Yueyang Road, Shanghai, 200031, China. zhuxinguang@picb.ac.cn.
authors.forename: Xin-Guang
authors.initials: XG
authors.lastname: Zhu
mesh_terms: D001665:Binding Sites; D005075:Biological Evolution; D004251:DNA Transposable Elements; D018506:Gene Expression Regulation, Plant; D053263:Gene Regulatory Networks; D012275:Oryza / Q000235:genetics; D010788:Photosynthesis / Q000235:genetics*; D011401:Promoter Regions, Genetic; D014157:Transcription Factors / Q000378:metabolism; D003313:Zea mays / Q000235:genetics
chemical_list: D004251:DNA Transposable Elements; D014157:Transcription Factors