title: Gains and Losses of Cis-regulatory Elements Led to Divergence of the Arabidopsis APETALA1 and CAULIFLOWER Duplicate Genes in the Time, Space, and Level of Expression and Regulation of One Paralog by the Other.
abstract: How genes change their expression patterns over time is still poorly understood. Here, by conducting expression, functional, bioinformatic, and evolutionary analyses, we demonstrate that the differences between the Arabidopsis (Arabidopsis thaliana) APETALA1 (AP1) and CAULIFLOWER (CAL) duplicate genes in the time, space, and level of expression were determined by the presence or absence of functionally important transcription factor-binding sites (TFBSs) in regulatory regions. In particular, a CArG box, which is the autoregulatory site of AP1 that can also be bound by the CAL protein, is a key determinant of the expression differences. Because of the CArG box, AP1 is both autoregulated and cross-regulated (by AP1 and CAL, respectively), and its relatively high-level expression is maintained till to the late stages of sepal and petal development. The observation that the CArG box was gained recently further suggests that the autoregulation and cross-regulation of AP1, as well as its function in sepal and petal development, are derived features. By comparing the evolutionary histories of this and other TFBSs, we further indicate that the divergence of AP1 and CAL in regulatory regions has been markedly asymmetric and can be divided into several stages. Specifically, shortly after duplication, when AP1 happened to be the paralog that maintained the function of the ancestral gene, CAL experienced certain degrees of degenerate evolution, in which several functionally important TFBSs were lost. Later, when functional divergence allowed the survival of both paralogs, CAL remained largely unchanged in expression, whereas the functions of AP1 were gradually reinforced by gains of the CArG box and other TFBSs.
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China (L.Y., B.W., W.Z., H.S., H.K.); andUniversity of the Chinese Academy of Sciences, Beijing 100049, China (L.Y., B.W., W.Z.).
authors.forename: Lingling
authors.identifier: 0000-0003-3834-862X
authors.initials: L
authors.lastname: Ye
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China (L.Y., B.W., W.Z., H.S., H.K.); andUniversity of the Chinese Academy of Sciences, Beijing 100049, China (L.Y., B.W., W.Z.).
authors.forename: Bin
authors.initials: B
authors.lastname: Wang
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China (L.Y., B.W., W.Z., H.S., H.K.); andUniversity of the Chinese Academy of Sciences, Beijing 100049, China (L.Y., B.W., W.Z.).
authors.forename: Wengen
authors.identifier: 0000-0003-0946-8614
authors.initials: W
authors.lastname: Zhang
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China (L.Y., B.W., W.Z., H.S., H.K.); andUniversity of the Chinese Academy of Sciences, Beijing 100049, China (L.Y., B.W., W.Z.) shanhongyan@ibcas.ac.cn hzkong@ibcas.ac.cn.
authors.forename: Hongyan
authors.identifier: 0000-0001-6662-2935
authors.initials: H
authors.lastname: Shan
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China (L.Y., B.W., W.Z., H.S., H.K.); andUniversity of the Chinese Academy of Sciences, Beijing 100049, China (L.Y., B.W., W.Z.) shanhongyan@ibcas.ac.cn hzkong@ibcas.ac.cn.
authors.forename: Hongzhi
authors.identifier: 0000-0002-0034-0510
authors.initials: H
authors.lastname: Kong
mesh_terms: D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D001483:Base Sequence; D001665:Binding Sites; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant; D020131:Genes, Duplicate; D026161:MADS Domain Proteins / Q000235:genetics* / Q000378:metabolism; D011485:Protein Binding / Q000235:genetics; D012045:Regulatory Sequences, Nucleic Acid / Q000235:genetics*; D012689:Sequence Homology, Nucleic Acid; D013997:Time Factors; D014157:Transcription Factors / Q000378:metabolism
chemical_list: C091535:AP1 protein, Arabidopsis; D029681:Arabidopsis Proteins; C091536:CAL protein, Arabidopsis; D026161:MADS Domain Proteins; D014157:Transcription Factors