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Evolution of the KCS gene family in plants: the history of gene duplication, sub/neofunctionalization and redundancy

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Abstract

Very long-chain fatty acids (VLCFAs) play an important role in the survival and development of plants, and VLCFA synthesis is regulated by β-ketoacyl-CoA synthases (KCSs), which catalyze the condensation of an acyl-CoA with malonyl-CoA. Here, we present a genome-wide survey of the genes encoding these enzymes, KCS genes, in 28 species (26 genomes and two transcriptomes), which represents a large phylogenetic scale, and also reconstruct the evolutionary history of this gene family. KCS genes were initially single-copy genes in the green plant lineage; duplication resulted in five ancestral copies in land plants, forming five fundamental monophyletic groups in the phylogenetic tree. Subsequently, KCS genes duplicated to generate 11 genes of angiosperm origin, expanding up to 20–30 members in further-diverged angiosperm species. During this process, tandem duplications had only a small contribution, whereas polyploidy events and large-scale segmental duplications appear to be the main driving force. Accompanying this expansion were variations that led to the sub- and neofunctionalization of different members, resulting in specificity that is likely determined by the 3-D protein structure. Novel functions involved in other physiological processes emerged as well, though redundancy is also observed, largely among recent duplications. Conserved sites and variable sites of KCS proteins are also identified by statistical analysis. The variable sites are likely to be involved in the emergence of product specificity and catalytic power, and conserved sites are possibly responsible for the preservation of fundamental function.

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Acknowledgments

We gratefully acknowledge the editor-in-chief Dr. Hohmann and two anonymous reviewers for their constructive suggestions to improve the manuscript, Dr. Zhu-Qing Shao at Nanjing University for his assistance in the bioinformatics analysis, and Dr. Yang Liu at the University of Connecticut for insightful discussions. This work was supported by grants from the National Natural Science Founding of China to JYX (31300190), XQS (31200177 and 31470448), the Natural Science Founding of Jiangsu Province (BK20130565) to JYX, and Funds of Jiangsu Province Key Laboratory for Plant Ex Situ Conservation to XQS (QIAN201202) (http://www.nsfc.gov.cn, http://www.jskjjh.gov.cn, http://www.cnbg.net/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Correspondence to Yue-Yu Hang or Jia-Yu Xue.

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H.-S. Guo and Y.-M. Zhang contributed equally to this work.

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438_2015_1142_MOESM1_ESM.pdf

Figure S1. The detailed phylogenetic tree of KCS genes. Five monophyletic land plant groups, A (red), B (light blue), C (orange), D (dark blue) and E (black) and 11 angiosperm groups (1–11) are indicated. The scale bars represent numbers of amino acid substitutions per site. The support values (SH-aLRT value) for basal nodes are indicated. Figure S2. The amino acid frequencies of KCS proteins (by WebLogo). Table S1. The positions and corresponding amino acids with frequencies >90 %, >70 % and >50 % among the whole gene family. Table S2. The tandem arrayed KCS genes among the surveyed plant genomes (PDF 8466 kb)

438_2015_1142_MOESM2_ESM.xlsx

Table S3. The identity and divergence of KCS proteins. Percent identities are in presented in upper triangle; percent divergences are presented in lower triangle; potential redundant genes are highlighted in red (XLSX 92 kb)

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Guo, HS., Zhang, YM., Sun, XQ. et al. Evolution of the KCS gene family in plants: the history of gene duplication, sub/neofunctionalization and redundancy. Mol Genet Genomics 291, 739–752 (2016). https://doi.org/10.1007/s00438-015-1142-3

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