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J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (10): 2191-2207.DOI: 10.1111/jipb.13743  cstr: 32098.14.jipb.13743

Special Issue: Plant genomics

• Functional Omics and Systems Biology • Previous Articles     Next Articles

Duplication and sub-functionalization of flavonoid biosynthesis genes plays important role in Leguminosae root nodule symbiosis evolution

Tengfei Liu1,2†, Haiyue Liu2,3†, Wenfei Xian4,5†, Zhi Liu1,2,6†, Yaqin Yuan1,2, Jingwei Fan1, Shuaiying Xiang1,2, Xia Yang1,2, Yucheng Liu1, Shulin Liu1, Min Zhang1, Yanting Shen1, Yuannian Jiao2,7, Shifeng Cheng4, Jeff J. Doyle8*, Fang Xie2,3*, Jiayang Li2,9,10* and Zhixi Tian1,2*   

  1. 1.Key Laboratory of Seed Innovation, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
    2.University of Chinese Academy of Sciences, Beijing 100049, China
    3.Key Laboratory of Plant Carbon Capture, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China
    4.Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, China
    5.Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen 72076, Germany
    6.Hebei Key Laboratory of Crop Genetics and Breeding, Institute of Cereal and Oil Crops, Hebei Academy of Agricultural and Forestry Sciences, Shi‐jiazhuang 050035, China
    7.State Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China
    8.School of Integrative Plant Science, Sections of Plant Biology and Plant Breeding & Genetics, Cornell University, Ithaca, New York 14853, USA
    9.State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
    10.Yazhouwan National Laboratory, Sanya 572024, China
    †These authors contributed equally to this work.
    *Correspondences: Jeff J. Doyle (jjd5@cornell.edu); Fang Xie (fxie@cemps.ac.cn); Jiayang Li (jyli@genetics.ac.cn); Zhixi Tian (zxtian@genetics.ac.cn, Dr. Tian is fully responsible for the distributions of all materials associated with this article)
  • Received:2024-05-15 Accepted:2024-06-25 Online:2024-08-02 Published:2024-10-01
  • Supported by:
    The National Natural Science Foundation of China (grant nos. 32388201, 32300512 and U22A20467), “Strategic Priority Research Program” of the Chinese Academy of Sciences (grant no. XDA24030501), CAS Project for Young Scientists in Basic Research (YSBR‐078), and the Xplorer Prize.

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Abstract: Gene innovation plays an essential role in trait evolution. Rhizobial symbioses, the most important N2-fixing agent in agricultural systems that exists mainly in Leguminosae, is one of the most attractive evolution events. However, the gene innovations underlying Leguminosae root nodule symbiosis (RNS) remain largely unknown. Here, we investigated the gene gain event in Leguminosae RNS evolution through comprehensive phylogenomic analyses. We revealed that Leguminosae-gain genes were acquired by gene duplication and underwent a strong purifying selection. Kyoto Encyclopedia of Genes and Genomes analyses showed that the innovated genes were enriched in flavonoid biosynthesis pathways, particular downstream of chalcone synthase (CHS). Among them, Leguminosae-gain type Ⅱ chalcone isomerase (CHI) could be further divided into CHI1A and CHI1B clades, which resulted from the products of tandem duplication. Furthermore, the duplicated CHI genes exhibited exon–intron structural divergences evolved through exon/intron gain/loss and insertion/deletion. Knocking down CHI1B significantly reduced nodulation in Glycine max (soybean) and Medicago truncatula; whereas, knocking down its duplication gene CHI1A had no effect on nodulation. Therefore, Leguminosae-gain type Ⅱ CHI participated in RNS and the duplicated CHI1A and CHI1B genes exhibited RNS functional divergence. This study provides functional insights into Leguminosae-gain genetic innovation and sub-functionalization after gene duplication that contribute to the evolution and adaptation of RNS in Leguminosae.

Key words: CHI1, duplication, gene gain, Leguminosae, root nodule symbiosis evolution, sub‐functionalization

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