Loss of Lateral suppressor gene is associated with evolution of root nodule symbiosis in Leguminosae

IF 10.1 1区生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY

Genome Biology Pub Date : 2024-09-30 DOI:10.1186/s13059-024-03393-6

Tengfei Liu, Zhi Liu, Jingwei Fan, Yaqin Yuan, Haiyue Liu, Wenfei Xian, Shuaiying Xiang, Xia Yang, Yucheng Liu, Shulin Liu, Min Zhang, Yuannian Jiao, Shifeng Cheng, Jeff J. Doyle, Fang Xie, Jiayang Li, Zhixi Tian

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引用次数: 0

Abstract

Root nodule symbiosis (RNS) is a fascinating evolutionary event. Given that limited genes conferring the evolution of RNS in Leguminosae have been functionally validated, the genetic basis of the evolution of RNS remains largely unknown. Identifying the genes involved in the evolution of RNS will help to reveal the mystery. Here, we investigate the gene loss event during the evolution of RNS in Leguminosae through phylogenomic and synteny analyses in 48 species including 16 Leguminosae species. We reveal that loss of the Lateral suppressor gene, a member of the GRAS-domain protein family, is associated with the evolution of RNS in Leguminosae. Ectopic expression of the Lateral suppressor (Ls) gene from tomato and its homolog MONOCULM 1 (MOC1) and Os7 from rice in soybean and Medicago truncatula result in almost completely lost nodulation capability. Further investigation shows that Lateral suppressor protein, Ls, MOC1, and Os7 might function through an interaction with NODULATION SIGNALING PATHWAY 2 (NSP2) and CYCLOPS to repress the transcription of NODULE INCEPTION (NIN) to inhibit the nodulation in Leguminosae. Additionally, we find that the cathepsin H (CTSH), a conserved protein, could interact with Lateral suppressor protein, Ls, MOC1, and Os7 and affect the nodulation. This study sheds light on uncovering the genetic basis of the evolution of RNS in Leguminosae and suggests that gene loss plays an essential role.

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侧抑制基因的缺失与豆科植物根瘤共生的进化有关

根瘤共生（RNS）是一个引人入胜的进化事件。鉴于豆科植物中促成 RNS 进化的基因得到的功能验证有限，RNS 进化的遗传基础在很大程度上仍然未知。确定参与 RNS 进化的基因将有助于揭开这一谜团。在此，我们通过对包括 16 个豆科植物在内的 48 个物种的系统发生组和同源关系分析，研究了豆科植物 RNS 进化过程中的基因缺失事件。我们发现，GRAS-domain 蛋白家族成员 Lateral 抑制基因的缺失与豆科植物中 RNS 的进化有关。番茄中的侧抑制因子（Ls）基因及其同源物水稻中的 MONOCULM 1（MOC1）和 Os7 在大豆和美智子中异位表达后，几乎完全丧失了结瘤能力。进一步的研究表明，侧抑制蛋白 Ls、MOC1 和 Os7 可能通过与 NODULATION SIGNALING PATHWAY 2（NSP2）和 CYCLOPS 相互作用，抑制 NODULE INCEPTION（NIN）的转录，从而抑制豆科植物的拔节。此外，我们还发现一种保守蛋白--凝血酶 H（CTSH）可与侧抑制蛋白 Ls、MOC1 和 Os7 相互作用，影响豆科植物的结瘤。这项研究揭示了豆科植物 RNS 演化的遗传基础，并表明基因缺失在其中发挥了重要作用。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Genome Biology Biochemistry, Genetics and Molecular Biology-Genetics

CiteScore

21.00

自引率

3.30%

发文量

241

审稿时长

2 months

期刊介绍： Genome Biology stands as a premier platform for exceptional research across all domains of biology and biomedicine, explored through a genomic and post-genomic lens. With an impressive impact factor of 12.3 (2022),* the journal secures its position as the 3rd-ranked research journal in the Genetics and Heredity category and the 2nd-ranked research journal in the Biotechnology and Applied Microbiology category by Thomson Reuters. Notably, Genome Biology holds the distinction of being the highest-ranked open-access journal in this category. Our dedicated team of highly trained in-house Editors collaborates closely with our esteemed Editorial Board of international experts, ensuring the journal remains on the forefront of scientific advances and community standards. Regular engagement with researchers at conferences and institute visits underscores our commitment to staying abreast of the latest developments in the field.