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

被引：1

作者：

Liu, Tengfei ^{[1
,8
]}

Liu, Zhi ^{[1
,8
,10
]}

Fan, Jingwei ^{[1
]}

Yuan, Yaqin ^{[1
,8
]}

Liu, Haiyue ^{[2
,8
]}

Xian, Wenfei ^{[3
,9
]}

Xiang, Shuaiying ^{[1
,8
]}

Yang, Xia ^{[1
,8
]}

Liu, Yucheng ^{[1
]}

Liu, Shulin ^{[1
]}

Zhang, Min ^{[1
]}

Jiao, Yuannian ^{[4
,8
]}

Cheng, Shifeng ^{[3
]}

Doyle, Jeff J. ^{[5
]}

Xie, Fang ^{[2
,8
]}

Li, Jiayang ^{[6
,7
,8
,11
]}

Tian, Zhixi ^{[1
,8
,11
]}

机构：

[1] Chinese Acad Sci, Inst Genet & Dev Biol, Key Lab Seed Innovat, Beijing, Peoples R China

[2] Chinese Acad Sci, Shanghai Inst Plant Physiol & Ecol, CAS Ctr Excellence Mol Plant Sci, Key Lab Plant Carbon Capture, Shanghai, Peoples R China

[3] Chinese Acad Agr Sci, Agr Genom Inst Shenzhen, Guangdong Lab Lingnan Modern Agr, Genome Anal Lab,Minist Agr,Shenzhen Branch, Shenzhen, Peoples R China

[4] Chinese Acad Sci, Inst Bot, State Key Lab Plant Divers & Specialty Crops, Beijing, Peoples R China

[5] Cornell Univ, Sch Integrat Plant Sci, Sect Plant Biol & Plant Breeding & Genet, Ithaca, NY 14850 USA

[6] Chinese Acad Sci, State Key Lab Plant Genom, Beijing, Peoples R China

[7] Chinese Acad Sci, Inst Genet & Dev Biol, Natl Ctr Plant Gene Res, Beijing, Peoples R China

[8] Univ Chinese Acad Sci, Beijing, Peoples R China

[9] Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany

[10] Hebei Acad Agr & Forestry Sci, Inst Cereal & Oil Crops, Hebei Key Lab Crop Genet & Breeding, Shijiazhuang, Peoples R China

[11] Yazhouwan Natl Lab, Sanya, Hainan, Peoples R China

来源：

GENOME BIOLOGY | 2024年 / 25卷 / 01期

基金：

中国国家自然科学基金;

关键词：

Evolution of root nodule symbiosis; Leguminosae; Phylogenomic analysis; Gene loss; Lateral suppressor; DRAFT GENOME SEQUENCE; SELF-INCOMPATIBILITY; MERISTEM FORMATION; PROVIDES INSIGHT; NODULATION; REVEALS; COMPLEX; EXPRESSION; DIVERSITY; ALIGNMENT;

D O I：

10.1186/s13059-024-03393-6

中图分类号：

Q81 [生物工程学（生物技术）]; Q93 [微生物学];

学科分类号：

071005 ; 0836 ; 090102 ; 100705 ;

摘要：

Background: 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. Results: 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. Conclusions: 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.

引用

页数：24

共 147 条

[1] Sulfur deficiency-induced genes affect seed protein accumulation and composition under sulfate deprivation [J].

Aarabi, Fayezeh ;

Rakpenthai, Apidet ;

Barahimipour, Rouhollah ;

Gorka, Michal ;

Alseekh, Saleh ;

Zhang, Youjun ;

Salem, Mohamed A. ;

Bruckner, Franziska ;

Omranian, Nooshin ;

Watanabe, Mutsumi ;

Nikoloski, Zoran ;

Giavalisco, Patrick ;

Tohge, Takayuki ;

Graf, Alexander ;

Fernie, Alisdair R. ;

Hoefgen, Rainer .

PLANT PHYSIOLOGY, 2021, 187 (04) :2419-2434

[2] Sulfur deficiency-induced repressor proteins optimize glucosinolate biosynthesis in plants [J].

Aarabi, Fayezeh ;

Kusajima, Miyuki ;

Tohge, Takayuki ;

Konishi, Tomokazu ;

Gigolashvili, Tamara ;

Takamune, Makiko ;

Sasazaki, Yoko ;

Watanabe, Mutsumi ;

Nakashita, Hideo ;

Fernie, Alisdair R. ;

Saito, Kazuki ;

Takahashi, Hideki ;

Hubberten, Hans-Michael ;

Hoefgen, Rainer ;

Maruyama-Nakashita, Akiko .

SCIENCE ADVANCES, 2016, 2 (10)

[3] Evolution by gene loss [J].

Albalat, Ricard ;

Canestro, Cristian .

NATURE REVIEWS GENETICS, 2016, 17 (07) :379-391

[4] The Amborella Genome and the Evolution of Flowering Plants [J].

Albert, Victor A. ;

Barbazuk, W. Bradley ;

dePamphilis, Claude W. ;

Der, Joshua P. ;

Leebens-Mack, James ;

Ma, Hong ;

Palmer, Jeffrey D. ;

Rounsley, Steve ;

Sankoff, David ;

Schuster, Stephan C. ;

Soltis, Douglas E. ;

Soltis, Pamela S. ;

Wessler, Susan R. ;

Wing, Rod A. ;

Albert, Victor A. ;

Ammiraju, Jetty S. S. ;

Barbazuk, W. Bradley ;

Chamala, Srikar ;

Chanderbali, Andre S. ;

dePamphilis, Claude W. ;

Der, Joshua P. ;

Determann, Ronald ;

Leebens-Mack, James ;

Ma, Hong ;

Ralph, Paula ;

Rounsley, Steve ;

Schuster, Stephan C. ;

Soltis, Douglas E. ;

Soltis, Pamela S. ;

Talag, Jason ;

Tomsho, Lynn ;

Walts, Brandon ;

Wanke, Stefan ;

Wing, Rod A. ;

Albert, Victor A. ;

Barbazuk, W. Bradley ;

Chamala, Srikar ;

Chanderbali, Andre S. ;

Chang, Tien-Hao ;

Determann, Ronald ;

Lan, Tianying ;

Soltis, Douglas E. ;

Soltis, Pamela S. ;

Arikit, Siwaret ;

Axtell, Michael J. ;

Ayyampalayam, Saravanaraj ;

Barbazuk, W. Bradley ;

Burnette, James M., III ;

Chamala, Srikar ;

De Paoli, Emanuele .

SCIENCE, 2013, 342 (6165) :1467-+

[5]

ALTSCHUL SF, 1990, J MOL BIOL, V215, P403, DOI 10.1006/jmbi.1990.9999

[6] A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny [J].

Azani, Nasim ;

Babineau, Marielle ;

Bailey, C. Donovan ;

Banks, Hannah ;

Barbosa, Ariane R. ;

Pinto, Rafael Barbosa ;

Boatwright, James S. ;

Borges, Leonardo M. ;

Brown, Gillian K. ;

Bruneau, Anne ;

Candido, Elisa ;

Cardoso, Domingos ;

Chung, Kuo-Fang ;

Clark, Ruth P. ;

Conceicao, Adilva de S. ;

Crisp, Michael ;

Cubas, Paloma ;

Delgado-Salinas, Alfonso ;

Dexter, Kyle G. ;

Doyle, Jeff J. ;

Duminil, Jerome ;

Egan, Ashley N. ;

de la Estrella, Manuel ;

Falcao, Marcus J. ;

Filatov, Dmitry A. ;

Fortuna-Perez, Ana Paula ;

Fortunato, Renee H. ;

Gagnon, Edeline ;

Gasson, Peter ;

Rando, Juliana Gastaldello ;

Goulart de Azevedo Tozzi, Ana Maria ;

Gunn, Bee ;

Harris, David ;

Haston, Elspeth ;

Hawkins, Julie A. ;

Herendeen, Patrick S. ;

Hughes, Colin E. ;

Iganci, Joao R. V. ;

Javadi, Firouzeh ;

Kanu, Sheku Alfred ;

Kazempour-Osaloo, Shahrokh ;

Kite, Geoffrey C. ;

Klitgaard, Bente B. ;

Kochanovski, Fabio J. ;

Koenen, Erik J. M. ;

Kovar, Lynsey ;

Lavin, Matt ;

le Roux, Marianne ;

Lewis, Gwilym P. ;

de Lima, Haroldo C. .

TAXON, 2017, 66 (01) :44-77

[7] The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution [J].

Badouin, Helene ;

Gouzy, Jerome ;

Grassa, Christopher J. ;

Murat, Florent ;

Staton, S. Evan ;

Cottret, Ludovic ;

Lelandais-Briere, Christine ;

Owens, Gregory L. ;

Carrere, Sebastien ;

Mayjonade, Baptiste ;

Legrand, Ludovic ;

Gill, Navdeep ;

Kane, Nolan C. ;

Bowers, John E. ;

Hubner, Sariel ;

Bellec, Arnaud ;

Berard, Aurelie ;

Berges, Helene ;

Blanchet, Nicolas ;

Boniface, Marie-Claude ;

Brunel, Dominique ;

Catrice, Olivier ;

Chaidir, Nadia ;

Claudel, Clotilde ;

Donnadieu, Cecile ;

Faraut, Thomas ;

Fievet, Ghislain ;

Helmstetter, Nicolas ;

King, Matthew ;

Knapp, Steven J. ;

Lai, Zhao ;

Le Paslier, Marie-Christine ;

Lippi, Yannick ;

Lorenzon, Lolita ;

Mandel, Jennifer R. ;

Marage, Gwenola ;

Marchand, Gwenaelle ;

Marquand, Elodie ;

Bret-Mestries, Emmanuelle ;

Morien, Evan ;

Nambeesan, Savithri ;

Thuy Nguyen ;

Pegot-Espagnet, Prune ;

Pouilly, Nicolas ;

Raftis, Frances ;

Sallet, Erika ;

Schiex, Thomas ;

Thomas, Justine ;

Vandecasteele, Celine ;

Vares, Didier .

NATURE, 2017, 546 (7656) :148-+

[8] Database Resources of the National Genomics Data Center, China National Center for Bioinformation in 2024 [J].

Bao, Yiming ;

Zhang, Zhang ;

Zhao, Wenming ;

Xiao, Jingfa ;

He, Shunmin ;

Zhang, Guoqing ;

Li, Yixue ;

Zhao, Guoping ;

Chen, Runsheng ;

Bu, Congfan ;

Zheng, Xinchang ;

Zhao, Xuetong ;

Xu, Tianyi ;

Bai, Xue ;

Jia, Yaokai ;

Chen, Meili ;

Hao, Lili ;

Tang, Bixia ;

Jin, Enhui ;

Zhao, Dongli ;

Wu, Gangao ;

Zhu, Junwei ;

Wang, Zhonghuang ;

Wei, Zhiyao ;

Zhang, Sisi ;

Wang, Anke ;

Chen, Xu ;

Sun, Yan-Ling ;

Zhang, Zhe ;

Meng, Yuanguang ;

Cao, Yongrong ;

Tian, Dongmei ;

Tang, Zhixin ;

Liu, Xiaonan ;

Hu, Weijuan ;

Song, Shuhui ;

Wang, Guoliang ;

Wu, Song ;

Xiong, Zhuang ;

Qu, Hongzhu ;

Fang, Xiangdong ;

Cao, Ruifang ;

Ling, Yunchao ;

Meng, Jiayue ;

He, Qinwen ;

Li, Cuidan ;

Qian, Qiheng ;

Yan, Cheng-hao ;

Lu, Mingming ;

Li, Pan .

NUCLEIC ACIDS RESEARCH, 2023, 52 (D1) :D18-D32

[9] The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut [J].

Bertioli, David John ;

Cannon, Steven B. ;

Froenicke, Lutz ;

Huang, Guodong ;

Farmer, Andrew D. ;

Cannon, Ethalinda K. S. ;

Liu, Xin ;

Gao, Dongying ;

Clevenger, Josh ;

Dash, Sudhansu ;

Ren, Longhui ;

Moretzsohn, Marcio C. ;

Shirasawa, Kenta ;

Huang, Wei ;

Vidigal, Bruna ;

Abernathy, Brian ;

Chu, Ye ;

Niederhuth, Chad E. ;

Umale, Pooja ;

Araujo, Ana Claudia G. ;

Kozik, Alexander ;

Do Kim, Kyung ;

Burow, Mark D. ;

Varshney, Rajeev K. ;

Wang, Xingjun ;

Zhang, Xinyou ;

Barkley, Noelle ;

Guimaraes, Patricia M. ;

Isobe, Sachiko ;

Guo, Baozhu ;

Liao, Boshou ;

Stalker, H. Thomas ;

Schmitz, Robert J. ;

Scheffler, Brian E. ;

Leal-Bertioli, Soraya C. M. ;

Xun, Xu ;

Jackson, Scott A. ;

Michelmore, Richard ;

Ozias-Akins, Peggy .

NATURE GENETICS, 2016, 48 (04) :438-+

[10] Trimmomatic: a flexible trimmer for Illumina sequence data [J].

Bolger, Anthony M. ;

Lohse, Marc ;

Usadel, Bjoern .

BIOINFORMATICS, 2014, 30 (15) :2114-2120

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