Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula

Qi Wang, Shengming Yang, Jinge Liu, Kata Terecskei, Edit Abrahám, Anikó Gombár, Agota Domonkos, A. Szűcs, Péter Körmöczi, Ting Wang, Lili Fodor, Linyong Mao, Zhangjun Fei, É. Kondorosi, P. Kaló, A. Kereszt, Hongyan Zhu

Research output: Article

36 Citations (Scopus)

Abstract

Legumes engage in root nodule symbioses with nitrogen-fixing soil bacteria known as rhizobia. In nodule cells, bacteria are enclosed in membrane-bound vesicles called symbiosomes and differentiate into bacteroids that are capable of converting atmospheric nitrogen into ammonia. Bacteroid differentiation and prolonged intracellular survival are essential for development of functional nodules. However, in the Medicago truncatula-Sinorhizobium meliloti symbiosis, incompatibility between symbiotic partners frequently occurs, leading to the formation of infected nodules defective in nitrogen fixation (Fix-). Here, we report the identification and cloning of the M. truncatula NFS2 gene that regulates this type of specificity pertaining to S. meliloti strain Rm41. We demonstrate that NFS2 encodes a nodule-specific cysteine-rich (NCR) peptide that acts to promote bacterial lysis after differentiation. The negative role of NFS2 in symbiosis is contingent on host genetic background and can be counteracted by other genes encoded by the host. This work extends the paradigm of NCR function to include the negative regulation of symbiotic persistence in host-strain interactions. Our data suggest that NCR peptides are host determinants of symbiotic specificity in M. truncatula and possibly in closely related legumes that form indeterminate nodules in which bacterial symbionts undergo terminal differentiation.

Original languageEnglish
Pages (from-to)6854-6859
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number26
DOIs
Publication statusPublished - jún. 27 2017

Fingerprint

Medicago truncatula
Symbiosis
Sinorhizobium meliloti
Cysteine
Fabaceae
Peptides
Nitrogen Fixation
Rhizobium
Ammonia
Genes
Organism Cloning
Nitrogen
Soil
Bacteria
Membranes

ASJC Scopus subject areas

  • General

Cite this

Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula. / Wang, Qi; Yang, Shengming; Liu, Jinge; Terecskei, Kata; Abrahám, Edit; Gombár, Anikó; Domonkos, Agota; Szűcs, A.; Körmöczi, Péter; Wang, Ting; Fodor, Lili; Mao, Linyong; Fei, Zhangjun; Kondorosi, É.; Kaló, P.; Kereszt, A.; Zhu, Hongyan.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 26, 27.06.2017, p. 6854-6859.

Research output: Article

Wang, Q, Yang, S, Liu, J, Terecskei, K, Abrahám, E, Gombár, A, Domonkos, A, Szűcs, A, Körmöczi, P, Wang, T, Fodor, L, Mao, L, Fei, Z, Kondorosi, É, Kaló, P, Kereszt, A & Zhu, H 2017, 'Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula', Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 26, pp. 6854-6859. https://doi.org/10.1073/pnas.1700715114
Wang, Qi ; Yang, Shengming ; Liu, Jinge ; Terecskei, Kata ; Abrahám, Edit ; Gombár, Anikó ; Domonkos, Agota ; Szűcs, A. ; Körmöczi, Péter ; Wang, Ting ; Fodor, Lili ; Mao, Linyong ; Fei, Zhangjun ; Kondorosi, É. ; Kaló, P. ; Kereszt, A. ; Zhu, Hongyan. / Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 26. pp. 6854-6859.
@article{22a0bf5fec39422f9c423d93c77a53dd,
title = "Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula",
abstract = "Legumes engage in root nodule symbioses with nitrogen-fixing soil bacteria known as rhizobia. In nodule cells, bacteria are enclosed in membrane-bound vesicles called symbiosomes and differentiate into bacteroids that are capable of converting atmospheric nitrogen into ammonia. Bacteroid differentiation and prolonged intracellular survival are essential for development of functional nodules. However, in the Medicago truncatula-Sinorhizobium meliloti symbiosis, incompatibility between symbiotic partners frequently occurs, leading to the formation of infected nodules defective in nitrogen fixation (Fix-). Here, we report the identification and cloning of the M. truncatula NFS2 gene that regulates this type of specificity pertaining to S. meliloti strain Rm41. We demonstrate that NFS2 encodes a nodule-specific cysteine-rich (NCR) peptide that acts to promote bacterial lysis after differentiation. The negative role of NFS2 in symbiosis is contingent on host genetic background and can be counteracted by other genes encoded by the host. This work extends the paradigm of NCR function to include the negative regulation of symbiotic persistence in host-strain interactions. Our data suggest that NCR peptides are host determinants of symbiotic specificity in M. truncatula and possibly in closely related legumes that form indeterminate nodules in which bacterial symbionts undergo terminal differentiation.",
keywords = "Legumes, NCR peptides, Nitrogen fixation, Rhizobial symbiosis, Symbiotic specificity",
author = "Qi Wang and Shengming Yang and Jinge Liu and Kata Terecskei and Edit Abrah{\'a}m and Anik{\'o} Gomb{\'a}r and Agota Domonkos and A. Szűcs and P{\'e}ter K{\"o}rm{\"o}czi and Ting Wang and Lili Fodor and Linyong Mao and Zhangjun Fei and {\'E}. Kondorosi and P. Kal{\'o} and A. Kereszt and Hongyan Zhu",
year = "2017",
month = "6",
day = "27",
doi = "10.1073/pnas.1700715114",
language = "English",
volume = "114",
pages = "6854--6859",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "26",

}

TY - JOUR

T1 - Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula

AU - Wang, Qi

AU - Yang, Shengming

AU - Liu, Jinge

AU - Terecskei, Kata

AU - Abrahám, Edit

AU - Gombár, Anikó

AU - Domonkos, Agota

AU - Szűcs, A.

AU - Körmöczi, Péter

AU - Wang, Ting

AU - Fodor, Lili

AU - Mao, Linyong

AU - Fei, Zhangjun

AU - Kondorosi, É.

AU - Kaló, P.

AU - Kereszt, A.

AU - Zhu, Hongyan

PY - 2017/6/27

Y1 - 2017/6/27

N2 - Legumes engage in root nodule symbioses with nitrogen-fixing soil bacteria known as rhizobia. In nodule cells, bacteria are enclosed in membrane-bound vesicles called symbiosomes and differentiate into bacteroids that are capable of converting atmospheric nitrogen into ammonia. Bacteroid differentiation and prolonged intracellular survival are essential for development of functional nodules. However, in the Medicago truncatula-Sinorhizobium meliloti symbiosis, incompatibility between symbiotic partners frequently occurs, leading to the formation of infected nodules defective in nitrogen fixation (Fix-). Here, we report the identification and cloning of the M. truncatula NFS2 gene that regulates this type of specificity pertaining to S. meliloti strain Rm41. We demonstrate that NFS2 encodes a nodule-specific cysteine-rich (NCR) peptide that acts to promote bacterial lysis after differentiation. The negative role of NFS2 in symbiosis is contingent on host genetic background and can be counteracted by other genes encoded by the host. This work extends the paradigm of NCR function to include the negative regulation of symbiotic persistence in host-strain interactions. Our data suggest that NCR peptides are host determinants of symbiotic specificity in M. truncatula and possibly in closely related legumes that form indeterminate nodules in which bacterial symbionts undergo terminal differentiation.

AB - Legumes engage in root nodule symbioses with nitrogen-fixing soil bacteria known as rhizobia. In nodule cells, bacteria are enclosed in membrane-bound vesicles called symbiosomes and differentiate into bacteroids that are capable of converting atmospheric nitrogen into ammonia. Bacteroid differentiation and prolonged intracellular survival are essential for development of functional nodules. However, in the Medicago truncatula-Sinorhizobium meliloti symbiosis, incompatibility between symbiotic partners frequently occurs, leading to the formation of infected nodules defective in nitrogen fixation (Fix-). Here, we report the identification and cloning of the M. truncatula NFS2 gene that regulates this type of specificity pertaining to S. meliloti strain Rm41. We demonstrate that NFS2 encodes a nodule-specific cysteine-rich (NCR) peptide that acts to promote bacterial lysis after differentiation. The negative role of NFS2 in symbiosis is contingent on host genetic background and can be counteracted by other genes encoded by the host. This work extends the paradigm of NCR function to include the negative regulation of symbiotic persistence in host-strain interactions. Our data suggest that NCR peptides are host determinants of symbiotic specificity in M. truncatula and possibly in closely related legumes that form indeterminate nodules in which bacterial symbionts undergo terminal differentiation.

KW - Legumes

KW - NCR peptides

KW - Nitrogen fixation

KW - Rhizobial symbiosis

KW - Symbiotic specificity

UR - http://www.scopus.com/inward/record.url?scp=85021390777&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85021390777&partnerID=8YFLogxK

U2 - 10.1073/pnas.1700715114

DO - 10.1073/pnas.1700715114

M3 - Article

C2 - 28607058

AN - SCOPUS:85021390777

VL - 114

SP - 6854

EP - 6859

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 26

ER -