Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility

Legume–rhizobium pairs are often observed that produce symbiotic root nodules but fail to fix nitrogen. Using the Sinorhizobium meliloti and Medicago truncatula symbiotic system, we previously described several naturally occurring accessory plasmids capable of disrupting the late stages of nodule de...

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Main Authors: Price, Paul A., Tanner, Houston R., Dillon, Brett A., Griffitts, Joel S., Shabab, Mohammed, Walker, Graham C.
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:en_US
Published: National Academy of Sciences (U.S.) 2017
Online Access:http://hdl.handle.net/1721.1/110516
https://orcid.org/0000-0002-3104-5856
https://orcid.org/0000-0001-7243-8261
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author Price, Paul A.
Tanner, Houston R.
Dillon, Brett A.
Griffitts, Joel S.
Shabab, Mohammed
Walker, Graham C.
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Price, Paul A.
Tanner, Houston R.
Dillon, Brett A.
Griffitts, Joel S.
Shabab, Mohammed
Walker, Graham C.
author_sort Price, Paul A.
collection MIT
description Legume–rhizobium pairs are often observed that produce symbiotic root nodules but fail to fix nitrogen. Using the Sinorhizobium meliloti and Medicago truncatula symbiotic system, we previously described several naturally occurring accessory plasmids capable of disrupting the late stages of nodule development while enhancing bacterial proliferation within the nodule. We report here that host range restriction peptidase (hrrP), a gene found on one of these plasmids, is capable of conferring both these properties. hrrP encodes an M16A family metallopeptidase whose catalytic activity is required for these symbiotic effects. The ability of hrrP to suppress nitrogen fixation is conditioned upon the genotypes of both the host plant and the hrrP-expressing rhizobial strain, suggesting its involvement in symbiotic communication. Purified HrrP protein is capable of degrading a range of nodule-specific cysteine-rich (NCR) peptides encoded by M. truncatula. NCR peptides are crucial signals used by M. truncatula for inducing and maintaining rhizobial differentiation within nodules, as demonstrated in the accompanying article [Horváth B, et al. (2015) Proc Natl Acad Sci USA, 10.1073/pnas.1500777112]. The expression pattern of hrrP and its effects on rhizobial morphology are consistent with the NCR peptide cleavage model. This work points to a symbiotic dialogue involving a complex ensemble of host-derived signaling peptides and bacterial modifier enzymes capable of adjusting signal strength, sometimes with exploitative outcomes.
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spelling mit-1721.1/1105162022-10-01T19:53:41Z Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility Price, Paul A. Tanner, Houston R. Dillon, Brett A. Griffitts, Joel S. Shabab, Mohammed Walker, Graham C. Massachusetts Institute of Technology. Department of Biology Shabab, Mohammed Walker, Graham C Legume–rhizobium pairs are often observed that produce symbiotic root nodules but fail to fix nitrogen. Using the Sinorhizobium meliloti and Medicago truncatula symbiotic system, we previously described several naturally occurring accessory plasmids capable of disrupting the late stages of nodule development while enhancing bacterial proliferation within the nodule. We report here that host range restriction peptidase (hrrP), a gene found on one of these plasmids, is capable of conferring both these properties. hrrP encodes an M16A family metallopeptidase whose catalytic activity is required for these symbiotic effects. The ability of hrrP to suppress nitrogen fixation is conditioned upon the genotypes of both the host plant and the hrrP-expressing rhizobial strain, suggesting its involvement in symbiotic communication. Purified HrrP protein is capable of degrading a range of nodule-specific cysteine-rich (NCR) peptides encoded by M. truncatula. NCR peptides are crucial signals used by M. truncatula for inducing and maintaining rhizobial differentiation within nodules, as demonstrated in the accompanying article [Horváth B, et al. (2015) Proc Natl Acad Sci USA, 10.1073/pnas.1500777112]. The expression pattern of hrrP and its effects on rhizobial morphology are consistent with the NCR peptide cleavage model. This work points to a symbiotic dialogue involving a complex ensemble of host-derived signaling peptides and bacterial modifier enzymes capable of adjusting signal strength, sometimes with exploitative outcomes. National Institutes of Health (U.S.) (GM31010) 2017-07-07T13:33:20Z 2017-07-07T13:33:20Z 2015-09 2014-09 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/110516 Price, Paul A.; Tanner, Houston R.; Dillon, Brett A.; Shabab, Mohammed; Walker, Graham C. and Griffitts, Joel S. “Rhizobial Peptidase HrrP Cleaves Host-Encoded Signaling Peptides and Mediates Symbiotic Compatibility.” Proceedings of the National Academy of Sciences 112, no. 49 (September 2015): 15244–15249 © 2015 National Academy of Sciences https://orcid.org/0000-0002-3104-5856 https://orcid.org/0000-0001-7243-8261 en_US http://dx.doi.org/10.1073/pnas.1417797112 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS
spellingShingle Price, Paul A.
Tanner, Houston R.
Dillon, Brett A.
Griffitts, Joel S.
Shabab, Mohammed
Walker, Graham C.
Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility
title Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility
title_full Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility
title_fullStr Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility
title_full_unstemmed Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility
title_short Rhizobial peptidase HrrP cleaves host-encoded signaling peptides and mediates symbiotic compatibility
title_sort rhizobial peptidase hrrp cleaves host encoded signaling peptides and mediates symbiotic compatibility
url http://hdl.handle.net/1721.1/110516
https://orcid.org/0000-0002-3104-5856
https://orcid.org/0000-0001-7243-8261
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