Rhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host Invasion

The genetic rules that dictate legume-rhizobium compatibility have been investigated for decades, but the causes of incompatibility occurring at late stages of the nodulation process are not well understood. An evaluation of naturally diverse legume (genus Medicago) and rhizobium (genus Sinorhizobiu...

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Main Authors: Matthew B. Crook, Daniel P. Lindsay, Matthew B. Biggs, Joshua S. Bentley, Jared C. Price, Spencer C. Clement, Mark J. Clement, Sharon R. Long, Joel S. Griffitts
Format: Article
Language:English
Published: The American Phytopathological Society 2012-08-01
Series:Molecular Plant-Microbe Interactions
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-02-12-0052-R
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author Matthew B. Crook
Daniel P. Lindsay
Matthew B. Biggs
Joshua S. Bentley
Jared C. Price
Spencer C. Clement
Mark J. Clement
Sharon R. Long
Joel S. Griffitts
author_facet Matthew B. Crook
Daniel P. Lindsay
Matthew B. Biggs
Joshua S. Bentley
Jared C. Price
Spencer C. Clement
Mark J. Clement
Sharon R. Long
Joel S. Griffitts
author_sort Matthew B. Crook
collection DOAJ
description The genetic rules that dictate legume-rhizobium compatibility have been investigated for decades, but the causes of incompatibility occurring at late stages of the nodulation process are not well understood. An evaluation of naturally diverse legume (genus Medicago) and rhizobium (genus Sinorhizobium) isolates has revealed numerous instances in which Sinorhizobium strains induce and occupy nodules that are only minimally beneficial to certain Medicago hosts. Using these ineffective strain-host pairs, we identified gain-of-compatibility (GOC) rhizobial variants. We show that GOC variants arise by loss of specific large accessory plasmids, which we call HR plasmids due to their effect on symbiotic host range. Transfer of HR plasmids to a symbiotically effective rhizobium strain can convert it to incompatibility, indicating that HR plasmids can act autonomously in diverse strain backgrounds. We provide evidence that HR plasmids may encode machinery for their horizontal transfer. On hosts in which HR plasmids impair N fixation, the plasmids also enhance competitiveness for nodule occupancy, showing that naturally occurring, transferrable accessory genes can convert beneficial rhizobia to a more exploitative lifestyle. This observation raises important questions about agricultural management, the ecological stability of mutualisms, and the genetic factors that distinguish beneficial symbionts from parasites.
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spelling doaj.art-4c0b45ae19a447e79bfa6b7159dcd7fd2022-12-22T03:18:24ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062012-08-012581026103310.1094/MPMI-02-12-0052-RRhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host InvasionMatthew B. CrookDaniel P. LindsayMatthew B. BiggsJoshua S. BentleyJared C. PriceSpencer C. ClementMark J. ClementSharon R. LongJoel S. GriffittsThe genetic rules that dictate legume-rhizobium compatibility have been investigated for decades, but the causes of incompatibility occurring at late stages of the nodulation process are not well understood. An evaluation of naturally diverse legume (genus Medicago) and rhizobium (genus Sinorhizobium) isolates has revealed numerous instances in which Sinorhizobium strains induce and occupy nodules that are only minimally beneficial to certain Medicago hosts. Using these ineffective strain-host pairs, we identified gain-of-compatibility (GOC) rhizobial variants. We show that GOC variants arise by loss of specific large accessory plasmids, which we call HR plasmids due to their effect on symbiotic host range. Transfer of HR plasmids to a symbiotically effective rhizobium strain can convert it to incompatibility, indicating that HR plasmids can act autonomously in diverse strain backgrounds. We provide evidence that HR plasmids may encode machinery for their horizontal transfer. On hosts in which HR plasmids impair N fixation, the plasmids also enhance competitiveness for nodule occupancy, showing that naturally occurring, transferrable accessory genes can convert beneficial rhizobia to a more exploitative lifestyle. This observation raises important questions about agricultural management, the ecological stability of mutualisms, and the genetic factors that distinguish beneficial symbionts from parasites.https://apsjournals.apsnet.org/doi/10.1094/MPMI-02-12-0052-R
spellingShingle Matthew B. Crook
Daniel P. Lindsay
Matthew B. Biggs
Joshua S. Bentley
Jared C. Price
Spencer C. Clement
Mark J. Clement
Sharon R. Long
Joel S. Griffitts
Rhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host Invasion
Molecular Plant-Microbe Interactions
title Rhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host Invasion
title_full Rhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host Invasion
title_fullStr Rhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host Invasion
title_full_unstemmed Rhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host Invasion
title_short Rhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host Invasion
title_sort rhizobial plasmids that cause impaired symbiotic nitrogen fixation and enhanced host invasion
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-02-12-0052-R
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