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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Format: | Article |
Language: | English |
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The American Phytopathological Society
2012-08-01
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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. |
first_indexed | 2024-04-12T20:05:35Z |
format | Article |
id | doaj.art-4c0b45ae19a447e79bfa6b7159dcd7fd |
institution | Directory Open Access Journal |
issn | 0894-0282 1943-7706 |
language | English |
last_indexed | 2024-04-12T20:05:35Z |
publishDate | 2012-08-01 |
publisher | The American Phytopathological Society |
record_format | Article |
series | Molecular Plant-Microbe Interactions |
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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