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Title: Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight

Abstract

The acidic polysaccharide succinoglycan produced by the rhizobial symbiont Sinorhizobium meliloti 1021 is required for this bacterium to invade the host plant Medicago truncatula and establish a nitrogen-fixing symbiosis. S. meliloti mutants that cannot make succinoglycan cannot initiate invasion structures called infection threads in plant root hairs. S. meliloti exoH mutants that cannot succinylate succinoglycan are also unable to form infection threads, despite the fact that they make large quantities of succinoglycan. Succinoglycan produced by exoH mutants is refractory to cleavage by the glycanases encoded by exoK and exsH, and thus succinoglycan produced by exoH mutants is made only in the high-molecular-weight (HMW) form. One interpretation of the symbiotic defect of exoH mutants is that the low-molecular-weight (LMW) form of succinoglycan is required for infection thread formation. However, our data demonstrate that production of the HMW form of succinoglycan by S. meliloti 1021 is sufficient for invasion of the host M. truncatula and that the LMW form is not required. Here, we show that S. meliloti strains deficient in the exoK- and exsH-encoded glycanases invade M. truncatula and form a productive symbiosis, although they do this with somewhat less efficiency than the wild type. We have also characterized the polysaccharidesmore » produced by these double glycanase mutants and determined that they consist of only HMW succinoglycan and no detectable LMW succinoglycan. This demonstrates that LMW succinoglycan is not required for host invasion. These results suggest succinoglycan function is not dependent upon the presence of a small, readily diffusible form.« less

Authors:
 [1];  [1];  [1];  [1]
  1. Florida State Univ., Tallahassee, FL (United States). Dept. of Biological Science
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; USDA
OSTI Identifier:
1626114
Grant/Contract Number:  
FG02-93ER20097; 2014-67013-21579
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 7; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology

Citation Formats

Mendis, Hajeewaka C., Madzima, Thelma F., Queiroux, Clothilde, and Jones, Kathryn M. Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight. United States: N. p., 2016. Web. doi:10.1128/mbio.00606-16.
Mendis, Hajeewaka C., Madzima, Thelma F., Queiroux, Clothilde, & Jones, Kathryn M. Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight. United States. https://doi.org/10.1128/mbio.00606-16
Mendis, Hajeewaka C., Madzima, Thelma F., Queiroux, Clothilde, and Jones, Kathryn M. Tue . "Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight". United States. https://doi.org/10.1128/mbio.00606-16. https://www.osti.gov/servlets/purl/1626114.
@article{osti_1626114,
title = {Function of Succinoglycan Polysaccharide in Sinorhizobium meliloti Host Plant Invasion Depends on Succinylation, Not Molecular Weight},
author = {Mendis, Hajeewaka C. and Madzima, Thelma F. and Queiroux, Clothilde and Jones, Kathryn M.},
abstractNote = {The acidic polysaccharide succinoglycan produced by the rhizobial symbiont Sinorhizobium meliloti 1021 is required for this bacterium to invade the host plant Medicago truncatula and establish a nitrogen-fixing symbiosis. S. meliloti mutants that cannot make succinoglycan cannot initiate invasion structures called infection threads in plant root hairs. S. meliloti exoH mutants that cannot succinylate succinoglycan are also unable to form infection threads, despite the fact that they make large quantities of succinoglycan. Succinoglycan produced by exoH mutants is refractory to cleavage by the glycanases encoded by exoK and exsH, and thus succinoglycan produced by exoH mutants is made only in the high-molecular-weight (HMW) form. One interpretation of the symbiotic defect of exoH mutants is that the low-molecular-weight (LMW) form of succinoglycan is required for infection thread formation. However, our data demonstrate that production of the HMW form of succinoglycan by S. meliloti 1021 is sufficient for invasion of the host M. truncatula and that the LMW form is not required. Here, we show that S. meliloti strains deficient in the exoK- and exsH-encoded glycanases invade M. truncatula and form a productive symbiosis, although they do this with somewhat less efficiency than the wild type. We have also characterized the polysaccharides produced by these double glycanase mutants and determined that they consist of only HMW succinoglycan and no detectable LMW succinoglycan. This demonstrates that LMW succinoglycan is not required for host invasion. These results suggest succinoglycan function is not dependent upon the presence of a small, readily diffusible form.},
doi = {10.1128/mbio.00606-16},
journal = {mBio (Online)},
number = 3,
volume = 7,
place = {United States},
year = {Tue Jun 21 00:00:00 EDT 2016},
month = {Tue Jun 21 00:00:00 EDT 2016}
}

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Works referenced in this record:

Water Relations in the Interaction of Foliar Bacterial Pathogens with Plants
journal, September 2011


A second exopolysaccharide of Rhizobium meliloti strain SU47 that can function in root nodule invasion.
journal, May 1989

  • Zhan, H. J.; Levery, S. B.; Lee, C. C.
  • Proceedings of the National Academy of Sciences, Vol. 86, Issue 9
  • DOI: 10.1073/pnas.86.9.3055

The acetyl substituent of succinoglycan is not necessary for alfalfa nodule invasion by Rhizobium meliloti Rm1021.
journal, January 1993


Receptor-mediated exopolysaccharide perception controls bacterial infection
journal, July 2015

  • Kawaharada, Y.; Kelly, S.; Nielsen, M. Wibroe
  • Nature, Vol. 523, Issue 7560
  • DOI: 10.1038/nature14611

A LuxR Homolog Controls Production of Symbiotically Active Extracellular Polysaccharide II by Sinorhizobium meliloti
journal, September 2002


Structure of the extracellular polysaccharide secreted by Rhizobium leguminosarum var. phaseoli CIAT 899
journal, September 1990


Growth of the plant cell wall
journal, November 2005

  • Cosgrove, Daniel J.
  • Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861
  • DOI: 10.1038/nrm1746

Suppression of the Fix- phenotype of Rhizobium meliloti exoB mutants by lpsZ is correlated to a modified expression of the K polysaccharide.
journal, January 1995


Rhizobium meliloti mutants that fail to succinylate their Calcofluor-binding exopolysaccharide are defective in nodule invasion
journal, November 1987


The Rhizobium meliloti ExoK and ExsH glycanases specifically depolymerize nascent succinoglycan chains
journal, April 1998

  • York, G. M.; Walker, G. C.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 9
  • DOI: 10.1073/pnas.95.9.4912

Exo-Oligosaccharides of Rhizobium sp. Strain NGR234 Are Required for Symbiosis with Various Legumes
journal, September 2006

  • Staehelin, Christian; Forsberg, Lennart S.; D'Haeze, Wim
  • Journal of Bacteriology, Vol. 188, Issue 17
  • DOI: 10.1128/JB.00365-06

Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules.
journal, January 1988


Proteolysis during Development and Senescence of Effective and Plant Gene-Controlled Ineffective Alfalfa Nodules
journal, October 1993


Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae
journal, August 1999


Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm1021.
journal, January 1994


Defective Infection and Nodulation of Clovers by Exopolysaccharide Mutants of Rhizobium leguminosarum bv. trifolii
journal, January 1996

  • Rolfe, Bg; Carlson, Rw; Ridge, Rw
  • Functional Plant Biology, Vol. 23, Issue 3
  • DOI: 10.1071/PP9960285

Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules.
journal, September 1985

  • Leigh, J. A.; Signer, E. R.; Walker, G. C.
  • Proceedings of the National Academy of Sciences, Vol. 82, Issue 18
  • DOI: 10.1073/pnas.82.18.6231

Ethylene Prevents Nodulation of Vicia sativas sp. nigra by Exopolysaccharide-Deficient Mutants of Rhizobium leguminosarum bv. Viciae
journal, January 1995

  • van Workum, Wilbert A. T.
  • Molecular Plant-Microbe Interactions, Vol. 8, Issue 2
  • DOI: 10.1094/MPMI-8-0278

Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa.
journal, June 1992

  • Battisti, L.; Lara, J. C.; Leigh, J. A.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 12
  • DOI: 10.1073/pnas.89.12.5625

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model
journal, August 2007

  • Jones, Kathryn M.; Kobayashi, Hajime; Davies, Bryan W.
  • Nature Reviews Microbiology, Vol. 5, Issue 8
  • DOI: 10.1038/nrmicro1705

Plant Cell Wall Remodelling in the Rhizobium–Legume Symbiosis
journal, July 2004


Biosynthetic control of molecular weight in the polymerization of the octasaccharide subunits of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti
journal, November 1998

  • Gonzalez, J. E.; Semino, C. E.; Wang, L. -X.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 23
  • DOI: 10.1073/pnas.95.23.13477

Family of glycosyl transferases needed for the synthesis of succinoglycan by Rhizobium meliloti.
journal, January 1993


Fate map of Medicago truncatula root nodules
journal, September 2014

  • Xiao, T. T.; Schilderink, S.; Moling, S.
  • Development, Vol. 141, Issue 18
  • DOI: 10.1242/dev.110775

Single-plant, Sterile Microcosms for Nodulation and Growth of the Legume Plant Medicago truncatula with the Rhizobial Symbiont Sinorhizobium meliloti
journal, January 2013

  • Jones, Kathryn M.; Mendis, Hajeewaka C.; Queiroux, Clothilde
  • Journal of Visualized Experiments, Issue 80
  • DOI: 10.3791/50916

Genetic analysis of a cluster of genes required for synthesis of the calcofluor-binding exopolysaccharide of Rhizobium meliloti.
journal, January 1988


Cyclic beta-glucans of members of the family Rhizobiaceae
journal, June 1994


Cyclic beta-glucans of members of the family Rhizobiaceae.
journal, January 1994


Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant
journal, January 2008

  • Jones, K. M.; Sharopova, N.; Lohar, D. P.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 2
  • DOI: 10.1073/pnas.0709338105

The Rules of Engagement in the Legume-Rhizobial Symbiosis
journal, December 2011


Bacterial Polysaccharides Suppress Induced Innate Immunity by Calcium Chelation
journal, July 2008


A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes
journal, August 1986


Exogenous suppression of the symbiotic deficiencies of Rhizobium meliloti exo mutants.
journal, January 1992


General transduction in Rhizobium meliloti.
journal, January 1984


Rhizobium meliloti exoG and exoJ mutations affect the exoX-exoY system for modulation of exopolysaccharide production.
journal, January 1991


A comparative genomics screen identifies a Sinorhizobium meliloti 1021 sodM-like gene strongly expressed within host plant nodules
journal, January 2012

  • Queiroux, Clothilde; Washburn, Brian K.; Davis, Olivia M.
  • BMC Microbiology, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2180-12-74

Environmental Regulation of Exopolysaccharide Production in Sinorhizobium meliloti
journal, February 2000


Xanthan Induces Plant Susceptibility by Suppressing Callose Deposition
journal, March 2006

  • Yun, Maximina H.; Torres, Pablo S.; Oirdi, Mohamed El
  • Plant Physiology, Vol. 141, Issue 1
  • DOI: 10.1104/pp.105.074542

Structural studies of a novel exopolysaccharide produced by a mutant of Rhizobium meliloti strain Rm1021
journal, May 1990


Rhizobium meliloti mutants that fail to succinylate their Calcofluor-binding exopolysaccharide are defective in nodule invasion
journal, November 1987


Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti
journal, July 1993


Bacterial Polysaccharides Suppress Induced Innate Immunity by Calcium Chelation
journal, July 2008


Effect of o-acyl substituents on the functional behaviour of Rhizobium meliloti succinoglycan
journal, February 1997

  • Ridout, M. J.; Brownsey, G. J.; York, G. M.
  • International Journal of Biological Macromolecules, Vol. 20, Issue 1
  • DOI: 10.1016/s0141-8130(96)01140-3

Two Types of Nodules Induced on Trifolium pratense by Mutants of Rhizobium leguminosarum bv. trifolii deficient in Exopolysaccharide Production
journal, January 1995

  • Skorupska, Anna; Białek, Urszula; Urbanik-Sypniewska, Teresa
  • Journal of Plant Physiology, Vol. 147, Issue 1
  • DOI: 10.1016/s0176-1617(11)81419-7

Growth of the plant cell wall
journal, November 2005

  • Cosgrove, Daniel J.
  • Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861
  • DOI: 10.1038/nrm1746

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model
journal, August 2007

  • Jones, Kathryn M.; Kobayashi, Hajime; Davies, Bryan W.
  • Nature Reviews Microbiology, Vol. 5, Issue 8
  • DOI: 10.1038/nrmicro1705

Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae
journal, August 1999


Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction
journal, September 1993


Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant
journal, January 2008

  • Jones, K. M.; Sharopova, N.; Lohar, D. P.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 2
  • DOI: 10.1073/pnas.0709338105

Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules.
journal, September 1985

  • Leigh, J. A.; Signer, E. R.; Walker, G. C.
  • Proceedings of the National Academy of Sciences, Vol. 82, Issue 18
  • DOI: 10.1073/pnas.82.18.6231

Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa.
journal, June 1992

  • Battisti, L.; Lara, J. C.; Leigh, J. A.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 12
  • DOI: 10.1073/pnas.89.12.5625

Plant Cell Wall Remodelling in the Rhizobium–Legume Symbiosis
journal, July 2004


The Succinoglycan Endoglycanase Encoded by exoK Is Required for Efficient Symbiosis of Sinorhizobium meliloti 1021 with the Host Plants Medicago truncatula and Medicago sativa (Alfalfa)
journal, September 2013

  • Mendis, Hajeewaka C.; Queiroux, Clothilde; Brewer, Tess E.
  • Molecular Plant-Microbe Interactions®, Vol. 26, Issue 9
  • DOI: 10.1094/mpmi-03-13-0087-r

Exopolysaccharide Production in Response to Medium Acidification Is Correlated With an Increase in Competition for Nodule Occupancy
journal, December 2014

  • Geddes, Barney A.; González, Juan E.; Oresnik, Ivan J.
  • Molecular Plant-Microbe Interactions®, Vol. 27, Issue 12
  • DOI: 10.1094/mpmi-06-14-0168-r

Conditional Requirement for Exopolysaccharide in the Mesorhizobium–Lotus Symbiosis
journal, March 2013

  • Kelly, Simon J.; Muszyński, Artur; Kawaharada, Yasuyuki
  • Molecular Plant-Microbe Interactions, Vol. 26, Issue 3
  • DOI: 10.1094/mpmi-09-12-0227-r

Exopolysaccharide Structure Is Not a Determinant of Host-Plant Specificity in Nodulation of Vicia sativa Roots
journal, November 2005

  • Laus, Marc C.; van Brussel, Anton A. N.; Kijne, Jan W.
  • Molecular Plant-Microbe Interactions®, Vol. 18, Issue 11
  • DOI: 10.1094/mpmi-18-1123

Proteolysis during Development and Senescence of Effective and Plant Gene-Controlled Ineffective Alfalfa Nodules
journal, October 1993


A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes
journal, August 1986


Structural Analysis of Succinoglycan Oligosaccharides from Sinorhizobium meliloti Strains with Different Host Compatibility Phenotypes
journal, March 2013

  • Simsek, S.; Wood, K.; Reuhs, B. L.
  • Journal of Bacteriology, Vol. 195, Issue 9
  • DOI: 10.1128/jb.00009-13

Exopolysaccharides from Sinorhizobium meliloti Can Protect against H2O2-Dependent Damage
journal, September 2013

  • Lehman, A. P.; Long, S. R.
  • Journal of Bacteriology, Vol. 195, Issue 23
  • DOI: 10.1128/jb.00681-13

Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules.
journal, January 1988


Genetic analysis of a cluster of genes required for synthesis of the calcofluor-binding exopolysaccharide of Rhizobium meliloti.
journal, January 1988


Rhizobium meliloti exoG and exoJ mutations affect the exoX-exoY system for modulation of exopolysaccharide production.
journal, January 1991


Exogenous suppression of the symbiotic deficiencies of Rhizobium meliloti exo mutants.
journal, January 1992


Family of glycosyl transferases needed for the synthesis of succinoglycan by Rhizobium meliloti.
journal, January 1993


Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm1021.
journal, January 1994


Structural Characterization of the Symbiotically Important Low-Molecular-Weight Succinoglycan ofSinorhizobium meliloti
journal, November 1999


Alfalfa Root Nodule Invasion Efficiency Is Dependent on Sinorhizobium melilotiPolysaccharides
journal, August 2000


Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes
journal, June 2004


Cyclic beta-glucans of members of the family Rhizobiaceae
journal, June 1994


The Rules of Engagement in the Legume-Rhizobial Symbiosis
journal, December 2011


Water Relations in the Interaction of Foliar Bacterial Pathogens with Plants
journal, September 2011


A comparative genomics screen identifies a Sinorhizobium meliloti 1021 sodM-like gene strongly expressed within host plant nodules
journal, January 2012

  • Queiroux, Clothilde; Washburn, Brian K.; Davis, Olivia M.
  • BMC Microbiology, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2180-12-74

Fate map of Medicago truncatula root nodules
journal, September 2014

  • Xiao, T. T.; Schilderink, S.; Moling, S.
  • Development, Vol. 141, Issue 18
  • DOI: 10.1242/dev.110775

Single-plant, Sterile Microcosms for Nodulation and Growth of the Legume Plant Medicago truncatula with the Rhizobial Symbiont Sinorhizobium meliloti
journal, October 2013

  • Jones, Kathryn M.; Mendis, Hajeewaka C.; Queiroux, Clothilde
  • Journal of Visualized Experiments, Issue 80
  • DOI: 10.3791/50916-v

Works referencing / citing this record:

Important Late-Stage Symbiotic Role of the Sinorhizobium meliloti Exopolysaccharide Succinoglycan
journal, April 2018

  • Arnold, Markus F. F.; Penterman, Jon; Shabab, Mohammed
  • Journal of Bacteriology, Vol. 200, Issue 13
  • DOI: 10.1128/jb.00665-17

Reports from a Healthy Community: the 7th Conference on Beneficial Microbes
journal, December 2018

  • Mandel, Mark J.; Broderick, Nichole A.; Martens, Eric C.
  • Applied and Environmental Microbiology, Vol. 85, Issue 10
  • DOI: 10.1128/aem.02562-18

Surface Properties of Wild-Type Rhizobium leguminosarum bv. trifolii Strain 24.2 and Its Derivatives with Different Extracellular Polysaccharide Content
journal, October 2016


Synthesis of Rhizobial Exopolysaccharides and Their Importance for Symbiosis with Legume Plants
journal, December 2017

  • Marczak, Małgorzata; Mazur, Andrzej; Koper, Piotr
  • Genes, Vol. 8, Issue 12
  • DOI: 10.3390/genes8120360