Salt stress enhances early symbiotic gene expression in Medicago truncatula and induces a stress-specific set of rhizobium-responsive genes

Sanhita Chakraborty, Heather E. Driscoll, Juan E. Abrahante, Fan Zhang, Robert F. Fisher, Jeanne M. Harris

Research output: Contribution to journalArticlepeer-review

Abstract

Salt stress is a major agricultural concern inhibiting not only plant growth but also the symbiotic association between legume roots and the soil bacteria rhizobia. This symbiotic association is initiated by a molecular dialogue between the two partners, leading to the activation of a signaling cascade in the legume host and, ultimately, the formation of nitrogen-fixing root nodules. Here, we show that a moderate salt stress increases the responsiveness of early symbiotic genes in Medicago truncatula to its symbiotic partner, Sinorhizobium meliloti while, conversely, inoculation with S. meliloti counteracts salt-regulated gene expression, restoring one-third to control levels. Our analysis of early nodulin 11 ( ENOD11) shows that salt-induced expression is dynamic, Nod-factor dependent, and requires the ionic but not the osmotic component of salt. We demonstrate that salt stimulation of rhizobium-induced gene expression requires NSP2, which functions as a node to integrate the abiotic and biotic signals. In addition, our work reveals that inoculation with S. meliloti succinoglycan mutants also hyperinduces ENOD11 expression in the presence or absence of salt, suggesting a possible link between rhizobial exopolysaccharide and the plant response to salt stress. Finally, we identify an accessory set of genes that are induced by rhizobium only under conditions of salt stress and have not been previously identified as being nodulation-related genes. Our data suggest that interplay of core nodulation genes with different accessory sets, specific for different abiotic conditions, functions to establish the symbiosis. Together, our findings reveal a complex and dynamic interaction between plant, microbe, and environment.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Original languageEnglish (US)
JournalMolecular Plant-Microbe Interactions
Volume34
Issue number8
DOIs
StateE-pub ahead of print - Sep 8 2021

Bibliographical note

Funding Information:
Support was provided by Gene Ontology, the National Institute of General Medical Sciences (grants GM093628 and P20GM103449), and Hatch (grant VT-H02104); and Kyoto Encyclopedia of Genes and Genomes pathway analyses were supported by the Vermont Biomedical Research Network (VBRN) Bioinformatics Core. We thank S. Long (Stanford University) for providing the rhizobial strains SL44 and Rm7210; M. Arnold and G. Walker (Massachusetts Institute of Technology) for providing the strain Rm7096; A. Becker (University of Minnesota Genomics Center) for generating the RNA-seq libraries; T. Delaney, S. Keller, J. Preston, and M. Tierney (University of Vermont) for their advice and generosity with the use of equipment; University of Vermont Advanced Genome Technologies Core for help with RNA quality assessment; J.-M. Ane (University of Wisconsin-Madison) for critical reading of the manuscript; A. Howard for statistical advice; and members of the Harris lab for suggestions and support.

Funding Information:
Funding: Support was provided by Gene Ontology, the National Institute of General Medical Sciences (grants GM093628 and P20GM103449), and Hatch (grant VT-H02104); and Kyoto Encyclopedia of Genes and Genomes pathway analyses were supported by the Vermont Biomedical Research Network (VBRN) Bioinformatics Core.

Publisher Copyright:
© 2021 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Keywords

  • ENOD11
  • Exopolysaccharides
  • ExoS
  • ExoY
  • Hyperinduction
  • Infection
  • Medicago truncatula
  • Nitrogen-fixation
  • NPL
  • NSP2
  • Priming
  • RNA-seq
  • Root nodules
  • Salt stress
  • Sinorhizobium meliloti
  • Succinoglycan
  • Symbiosis

PubMed: MeSH publication types

  • Journal Article

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