Sinorhizobium meliloti succinylated high-molecular-weight succinoglycan and the Medicago truncatula LysM receptor-like kinase MtLYK10 participate independently in symbiotic infection

Plant J. 2020 Apr;102(2):311-326. doi: 10.1111/tpj.14625. Epub 2020 Jan 11.

Abstract

The formation of nitrogen-fixing nodules on legume hosts is a finely tuned process involving many components of both symbiotic partners. Production of the exopolysaccharide succinoglycan by the nitrogen-fixing bacterium Sinorhizobium meliloti 1021 is needed for an effective symbiosis with Medicago spp., and the succinyl modification to this polysaccharide is critical. However, it is not known when succinoglycan intervenes in the symbiotic process, and it is not known whether the plant lysin-motif receptor-like kinase MtLYK10 intervenes in recognition of succinoglycan, as might be inferred from work on the Lotus japonicus MtLYK10 ortholog, LjEPR3. We studied the symbiotic infection phenotypes of S. meliloti mutants deficient in succinoglycan production or producing modified succinoglycan, in wild-type Medicago truncatula plants and in Mtlyk10 mutant plants. On wild-type plants, S. meliloti strains producing no succinoglycan or only unsuccinylated succinoglycan still induced nodule primordia and epidermal infections, but further progression of the symbiotic process was blocked. These S. meliloti mutants induced a more severe infection phenotype on Mtlyk10 mutant plants. Nodulation by succinoglycan-defective strains was achieved by in trans rescue with a Nod factor-deficient S. meliloti mutant. While the Nod factor-deficient strain was always more abundant inside nodules, the succinoglycan-deficient strain was more efficient than the strain producing only unsuccinylated succinoglycan. Together, these data show that succinylated succinoglycan is essential for infection thread formation in M. truncatula, and that MtLYK10 plays an important, but different role in this symbiotic process. These data also suggest that succinoglycan is more important than Nod factors for bacterial survival inside nodules.

Keywords: Medicago truncatula; Sinorhizobium meliloti; LysM-receptor-like kinase; beneficial microbes; exopolysaccharide; infection thread; microbiome; root hair; succinoglycan; symbiotic nitrogen fixation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Medicago truncatula / enzymology
  • Medicago truncatula / genetics
  • Medicago truncatula / microbiology*
  • Molecular Weight
  • Mutation
  • Nitrogen Fixation
  • Phenotype
  • Phosphotransferases / genetics
  • Phosphotransferases / metabolism
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Polysaccharides, Bacterial / genetics
  • Polysaccharides, Bacterial / metabolism*
  • Root Nodules, Plant / enzymology
  • Root Nodules, Plant / genetics
  • Root Nodules, Plant / microbiology
  • Sinorhizobium meliloti / genetics
  • Sinorhizobium meliloti / physiology*
  • Symbiosis*

Substances

  • Plant Proteins
  • Polysaccharides, Bacterial
  • succinoglycan
  • Phosphotransferases