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

Fabienne Maillet,Kirankumar S. Mysore,Jiangqi Wen,Kathryn M. Jones,Clare Gough,Million Tadege,Joëlle Fournier,Pascal Ratet,Hajeewaka C. Mendis

doi:10.1111/tpj.14625

Abstract

SummaryThe 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.

Highlights

Sinorhizobium meliloti 1021 is a nitrogen-fixing symbiont of the plants Medicago truncatula cv
We identified a M. truncatula mutant in MtLYK10, and determined how this line interacts with WT S. meliloti and S. meliloti mutants that are completely succinoglycan deficient, those that do not produce LMW succinoglycan and those that produce only unsuccinylated high molecular weight (HMW) succinoglycan
Our results suggest that S. meliloti succinoglycan has a function in infection of M. truncatula that is independent of LYK10, but is entirely dependent on succinylation of the polysaccharide

Summary

Introduction

Sinorhizobium meliloti 1021 is a nitrogen-fixing symbiont of the plants Medicago truncatula cv. On roots of compatible hosts, S. meliloti induces nodule organogenesis, and invades and colonizes the developing nodule primordia, being endocytosed by cells of the nodule cortex (Oldroyd et al, 2011). S. meliloti produces a lipo-chitooligosaccharide signal called Nod factor (NF) (Peters et al, 1986; Lerouge et al, 1990) responsible for inducing root hair curling around attached rhizobia. This traps S. meliloti microcolonies within an infection chamber (Fournier et al, 2015). Rhizobia access root cortical cell layers through structures called infection threads that initiate from the colonized curled root hairs (CCRHs). Infection threads extend through each successive cell layer until they reach the inner cortex, where bacteria are endocytosed by proliferating cells of the nodule primordium (Timmers et al, 1999; Xiao et al, 2014)

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Conclusion