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

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.

Structural signatures in EPR3 define a unique class of plant carbohydrate receptors

“…Monomeric octasaccharides (R7A EPS) 10 are recognised through direct binding to EPR3 1 . Studies of rhizobia and host plant mutants show that EPS perception and subsequent EPR3 signalling promotes infection of the epidermal and cortical tissues of Lotus and Medicago roots 1,5,11 . In contrast, truncated EPS produced by the exoU mutant strain (R7A exoU EPS) blocks rhizobial infection and colonisation in an EPR3-dependent manner, suggesting that the perception of EPS is an additional compatibility-determining step in legume-rhizobia interactions 1,6 .…”

The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infection

“…The fact that Mtnf-ya1 roots–but not exoY- nodulated M . truncatula roots [ 47 ]- are hyper-infected [ 35 ] also support this conclusion. Many changes occur during nodule development including the establishment of nodule hypoxia [ 9 ] and profound alterations in the cell cycle [ 48 ] which may result in a ribosome stress, possibly triggering the dissociation of ribosomes and the export of free RPs to the cytosol.…”

“…Nod factors then simultaneously trigger nodule formation in the root cortex and the formation of specialized infection structures called infection threads (ITs) in the epidermis ([ 5 ] for a recent review). Bacterial exopolysaccharides also contribute to IT formation and enhance bacterial survival [ 6 – 8 ]. Inside the nodules, hypoxia triggers bacteroid differentiation and nitrogen fixation [ 9 , 10 ].…”

A Novel OmpR-Type Response Regulator Controls Multiple Stages of the Rhizobium etli – Phaseolus vulgaris N2-Fixing Symbiosis

“…Our data indicate that RetPC55, RetPC56 and nodTc encode for this type of proteins that may comprise the structural components of an efflux pump, whose expression is under the control of RetPC57 in response to plant exudates and that contributes to the successful interaction of R. etli with common bean. This proposed efflux pump may participate, together with other components such as NodI and NodJ, in the secretion of the NFs and additional rhizobial-derived signal molecules such as succinoglycans which play a crucial role in the progression of the rhizobial infection beyond the root epidermal cells (Kawaharada et al, 2015;Maillet et al, 2020). In R. etli and in R. leguminosarum bv.…”