Differential regulation of the Epr3 receptor coordinates membrane-restricted rhizobial colonization of root nodule primordia

Abstract

In Lotus japonicus, a LysM receptor kinase, EPR3, distinguishes compatible and incompatible rhizobial exopolysaccharides at the epidermis. However, the role of this recognition system in bacterial colonization of the root interior is unknown. Here we show that EPR3 advances the intracellular infection mechanism that mediates infection thread invasion of the root cortex and nodule primordia. At the cellular level, Epr3 expression delineates progression of infection threads into nodule primordia and cortical infection thread formation is impaired in epr3 mutants. Genetic dissection of this developmental coordination showed that Epr3 is integrated into the symbiosis signal transduction pathways. Further analysis showed differential expression of Epr3 in the epidermis and cortical primordia and identified key transcription factors controlling this tissue specificity. These results suggest that exopolysaccharide recognition is reiterated during the progressing infection and that EPR3 perception of compatible exopolysaccharide promotes an intracellular cortical infection mechanism maintaining bacteria enclosed in plant membranes.

Legumes versus rhizobia: a model for ongoing conflict in symbiosis

“…Conversely, plant hosts benefit from nodulation only under certain conditions, such as when soils are nitrogen poor and contain compatible, nitrogen-fixing rhizobia (Regus et al, 2017b). Among legume taxa, there is wide variation in their specificity for restricting nodulation, often dependent on the production of host-specific flavonoids (Wasson et al, 2006;Liu & Murray, 2016) and host root receptors that recognize specific rhizobia (Via et al, 2016;Kawaharada et al, 2017). 'Specialist' legume species are only able to form nodules with a low genetic diversity of rhizobia strainsand thus might occupy fewer environmentsbut can gain greater mean fitness benefits from the symbiosis than more 'generalist' hosts (Ehinger et al, 2014).…”

“…Recent work on host control of nodule formation has highlighted the importance of legume root receptors that recognize strain-specific surface polysaccharides of rhizobia (Via et al, 2016;Kawaharada et al, 2017). In some instances, mutations introduced into the host receptors or the corresponding symbiont polysaccharides can lead to rhizobia being diverted from their normal route of intracellular infection (Kawaharada et al, 2017). However, the rhizobia can nonetheless form nodules via passive crack entry (Acosta-Jurado et al, 2016), or through reentry into plant cells from intercellular space (Kawaharada et al, 2017).…”

“…In some instances, mutations introduced into the host receptors or the corresponding symbiont polysaccharides can lead to rhizobia being diverted from their normal route of intracellular infection (Kawaharada et al, 2017). However, the rhizobia can nonetheless form nodules via passive crack entry (Acosta-Jurado et al, 2016), or through reentry into plant cells from intercellular space (Kawaharada et al, 2017). Moreover, host control over nodulation specificity can also be overwhelmed.…”

Inside out: root cortex‐localized LHK1 cytokinin receptor limits epidermal infection of Lotus japonicus roots by Mesorhizobium loti

“…Synthesized by rhizobia in the presence of a compatible plant host (Lerouge et al ., ), NFs initiate symbiotic root development by selectively activating specific plant lysine motif (LysM) receptor‐like kinase molecules, known as NF receptors (Limpens et al ., ; Madsen et al ., ; Radutoiu et al ., , ; Arrighi et al ., ; Den Camp et al ., ; Broghammer et al ., ; Liang et al ., ; Murakami et al ., ). This leads to cellular reprogramming, which drives symbiotic infection and nodule organogenesis (Madsen et al ., ; Ariel et al ., ; Singh et al ., ; Soyano & Hayashi, ; Kawaharada et al ., , ). Deleterious mutations in the Lotus japonicus LHK1 cytokinin receptor gene and its Medicago truncatula and Arachis hypogea counterparts, MtCRE1 and AhHK1 , respectively, significantly attenuate nodule formation (Gonzalez‐Rizzo et al ., ; Murray et al ., ; Plet et al ., ; Kundu & Dasgupta, ) and the L. japonicus lhk1‐1 lhk1a‐1 lhk3‐1 triple cytokinin receptor mutant is unable to form nodules (Held et al ., ).…”

Genome‐wide identification of genes directly regulated by ChvI and a consensus sequence for ChvI binding in Sinorhizobium meliloti

“…In addition to helping rhizobia tolerate varied environmental stresses (Miller-Williams et al, 2006;Davies and Walker, 2007;Vriezen et al, 2007;Morris and González, 2009;Barnett et al, 2012;Lehman and Long, 2013;Geddes et al, 2014;Arnold et al, 2017), EPS are important signaling molecules that contribute to the specificity of the host-microbe interaction and promote infection (Kawaharada et al, 2015(Kawaharada et al, , 2017. In the Rm1021 strain of Sinorhizobium meliloti, a symbiont of Medicago spp., EPS-I or succinoglycan is the only symbiotically active EPS produced.…”