Molecular Mechanisms of Intercellular Rhizobial Infection: Novel Findings of an Ancient Process

Abstract

Establishment of the root-nodule symbiosis in legumes involves rhizobial infection of nodule primordia in the root cortex that is dependent on rhizobia crossing the root epidermal barrier. Two mechanisms have been described: either through root hair infection threads or through the intercellular passage of bacteria. Among the legume genera investigated, around 75% use root hair entry and around 25% the intercellular entry mode. Root-hair infection thread-mediated infection has been extensively studied in the model legumes Medicago truncatula and Lotus japonicus. In contrast, the molecular circuit recruited during intercellular infection, which is presumably an ancient and simpler pathway, remains poorly known. In recent years, important discoveries have been made to better understand the transcriptome response and the genetic components involved in legumes with obligate (Aeschynomene and Arachis spp.) and conditional (Lotus and Sesbania spp.) intercellular rhizobial infections. This review addresses these novel findings and briefly considers possible future research to shed light on the molecular players that orchestrate intercellular infection in legumes.

The Rhizobial Type 3 Secretion System: The Dr. Jekyll and Mr. Hyde in the Rhizobium–Legume Symbiosis

“…Rhizobia must penetrate the root epidermal barrier to reach the developing nodule. To date, two different mechanisms have been described for this infection event: entry by infection threads (IT) or through intercellular infection [ 14 , 15 ]. These mechanisms take place in approximately 75% and 25% of the legume genera, respectively [ 15 ].…”

“…To date, two different mechanisms have been described for this infection event: entry by infection threads (IT) or through intercellular infection [ 14 , 15 ]. These mechanisms take place in approximately 75% and 25% of the legume genera, respectively [ 15 ]. Root hair IT-mediated infection, which is considered a mode of infection more evolved than intercellular infection, is an NF-dependent process: perception of these signal molecules by root hair receptors is required for root hair deformation and the entrapping of rhizobial cells, and for root hair plasmatic membrane invagination, which initiates the formation of the tubular structure that will elongate and branch, as the way for rhizobia to reach nodule primordia.…”

“…In contrast to IT formation, intercellular infection remains poorly understood [ 14 , 15 , 19 ]. In some legumes, such as Sesbania spp.…”

“…In any case, intercellular infection can develop via a crack-entry mechanism, typically through epidermal fissures of emerging lateral roots, such as in Sesbania , Aeschynomene or Arachis , or in root zones where massive root hair curling and twisting takes place, such as in the interaction of strain IRBG74 with L. japonicus [ 19 ]. Several studies indicate NF are required in some but not all the intercellular infection processes described so far [ 15 , 19 , 22 , 23 , 24 ].…”

Aromatic amino acid biosynthesis by aLotusAldolase impacts root hair development and symbiotic associations

“…Arbuscular mycorrhizal symbiosis (AMS) and nitrogen-fixing symbiosis (RNS) are two well-known examples, which provide phosphorus and nitrogen sources, respectively, to the host (Oldroyd, 2013). In the model legume Lotus japonicus ( Lotus ), two modalities of root colonization exist in the RNS, depending on the bacterial partner (Montiel et al ., 2021; Quilbe et al ., 2022). The cognate rhizobial partner Mesorhizobium loti synthesizes and releases lipochito-oligosaccharide nodulation factors (NFs) signalling molecules, after perception of flavonoid compounds secreted by roots (Bek et al ., 2010; Shimamura et al ., 2022).…”