Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA

Abstract

Nitrogen-fixing root nodules on legumes result from two developmental processes, bacterial infection and nodule organogenesis. To balance symbiosis and plant growth, legume hosts restrict nodule numbers through an inducible autoregulatory process. Here, we present a mechanism where repression of a negative regulator ensures symbiotic susceptibility of uninfected roots of the host We show that microRNA miR2111 undergoes shoot-to-root translocation to control rhizobial infection through posttranscriptional regulation of the symbiosis suppressor TOO MUCH LOVE in roots. miR2111 maintains a susceptible default status in uninfected hosts and functions as an activator of symbiosis downstream of LOTUS HISTIDINE KINASE1-mediated cytokinin perception in roots and HYPERNODULATION ABERRANT ROOT FORMATION1, a shoot factor in autoregulation. The miR2111- node ensures activation of feedback regulation to balance infection and nodulation events.

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

“…Consistent with Tsikou et al . (), when examined at 3 dai, lhk1‐1 roots were not significantly different from the corresponding wild‐type samples in terms of the CLE‐RS1 gene expression, whereas CLE‐RS3 was significantly lower in the mutant (Fig. S4).…”

“…Consistent with Tsikou et al . (), the absence of functional LHK1 strongly limited the steady‐state level of the TML mRNA in M. loti ‐inoculated roots. However, under the conditions used in this studies, TML remained somewhat responsive to M. loti infection in the lhk1‐1 single mutant, whereas this was totally lost in the triple cytokinin receptor mutant.…”

“…3–5 d (Suzuki et al ., ), which would not be fast enough to limit the initial M. loti infections. However, significant changes to shoot and root miR2111 levels were already detected within the first 2 d after M. loti inoculation (Tsikou et al ., ), indicating that regulation of TML is a relatively rapid process. Our data emphasize the root function of LHK1‐cortex in regulating M. loti infection (Fig.…”

Connecting the pieces: uncovering the molecular basis for long‐distance communication through plant grafting

“…Plants engage in symbiotic and parasitic interactions through coordinated interorganismal communication. Two recent studies used grafting to uncover miRNAs that participate in this communication system during symbiotic plant–microbe and pathogenic plant–parasite interactions (Shahid et al ., ; Tsikou et al ., ). Members of the legume family participate in tight symbiotic associations with N‐fixing rhizobia through the formation of specialized root‐derived nodules.…”

“…Although grafting plays a central role in the successful production of many crops, the underlying mechanisms that make particular graft combinations productive remain largely unknown. Independent of its application in agriculture, grafting experiments have been used to discover mobile proteins, mRNAs, small RNAs, and small molecules that impact plant morphology (Kim, ; Haywood et al ., ), reproductive transitions (Corbesier et al ., ; Jaeger & Wigge, ), host–microbe and plant–parasite interactions (Shahid et al ., ; Tsikou et al ., ), root–shoot balance (Lin et al ., ; Spiegelman et al ., ; Chen et al ., ; Landrein et al ., ), and other fundamental organismal processes (Martin et al ., ; Navarro et al ., ; Takahashi et al ., ; Tylewicz et al ., ). Advances in genomic resources and molecular techniques that support grafted crops make it possible for the distinct fields of agricultural and experimental grafting to be merged.…”