NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula

Abstract

SummaryTo overcome nitrogen deficiencies in the soil, legumes enter symbioses with rhizobial bacteria that convert atmospheric nitrogen into ammonium. Rhizobia are accommodated as endosymbionts within lateral root organs called nodules that initiate from the inner layers of Medicago truncatula roots in response to rhizobial perception. In contrast, lateral roots emerge from predefined founder cells as an adaptive response to environmental stimuli, including water and nutrient availability. CYTOKININ RESPONSE 1 (CRE1)-mediated signaling in the pericycle and in the cortex is necessary and sufficient for nodulation, whereas cytokinin is antagonistic to lateral root development, with cre1 showing increased lateral root emergence and decreased nodulation. To better understand the relatedness between nodule and lateral root development, we undertook a comparative analysis of these two root developmental programs. Here, we demonstrate that despite differential induction, lateral roots and nodules share overlapping developmental programs, with mutants in LOB-DOMAIN PROTEIN 16 (LBD16) showing equivalent defects in nodule and lateral root initiation. The cytokinin-inducible transcription factor NODULE INCEPTION (NIN) allows induction of this program during nodulation through activation of LBD16 that promotes auxin biosynthesis via transcriptional induction of STYLISH (STY) and YUCCAs (YUC). We conclude that cytokinin facilitates local auxin accumulation through NIN promotion of LBD16, which activates a nodule developmental program overlapping with that induced during lateral root initiation.

An ancestral signalling pathway is conserved in plant lineages forming intracellular symbioses

“…Plasmid construction. The Golden Gate modular cloning system was used to prepare the plasmids as described in Schiessl et al 85 . Levels 0 and 1 used in this study are listed in Supplemental Table 6 and held for distribution in the ENSA project core collection (https://www.ensa.ac.…”

The role of CLV1, CLV2 and HPAT homologs in nitrogen-regulation of root development

“…Many legumes can form a second secondary root organ, the nodule, which house nitrogen-fixing rhizobial bacteria and the formation of these nodule organs is dramatically repressed by nitrogen supply (Goh et al 2018). Indeed, in legumes there is a clear overlap in some of the genes and signals that regulate root development and nodulation in response to nitrogen and this dovetails with recent evidence that legume nodules are derived in part from a modified lateral root organ development program (Schiessl et al 2019;Soyano et al 2019).…”

Receptor-Like Kinases Sustain Symbiotic Scrutiny

“…Downstream of LysM-RLKs, multiple signalling pathways emerge from SYMRK; ranging from the activation of mevalonate pathway for a putative secondary messenger for activating Ca 2+ -oscillations (Kevei et al, 2007;Venkateshwaran et al, 2015), inhibition of MAPKK activity (Chen et al, 2012) and importantly to activation of LjNIN (Zhu et al, 2008;Wang et al, 2013), a transcriptional regulator that coordinates both infection and nodule organogenesis, and recently demonstrated to have recruited the lateral root development pathway for nodule development (Schiessl et al, 2019). Because overexpression of LjNFR5, LjNFR1 or especially, LjSYMRK is sufficient for spontaneous nodule formation in the absence of symbiont (Ried et al, 2014); it is unsurprising that there is a multitude of regulatory mechanisms on the receptors to ensure appropriate activation only when the symbiont is present.…”