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

Katharina Schiessl,Matthew D Carpenter,Ioannis Tamvakis,Paul C Bailey,Karunakaran Ramakrishnan,Giles E.D Oldroyd,Aaron Thomas,Veronica A Grieneisen,Tak Lee,Jiangqi Wen,Kirankumar S Mysore,Jodi L.S Lilley,Wouter Kohlen,Sebastian Ahnert,Jakub Luptak

doi:10.1016/j.cub.2019.09.005

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.

Highlights

Nodules initiate as lateral root organs in response to the perception of rhizobial bacteria at the root surface
To initiate lateral roots in Medicago truncatula, we turned 2-day-old seedlings 135 to create a bend in the root [29], while nodules were induced with droplets of Sinorhizobium meliloti culture applied on the root susceptibility zone (Figures S1A and S1B)
Similar to what has been reported in Arabidopsis [36], we found that indole-3-acetic acid (IAA) treatment of M. truncatula roots activates LOB-DOMAIN PROTEIN 16 (LBD16) expression (Figure S5H), revealing that LBD16 is responsive to auxin accumulation

Summary

Introduction

Nodules initiate as lateral root organs in response to the perception of rhizobial bacteria at the root surface. Nodules and lateral roots initiate from pericycle, endodermal, and inner-cortical cells as a function of local auxin accumulation [16, 17]. Accompanying both lateral root and nodule development is upregulation of auxin-responsive WOX5 and PLETHORAs at the initiation site of both organs [18, 19]. The initiation of an auxin maxima during nodulation has been proposed to result from suppression of rootward polar auxin transport below the site of rhizobial recognition as a function of cytokinin recognition by CRE1 [3, 22,23,24].

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Discussion

Conclusion