A CEP Peptide Receptor-Like Kinase Regulates Auxin Biosynthesis and Ethylene Signaling to Coordinate Root Growth and Symbiotic Nodulation in Medicago truncatula.

Fugui Zhu,Jiangli Dong,Mathias Brault,Lihua Zheng,Jiangqi Wen,Peng Liu,Florian Frugier,Qinyi Ye,Tao Wang,Jie Deng,Hong Chen,Rui Li

doi:10.1105/tpc.20.00248

Abstract

Because of the large amount of energy consumed during symbiotic nitrogen fixation, legumes must balance growth and symbiotic nodulation. Both lateral roots and nodules form on the root system, and the developmental coordination of these organs under conditions of reduced nitrogen (N) availability remains elusive. We show that the Medicago truncatula COMPACT ROOT ARCHITECTURE2 (MtCRA2) receptor-like kinase is essential to promote the initiation of early symbiotic nodulation and to inhibit root growth in response to low N. C-TERMINALLY ENCODED PEPTIDE (MtCEP1) peptides can activate MtCRA2 under N-starvation conditions, leading to a repression of YUCCA2 (MtYUC2) auxin biosynthesis gene expression, and therefore of auxin root responses. Accordingly, the compact root architecture phenotype of cra2 can be mimicked by an auxin treatment or by overexpressing MtYUC2, and conversely, a treatment with YUC inhibitors or an MtYUC2 knockout rescues the cra2 root phenotype. The MtCEP1-activated CRA2 can additionally interact with and phosphorylate the MtEIN2 ethylene signaling component at Ser643 and Ser924, preventing its cleavage and thereby repressing ethylene responses, thus locally promoting the root susceptibility to rhizobia. In agreement with this interaction, the cra2 low nodulation phenotype is rescued by an ein2 mutation. Overall, by reducing auxin biosynthesis and inhibiting ethylene signaling, the MtCEP1/MtCRA2 pathway balances root and nodule development under low-N conditions.

Highlights

Plants possess an extremely plastic root system
MtCEP1 peptides acting through the presumptive Medicago truncatula COMPACT ROOT ARCHITECTURE2 (MtCRA2) receptor-like kinase were previously reported to antagonistically regulate the lateral roots locally from root and nodule formation systemically from shoots (Huault et al, 2014), which is in agreement with phenotypic data reported here
The phenotype complementation of cra2 by MtCRA2 confirmed the role of MtCRA2 in regulating both lateral root and nodule number, and a transcriptomic analysis of the cra2 mutant revealed that the MtCRA2 pathway promoting early nodulation regulates the NF signaling symbiotic pathway, as was recently shown for Jemalong A17 cra2 mutants (Laffont et al, 2019)

Summary

Introduction

Plants possess an extremely plastic root system. The growth and architecture of roots are modulated according to extrinsic nitrogen (N) availability in the soil. The root system architecture (RSA) involves the formation of N-fixing root nodules as well as lateral roots. Under N-limiting conditions, plants adapt their main and lateral root growth to facilitate N-uptake efficiency (Xu et al, 2012). Legumes form symbioses with rhizobia to initiate specialized root organs called nodules where atmospheric N2 is converted into ammonium (NH41) to provide legumes with N and sustain their growth (Oldroyd et al, 2011). As lateral root and nodule development are energetically costly, the coordination of these two root-derived developmental processes to maintain an optimal number of organs relative to the carbon and N availability relies on regulatory mechanisms that remain largely unknown

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Conclusion