MtNODULE ROOT1 and MtNODULE ROOT2 Are Essential for Indeterminate Nodule Identity

Abstract

One-sentence summary: 40The loss-of-function of MtNOOT1 and MtNOOT2 leads to the complete loss of nodule identity, prevents 41 the symbiotic process, and results in the absence of nitrogen fixation in Medicago truncatula. 56VZ, SC, GEDO, and PR analyzed the data. KM, KS and PR wrote the article. 58This work was supported by the CNRS, by the grants ANR SVSE 6.2010.1 (LEGUMICS) and ANR-14- 62Agriculture (Dufrenoy Grant, 2011). This work has benefited from the facilities and expertise of the IMAGIF 63Cell Biology Unit of the Gif campus (www.imagif.cnrs.fr) which is supported by the Conseil Général de 64 l'Essonne. 66The author responsible for distribution of materials integral to the findings presented in this article in 67 accordance with the policy described in the instructions for authors (www.plantphysiol.org) is: Pascal 68 Ratet (pascal.ratet@u-psud.fr). 70 71 Acknowledgments 72The Institute of Plant Sciences Paris-Saclay (IPS2, France) benefits from the support of the LabEx Saclay 97fixing root-like structures that were no longer able to host symbiotic rhizobia. This study provides original 98 insights into the molecular basis underlying nodule identity in legumes forming indeterminate nodules. 100 INTRODUCTION 102The symbiotic interaction between legumes and rhizobia results in the formation of root nodules 103 dedicated to host nitrogen-fixing rhizobia. This unique ability to form root nodules is restricted to the 104 Rosids I clade. The predisposition of plants to enter symbiosis with nitrogen-fixing rhizobia seems to have 105 evolved once, between 70 and 100 million years ago and to have derived from an ancestral and 106 widespread symbiosis, the arbuscular mycorrhizal symbiosis (AMS, Soltis et al., 1995; Smith and Read, 107 2008;Bonfante and Genre, 2010;Humphreys et al., 2010;Werner et al., 2014). 109Genetic approaches using nodule-deficient (nod -) and non-functional nodule (fix -) mutant plants 110 allowed the identification of many genes essential for the early steps of root nodule symbiosis. 111Recognition between symbiotic partners, rhizobial infection and nodule organogenesis are initiated by the 112 host plant perception of rhizobial lipo-chitooligosacharidic compounds Jones et al., 113 2007;Kouchi et al., 2010; Horvath et al., 2011;Ovchinnikova et al., 2011; 114 . These compounds are called Nod factors 115and they are structurally similar to the mycorrhization factors (Myc factors) required for AMS initiation 116 (Maillet et al., 2011). 118In the Papilionaceae family, determinate nodules formed in the Phaseoleae, Loteae and 119Dalbergieae tribes have no persistent apical nodule meristem (NM). However, indeterminate nodules 120 formed in the Trifolieae and Fabeae tribes have a persistent apical NM. Indeterminate nodules are highly-121 structured and present different zones; the NM, the infection zone, the nitrogen fixation zone and the older 122 senescent zone (from top to bottom; . The ability of indeterminate nodules to grow 123 continuously results from the presence of the NM. ...

Gene regulatory networks associated with lateral root and nodule development in soybean

“…A number of TFs were demonstrated to play a crucial role in nodule development through genetic evidence from model legumes (4, 30). These include NODULE INCEPTION ( NIN ) (RWP-RK family; (31), NODULATION SIGNALING PATHWAY1 and 2 (NSP1 and NSP2; GRAS domain proteins), Nuclear Factor Y (NF-YA1; (32)), E thylene Response Factors R equired for N odulation (ERN1 and ERN2; AP2/ERF family; (33)), and CYCLOPS (coiled-coil domain protein) (34–37).…”

A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-Type Ontogeny

“…Mtnoot2 mutants do not form nodules with root outgrowths. However, the occurrence of nodule roots increases in Mtnoot1 Mtnoot2 double mutants (Magne et al, 2018a). Therefore, MtNOOT2 also plays a role in maintaining nodule organ identity.…”

“…To investigate this notion, we searched for a legume mutant with the ability to form roots at the apex of nodules. We selected a legume with a mutation in the NOOT/NBCL gene, which can form functional nodules and, like some actinorhizal-type nodules, can form a root at their apex (Couzigou et al 2012;Magne et al 2018a). To determine if the vascular bundles in noot/nbcl mutant nodules have a similar ontogeny to that observed in actinorhizal-type nodules, we studied nodule development in the Medicago Mtnoot1 knockout mutant.…”

Roles of BdUNICULME4 and BdLAXATUM‐A in the non‐domesticated grass Brachypodium distachyon

“…Zmliguleless narrow (Zmlgn), encoding a kinase likely acting upstream of Zmlg1 and Zmlg2, is also required for ligule and auricle development (Moon et al, 2013). The NBCL genes encode BTB/POZ and ankyrin repeat containing proteins that can act as E3 ubiquitin ligases but that are also able to interact with themselves and with TGA bZIP TFs (Zhang et al, 1999;Despr es et al, 2000;Zhou et al, 2000;Despr es et al, 2003;Hepworth et al, 2005;Boyle et al, 2009;Wu et al, 2012;Zhang et al, 2017;Magne et al, 2018b;Wang et al, 2019). ZmLG2 is orthologous to a TGA bZIP TF encoded by the Bra-di2g55567 locus in B. distachyon (similarity 87.3%, identity 78.1%).…”

“…Pictures of whole organs were acquired using a Nikon AZ100 Microscope (Nikon, http://www.nikoninstruments.com/). Technovit sections were performed as described in Magne et al (2018b), sections were observed with a microscope (BX53; Olympus, https:// www.olympus-lifescience.com/) and pictures acquired using cell-Sens Standard software (Olympus).…”