Lotus japonicus NOOT‐BOP‐COCH‐LIKE1 is essential for nodule, nectary, leaf and flower development

Abstract

The NOOT-BOP-COCH-LIKE (NBCL) genes are orthologs of Arabidopsis thaliana BLADE-ON-PETIOLE1/2. The NBCLs are developmental regulators essential for plant shaping, mainly through the regulation of organ boundaries, the promotion of lateral organ differentiation and the acquisition of organ identity. In addition to their roles in leaf, stipule and flower development, NBCLs are required for maintaining the identity of indeterminate nitrogen-fixing nodules with persistent meristems in legumes. In legumes forming determinate nodules, without persistent meristem, the roles of NBCL genes are not known. We thus investigated the role of Lotus japonicus NOOT-BOP-COCH-LIKE1 (LjNBCL1) in determinate nodule identity and studied its functions in aerial organ development using LORE1 insertional mutants and RNA interference-mediated silencing approaches. In Lotus, LjNBCL1 is involved in leaf patterning and participates in the regulation of axillary outgrowth. Wild-type Lotus leaves are composed of five leaflets and possess a pair of nectaries at the leaf axil. Legumes such as pea and Medicago have a pair of stipules, rather than nectaries, at the base of their leaves. In Ljnbcl1, nectary development is abolished, demonstrating that nectaries and stipules share a common evolutionary origin. In addition, ectopic roots arising from nodule vascular meristems and reorganization of the nodule vascular bundle vessels were observed on Ljnbcl1 nodules. This demonstrates that NBCL functions are conserved in both indeterminate and determinate nodules through the maintenance of nodule vascular bundle identity. In contrast to its role in floral patterning described in other plants, LjNBCL1 appears essential for the development of both secondary inflorescence meristem and floral meristem.

Systems Biology of Plant-Microbiome Interactions

“…The recently described SA receptors, NPR1, NPR3, NPR4 (Canet et al, 2010), together mediate responses to different SA concentrations (Fu et al, 2012;Kuai et al, 2015;Castello et al, 2018). In contrast, the more distant family members, BOP1 and BOP2, appear to have no function in SA signaling (Canet et al, 2012) but have been implicated in developmental programs such as flowering and nodule formation in legumes (Couzigou et al, 2012;Magne et al, 2018). At the same time, the biochemical regulation of NPR1, and possibly also its paralogs, is complex and involves multiple cellular compartments, redox potential, phosphorylation, and degradation.…”

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

“…Therefore, the ontogeny of the Mtnoot1 nodule vasculature is different from that of the wild type and more similar to that of actinorhizaltype nodules. Mutations in the MtNOOT1 orthologs of pea (Pscoch1) and L. japonicus (Ljnbcl1) can also cause root outgrowth from nodules (Couzigou et al 2012;Magne et al 2018b) Therefore, we assume that the ontogeny of the nodule vasculature is also actinorhizal-like in these legume mutants. In actinorhizal-type nodules (in plants such as M. gale and Datisca glomerata), which can form so-called nodule roots, the apical 10" " meristems of lobes have the potential to switch to root production (Pawlowski and Bisseling, 1996;Franche et al, 2009).…”

“…One such gene is NOOT-BOP-COCH-LIKE (NBCL), encoding a cotranscriptional regulator. Mutations in this gene (named NODULE ROOT1 [MtNOOT1] in Medicago, COCHLEATIA1 [PsCOCH1] in pea [Pisum sativum], and LjNBCL1 in Lotus japonicus) can cause root outgrowth from nodules, suggesting that this gene functions in maintaining nodule identity (Couzigou et al 2012;Magne et al 2018b).…”

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

“…In dicots, NBCL genes participate in many developmental processes, such as in the differentiation and patterning of stipules/nectary glands and leaves (Yaxley et al, 2001;Ha et al, 2003Ha et al, , 2004Ha et al, , 2007McKim et al, 2008;Couzigou et al, 2012;Magne et al, 2018a), in internode elongation, in floral meristem identity acquisition and in flower patterning and identity (Yaxley et al, 2001;Ha et al, 2003Ha et al, , 2004Ha et al, , 2007Hepworth et al, 2005;Norberg et al, 2005;Xu et al, 2010;Couzigou et al, 2012;Khan et al, 2012;Khan et al, 2015). NBCL genes are also involved in inflorescence architecture, in fruit development (Hepworth et al, 2005;Ragni et al, 2008;Khan et al, 2012;Xu et al, 2016) and in the establishment and functioning of abscission zones (Clements and Atkins, 2001a,b;Hepworth et al, 2005;Norberg et al, 2005;McKim et al, 2008;Wu et al, 2012;Frankowski et al, 2015;Couzigou et al, 2016;Wilmowicz et al, 2016).…”