CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically      

Abstract

The CLAVATA3/embryo-surrounding region (CLE) peptides control the fine balance between proliferation and differentiation in plant development. We studied the role of CLE peptides during indeterminate nodule development and identified 25 MtCLE peptide genes in the Medicago truncatula genome, of which two genes, MtCLE12 and MtCLE13, had nodulation-related expression patterns that were linked to proliferation and differentiation. MtCLE13 expression was up-regulated early in nodule development. A high-to-low expression gradient radiated from the inner toward the outer cortical cell layers in a region defining the incipient nodule. At later stages, MtCLE12 and MtCLE13 were expressed in differentiating nodules and in the apical part of mature, elongated nodules. Functional analysis revealed a putative role for MtCLE12 and MtCLE13 in autoregulation of nodulation, a mechanism that controls the number of nodules and involves systemic signals mediated by a leucine-rich repeat receptor-like kinase, SUNN, which is active in the shoot. When MtCLE12 and MtCLE13 were ectopically expressed in transgenic roots, nodulation was abolished at the level of the nodulation factor signal transduction, and this inhibition involved long-distance signaling. In addition, composite plants with roots ectopically expressing MtCLE12 or MtCLE13 had elongated petioles. This systemic effect was not observed in transgenic roots ectopically expressing MtCLE12 and MtCLE13 in a sunn-1 mutant background, although nodulation was still strongly reduced. These results suggest multiple roles for CLE signaling in nodulation.

NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes

“…If NOOT and COCH regulate (or interact with) stem cell activity in the meristem, as suggested by the meristem enlargement observed in the noot and coch mutant nodules, then we can hypothesize that a WUSCHEL-HOMEOBOX/CLE regulatory loop operates in the nodule meristem. In support of this hypothesis, Mortier et al (2010) have shown that at least two CLE peptides are expressed in the meristematic region of the nodule. It will thus be interesting to know if the cytokinininduced Mt-WUSCHEL described by Chen et al (2009) is also expressed in the nodule meristem.…”

Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase

“…Conversely, knockdown of Medicago truncatula MtCLE12 and MtCLE13 resulted in a significant increase in nodule number 17 . Functionally similar CLE genes have also been identified in other leguminous species [18][19][20][21] . Thus, CLE-RS peptides are strong candidates for the root-derived signals that might act as ligands for HAR1.…”

Different Pathways Act Downstream of the CEP Peptide Receptor CRA2 to Regulate Lateral Root and Nodule Development

“…Rhizobial NFs rapidly trigger nuclear calcium oscillations in root hair cells (Lévy et al, 2004;Miwa et al, 2006), which transcriptionally activate key symbiotic (SYM) genes (e.g. NODULE INCEPTION and NODULATION SIGNALING PATHWAY1 and 2 [Kaló et al, 2005;Smit et al, 2005] and MtCLV3/ESR-RELATED12 and 13 [MtCLE12 and 13; Mortier et al, 2010;Saur et al, 2011]). Nodulation is also positively and negatively controlled by complex, context-dependent interactions with various hormones and peptides (Penmetsa and Cook, 1997;Gonzalez-Rizzo et al, 2006;Penmetsa et al, 2008;Mortier et al, 2010;Plet et al, 2011;Saur et al, 2011;Mortier et al, 2012;Larrainzar et al, 2015;van Zeijl et al, 2015).…”

“…NODULE INCEPTION and NODULATION SIGNALING PATHWAY1 and 2 [Kaló et al, 2005;Smit et al, 2005] and MtCLV3/ESR-RELATED12 and 13 [MtCLE12 and 13; Mortier et al, 2010;Saur et al, 2011]). Nodulation is also positively and negatively controlled by complex, context-dependent interactions with various hormones and peptides (Penmetsa and Cook, 1997;Gonzalez-Rizzo et al, 2006;Penmetsa et al, 2008;Mortier et al, 2010;Plet et al, 2011;Saur et al, 2011;Mortier et al, 2012;Larrainzar et al, 2015;van Zeijl et al, 2015). Collectively, these signals, along with the NF/SYM pathway, determine how, when, and where nodules form, as well as the overall nodule number on the root system (Penmetsa and Cook, 1997;Oldroyd et al, 2011).…”