NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Abstract

Autoregulatory negative-feedback loops play important roles in finebalancing tissue and organ development. Such loops are composed of short-range intercellular signaling pathways via cell-cell communications. On the other hand, leguminous plants use a long-distance negative-feedback system involving root-shoot communication to control the number of root nodules, root lateral organs that harbor symbiotic nitrogen-fixing bacteria known as rhizobia. This feedback system, known as autoregulation of nodulation (AON), consists of two long-distance mobile signals: root-derived and shoot-derived signals. Two Lotus japonicus CLAVATA3/ENDOSPERM SURROUNDING REGION (CLE)-related small peptides, CLE ROOT SIGNAL1 (CLE-RS1) and CLE-RS2, function as root-derived signals and are perceived by a shoot-acting AON factor, the HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1) receptor protein, an ortholog of Arabidopsis CLAVATA1, which is responsible for shoot apical meristem homeostasis. This peptide-receptor interaction is necessary for systemic suppression of nodulation. How the onset of nodulation activates AON and how optimal nodule numbers are maintained remain unknown, however. Here we show that an RWP-RK-containing transcription factor, NODULE INCEPTION (NIN), which induces nodule-like structures without rhizobial infection when expressed ectopically, directly targets CLE-RS1 and CLE-RS2. Roots constitutively expressing NIN systemically repress activation of endogenous NIN expression in untransformed roots of the same plant in a HAR1-dependent manner, leading to systemic suppression of nodulation and down-regulation of CLE expression. Our findings provide, to our knowledge, the first molecular evidence of a long-distance autoregulatory negative-feedback loop that homeostatically regulates nodule organ formation.L ong-distance organ-to-organ communications are generally critical for coordinating development and environmental adaptation in multicellular organisms, particularly plants that continuously produce postembryonic organs in various environmental conditions (1, 2). Autoregulatory negative-feedback loops play important roles in fine-balancing tissue and organ development. Such feedback loops include short-range intercellular signaling via cell-cell communication. In Arabidopsis, shoot apical meristem (SAM) regulation involves a well-characterized short-range negative-feedback loop that maintains the homeostasis of plant organ development (3-6). The molecular substance of long-distance negative-feedback loops that homeostatically regulate organ production and development remains largely unknown, however.Leguminous plants use long-distance autoregulatory negativefeedback systems involving root-shoot communications to control the number of root nodules, symbiotic root lateral organs formed as consequence of successful interaction with nitrogenfixing bacteria, collectively known as rhizobia. This nodule symbiosis is beneficial to host plants, because rhizobia accommodated in nodules convert atmospheric nitrogen to ammonium, a ...

A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis

“…This would be similar to NIN, which is required for symbiotic gene induction in the epidermis and cortex, as well as Rhizobium spp. infection and nodule initiation, while restricting ENOD11 expression on the one hand and nodulation on the other hand, via CLE peptides Soyano et al, 2013Soyano et al, , 2014Laloum et al, 2014;Yoro et al, 2014;Fournier et al, 2015;Vernié et al, 2015). Consequently, the impact of the pEPI:AtCKX3 construct might depend on the relative efficiency of different processes (e.g.…”

“…Indeed, CKs have been shown in L. japonicus to mimic the activity of the shoot-derived signal that inhibits nodule formation during systemic autoregulation of nodulation (Sasaki et al, 2014), while CKs induce, via CRE1/LHK1 in M. truncatula and L. japonicus, the expression of CLAVATA3-LIKE (CLE) peptides promoting systemic autoregulation of nodulation (Mortier et al, 2012a;Soyano et al, 2014). In addition, the observations that, first, the expression of a CK-responsive reporter (TWO COMPONENT SIGNALING SENSOR [TCS]; Müller and Sheen, 2008),increases with time in the epidermis of rhizobium-infected L. japonicus roots and, second, that the lhk1-1 mutant is hyperinfected led to the suggestion that CK might be involved in locally restricting the number of infections in L. japonicus (Held et al, 2014).…”

A Medicago truncatula Cystathionine-β-Synthase-like Domain-Containing Protein Is Required for Rhizobial Infection and Symbiotic Nitrogen Fixation

“…Recently, it has been shown that LjCyclops is a TF that it is required for induction of NIN expression (Singh et al, 2014). Further, it has been shown that NIN binds to and activates the promoters of the Nodulation Pectate Lyase gene (LjNPL, Xie et al, 2012), LjNF-YA1, and LjNF-YB1, and the genes encoding two LjCLAVATA3/ENDOSPERM SURROUNDING REGION (CLE)-related small peptides, CLE ROOT SIGNAL (CLE1 and CLE2, Soyano et al, 2013Soyano et al, , 2014.…”

Does SUNN-SYMRK Crosstalk occur in Medicago truncatula for regulating nodule organogenesis?

“…[8][9][10][11] The transcription factor NODULE INCEPTION (NIN) is projected as the central coordinator, as it is essential for both nodule primordium formation and CLE peptide generation that results in systemic suppression of nodulation. [12][13][14] Several plant hormones are associated with the control of nodule number by AON. For example, long distance auxin transport is defective in sunn-1 15 and supernodulation in har1 can be suppressed by cytokinin receptor mutations.…”