Abstract
Brassinosteroids (BRs) play an essential role in plant growth, and BRI1-EMS suppressor 1 (BES1)/brassinazole-resistant 1 (BZR1) family transcription factors integrate a variety of plant signaling pathways. Despite the fact that BRs inhibit nodulation in leguminous plants, how BRs modulate rhizobia-host interactions and nodule morphogenesis is unknown. Here, we show that GmBEHL1, a soybean homolog of Arabidopsis BES1/BZR1 homolog 1 (BEH1), is an interacting partner of Nodule Number Control 1, a transcriptional repressor that mediates soybean nodulation. GmBEHL1 was highly expressed at the basal parts of emerging nodules, and its expression gradually expanded during nodule maturation. The overexpression and downregulation of GmBEHL1 inhibited and enhanced the number of nodules, respectively, in soybean. Intriguingly, alterations in GmBEHL1 expression repressed the expression of genes in the BR biosynthesis pathway, including homologs of Arabidopsis Constitutive Photomorphogenesis and Dwarf and Dwarf 4. We also detected an interaction between GmBEHL1 and GmBIN2, a putative BR-insensitive 2 (BIN2) homolog, in soybean. Moreover, BR treatment reduced the number, but increased the size, of soybean nodules. Our results reveal GmBEHL1 to be a potent gene that integrates BR signaling with nodulation signaling pathways to regulate symbiotic nodulation.
Highlights
Nitrogen is an essential element for plant growth and development
Nodule development is trigged by a rhizobial infection, and both the initiation of rhizobial entry into roots and the onset of nodulation are dependent on the perception of nodulation factors (NFs) by LysM receptors (e.g., NF Perception [NFP] in M. truncatula, NF Receptors 1 and 5 [NFR1/5] in L. japonicus, and NFR1/5α in soybean), which activate a signaling cascade that triggers nodule formation[4,5,6,7,8,9]
Nodule number is controlled by the autoregulation of nodulation (AON) signaling pathway, which is initiated by the activation of CLE-RS1 and CLE-RS2 (CLE-Root Signal1/2) in rhizobia-infected roots during primordia formation; signaling is in turn perceived by specific receptors, including SUNN(Super Numerary Nodules)in M. truncatula, HAR1(Hypernodulation Aberrant Root Formation 1) in L. japonicus, and GmNARK (Nodule Autoregulation Recepter Kinase) in soybean[23,24,25]
Summary
Nitrogen is an essential element for plant growth and development. To obtain sufficient nitrogen, non-leguminous plants have evolved developmental plasticity of the root system that enables them to remodel their root architecture (i.e., lateral root formation) in response to fluctuating levels of nitrogen in the growth environment[1]. NIN is a central regulator of nodulation, which targets early nodulation genes (ENODs) such as ENOD11 in the root epidermis and Cytokinin Receptor 1 (CRE1) in the cortex of M. truncatula roots to repress or activate www.nature.com/scientificreports/. BRASSINAZOLE-RESISTANT 1 (BZR1) and its homologs (BES1/BZR1-like genes [BEHs]) are key regulators of BR signaling that repress or activate the transcription of BR-responsive genes to mediate plant growth and development[34,35]. Our results suggest that GmBEHL1 functions as a co-repressor to negatively regulate soybean nodulation; they reveal for the first time direct crosstalk between the NF and BR signaling pathways in soybean
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