Endogenous gibberellins affect root nodule symbiosis via transcriptional regulation of NODULE INCEPTION in Lotus japonicus

• Published in: The Plant journal : for cell and molecular biology 2021-03, Vol.105 (6), p.1507-1520
• Main Authors: Akamatsu, Akira, Nagae, Miwa, Nishimura, Yuka, Romero Montero, Daniela, Ninomiya, Satsuki, Kojima, Mikiko, Takebayashi, Yumiko, Sakakibara, Hitoshi, Kawaguchi, Masayoshi, Takeda, Naoya
• Format: Article
• Language: English
• Subjects: autoregulation of nodulation; Biological activity; Biosynthesis; cis‐acting region; Defective mutant; Gene regulation; Gibberellic acid; gibberellin; Gibberellins; Hormones; Legumes; Lotus japonicus; Nodulation; Nodule; NODULE INCEPTION; Phenotypes; Plant hormones; root nodule symbiosis; Signaling; Symbiosis
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15128

SUMMARY Legumes and nitrogen‐fixing rhizobial bacteria establish root nodule symbiosis, which is orchestrated by several plant hormones. Exogenous addition of biologically active gibberellic acid (GA) is known to inhibit root nodule symbiosis. However, the precise role of GA has not been elucidated because of the trace amounts of these hormones in plants and the multiple functions of GAs. Here, we found that GA signaling acts as a key regulator in a long‐distance negative‐feedback system of root nodule symbiosis called autoregulation of nodulation (AON). GA biosynthesis is activated during nodule formation in and around the nodule vascular bundles, and bioactive GAs accumulate in the nodule. In addition, GA signaling induces expression of the symbiotic transcription factor NODULE INCEPTION (NIN) via a cis‐acting region on the NIN promoter. Mutants with deletions of this cis‐acting region have increased susceptibility to rhizobial infection and reduced GA‐induced CLE‐RS1 and CLE‐RS2 expression, suggesting that the inhibitory effect of GAs occurs through AON. This is supported by the GA‐insensitive phenotypes of an AON‐defective mutant of HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1) and a reciprocal grafting experiment. Thus, endogenous GAs induce NIN expression via its GA‐responsive cis‐acting region, and subsequently the GA‐induced NIN activates the AON system to regulate nodule formation. Significance Statement Numerous recent discoveries pertaining to the molecular basis of hormonal activity during fruit development provide new insights into the role of hormones in this biological and agriculturally important process and highlight important open questions related to molecular mechanisms and conservation of regulatory phenomena across diverse taxa.