Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling

Abstract

Light is critical for supplying carbon to the energetically expensive, nitrogen-fixing symbiosis between legumes and rhizobia. Here, we show that phytochrome B (phyB) is part of the monitoring system to detect suboptimal light conditions, which normally suppress Lotus japonicus nodule development after Mesorhizobium loti inoculation. We found that the number of nodules produced by L. japonicus phyB mutants is significantly reduced compared with the number produced of WT Miyakojima MG20. To explore causes other than photoassimilate production, the possibility that local control by the root genotype occurred was investigated by grafting experiments. The results showed that the shoot and not the root genotype is responsible for root nodule formation. To explore systemic control mechanisms exclusive of photoassimilation, we moved WT MG20 plants from white light to conditions that differed in their ratios of low or high red/far red (R/FR) light. In low R/FR light, the number of MG20 root nodules dramatically decreased compared with plants grown in high R/FR, although photoassimilate content was higher for plants grown under low R/FR. Also, the expression of jasmonic acid (JA) -responsive genes decreased in both low R/FR light-grown WT and white light-grown phyB mutant plants, and it correlated with decreased jasmonoyl-isoleucine content in the phyB mutant. Moreover, both infection thread formation and root nodule formation were positively influenced by JA treatment of WT plants grown in low R/FR light and white lightgrown phyB mutants. Together, these results indicate that root nodule formation is photomorphogenetically controlled by sensing the R/FR ratio through JA signaling.symbiotic nitrogen fixation | shade avoidance syndrome

Additional cause for reduced JA-Ile in the root of a Lotus japonicus phyB mutant

“…By using grafted plants prepared from MG20 and phyB mutant plants, we also showed that shoot genotype controls root nodule formation. 9 Here we report additional data confirms that root nodulation is controlled by shoot genotype. The expression level of marker gene NIN, 10 which is required for infection thread formation and nodule primordium initiation, was analyzed in the root of grafted plants by using real time RT-PCR by the methods described in Tominaga et al 11 The roots and shoots of five-day-old MG20 and phyB mutant plants were grafted in various combinations, as described by Magori et al 12 After 7 d, the grafted plants were inoculated with M. loti, and expression was analyzed 7 d after inoculation.…”

“…9 In that paper, we concluded that the cause of reduced root nodule formation in low-R/FR-grown MG20 (wild-type) plants and white-light-grown phyB mutants is inhibition of JA-Ile (an active JA derivative) production in root. By using grafted plants prepared from MG20 and phyB mutant plants, we also showed that shoot genotype controls root nodule formation.…”

“…9 Because JAR1 codes for an enzyme that conjugates JA with amino acids to produce the active JA derivative [most likely jasmonoyl-isoleucine (JA-Ile)], 13 we suggested that inhibition of root nodule formation in phyB mutants is caused by suppression of the conversion of JA to JA-Ile. To investigate whether JA-Ile levels decreased throughout the whole plant or only in root, we measured the endogenous concentrations of JA and JA-Ile in shoots of white light-grown MG20 and phyB.…”

Clock-Controlled and FLOWERING LOCUS T (FT)-Dependent Photoperiodic Pathway in Lotus japonicus I: Verification of the Flowering-Associated Function of an FT Homolog

“…5). 49) It was further observed that the phyB mutant plants set the first flower at the 7th node on average, while wild-type plants did so at the 13th node on average. This event observed for phyB is a hallmark of the early flowering phenotype.…”

“…Recently, a stable phyB (the gene encoding one of the red light photoreceptors) mutant of L. japonicus was isolated and characterized in terms of a linkage between nodulation in roots and far-red response in shoots. 49) The phyB mutant allowed us to characterize the L. japonicus plant itself with special reference to the flowering time. It is well known of A. thaliana that the phyB photoreceptor regulates (or inhibits) flowering through AtFT in response to changes in light quality.…”