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

Abstract

Light is critical for supplying carbon for use in the energetically expensive process of nitrogen-fixing symbiosis between legumes and rhizobia. We recently showed that root nodule formation in phyB mutants [which have a constitutive shade avoidance syndrome (SAS) phenotype] was suppressed in white light, and that nodulation in wild-type is controlled by sensing the R/FR ratio through jasmonic acid (JA) signaling. We concluded that the cause of reduced root nodule formation in phyB mutants was the inhibition of JA-Ile production in root. Here we show that the shoot JA-Ile level of phyB mutants is higher than that of the wild-type strain MG20, suggesting that translocation of JA-Ile from shoot to root is impeded in the mutant. These results indicate that root nodule formation in phyB mutants is suppressed both by decreased JA-Ile production, caused by reduced JAR1 activity in root, and by reduced JA-Ile translocation from shoot to root.Light is an important environmental factor controlling plant growth. It is well known that plants require light for photosynthesis and are able to monitor both light quality and quantity for optimal survival. Plants have photoreceptors that sense the presence of their neighbors by monitoring the ratio of red light (R), which is absorbed by chlorophyll, and far red light (FR), which is not. A low R/FR ratio indicates the presence of neighbors that may compete for photosynthetically active radiation (PAR) and initiates the shade avoidance syndrome (SAS), causing plants to grow taller or bend to the light to avoid shade. [1][2][3][4] Many leguminous plants establish a symbiosis with nitrogenfixing soil bacteria called rhizobia. Inside the root nodules, the rhizobia differentiate into nitrogen-fixing bacteroids. The bacteroids convert atmospheric nitrogen into ammonia, a source of fixed nitrogen for the host plant. Because assimilates from photosynthesis provide energy to fuel the symbiosis between legumes and rhizobia, the light conditions under which host plants grow are very important. 5-8Previously we reported that root nodule formation was suppressed in a Lotus japonicus phytochrome B (phyB) mutant having a constitutive SAS phenotype. 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 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 plant...

Jasmonates: Multifunctional Roles in Stress Tolerance

“…Nodulation inhibition by JA has recently been reported in Medicago truncatula ( Sun et al, 2006 ) and Lotus japonicus ( Nakagawa and Kawaguchi, 2006 ). EST analysis of Lotus japonica showed that during Rhizobium – Lotus interaction, genes involved in pathogen defense response and JA biosynthetic enzyme (AOC and OPRs) were upregulated and suppressed during the late nodule formation step ( Shigeyama et al, 2012 ; Bordenave et al, 2013 ). According to Kouchi et al (2004) , in the JA biosynthetic pathway, genes responsible for lipooxygenase were mostly downregulated.…”

Canopy Light Quality Modulates Stress Responses in Plants

“…The phyB mutant of Lotus japonicus exhibits a constitutive shade avoidance phenotype just as in Arabidopsis but also has a reduced number of nodules compared with WT plants (Figure 3) (Suzuki et al., 2011). Grafting experiments showed that nodulation can be reduced in plants composed of phyB shoots and WT roots, indicating that the mutation in the shoot is sufficient to get the impoverished nodulation phenotype in the roots (Shigeyama et al., 2012, Suzuki et al., 2011). The nodulation deficiency in phyB mutants is associated with decreased root JA levels and a downregulation of JA-responsive gene expression compared with WT roots (Shigeyama et al., 2012, Suzuki et al., 2011).…”

“…Grafting experiments showed that nodulation can be reduced in plants composed of phyB shoots and WT roots, indicating that the mutation in the shoot is sufficient to get the impoverished nodulation phenotype in the roots (Shigeyama et al., 2012, Suzuki et al., 2011). The nodulation deficiency in phyB mutants is associated with decreased root JA levels and a downregulation of JA-responsive gene expression compared with WT roots (Shigeyama et al., 2012, Suzuki et al., 2011). Interestingly, nodulation by Bradyrhizobium japonicum was promoted by end-of-day (EOD) low R:FR treatment in soybean (Balatti and Montaldi, 1986, Hunt et al., 1990), suggesting that there may be substantial species-specificity of the interplay between light and beneficial interactions.…”

Plant Defense Responses to Biotic Stress and Its Interplay With Fluctuating Dark/Light Conditions

“…Experimental validation reveals that the nodulation is decreased in grafted plants with phyB shoots and control roots. This is indicative of the fact that the mutations in the shoot tissue decrease nodulation in the roots ( Suzuki et al, 2011 ; Shigeyama et al, 2012 ). The decreased nodulation in phyB mutants can be linked to downregulation of JA-responsive gene expression leading to lower JA levels in roots ( Suzuki et al, 2011 ; Shigeyama et al, 2012 ).…”

“…This is indicative of the fact that the mutations in the shoot tissue decrease nodulation in the roots ( Suzuki et al, 2011 ; Shigeyama et al, 2012 ). The decreased nodulation in phyB mutants can be linked to downregulation of JA-responsive gene expression leading to lower JA levels in roots ( Suzuki et al, 2011 ; Shigeyama et al, 2012 ). Next, taking into account the impact of R:FR exposures, the plant defense mechanisms against herbivores and pathogens are downregulated under low R:FR conditions ( Ballaré, 2014 ; Ballaré and Austin, 2019 ; Figure 5 ).…”