Medicago truncatula Yellow Stripe‐Like7 encodes a peptide transporter participating in symbiotic nitrogen fixation

Abstract

Yellow Stripe-Like (YSL) proteins are a family of plant transporters that are typically involved in transition metal homeostasis. Three of the four YSL clades (I, II and IV) transport metals complexed with the non-proteinogenic amino acid nicotianamine or its derivatives. No such capability has been shown for any member of clade III, but the link between these YSLs and metal homeostasis could be masked by functional redundancy. We studied the role of the clade III YSL protein MtSYL7 in Medicago truncatula nodules. MtYSL7, which encodes a plasma membrane-bound protein, is mainly expressed in the pericycle and cortex cells of the root nodules. Yeast complementation assays revealed that MtSYL7 can transport short peptides. M. truncatula transposon insertion mutants with decreased expression of MtYSL7 had lower nitrogen fixation rates and showed reduced plant growth whether grown in symbiosis with rhizobia or not. YSL7 mutants accumulated more copper and iron in the nodules, which is likely to result from the increased expression of iron uptake and delivery genes in roots. Taken together, these data suggest that MtYSL7 plays an important role in the transition metal homeostasis of nodules and symbiotic nitrogen fixation.

Nitrogen fertilization differentially affects the symbiotic capacity of two co‐occurring ectomycorrhizal species

“…This was not limited to one type of transporter but encompassed reduced expression of inorganic, amino acid and peptide transporters, as well as other transporters implicated in N transport, including several major facilitator superfamily transporters and YELLOW STRIPE ‐like genes. While typically associated with metal transport, some YELLOW STRIPE ‐like genes have recently been shown to transport oligopeptides and have an important role in the maintenance of nitrogen fixation in rhizobial symbiosis (Castro‐Rodriguez et al ., 2021; Gavrin et al ., 2021). Some transporters were also highly expressed in the P. albus high N‐colonized roots compared to other tissues, including a set of lysine/histidine transporters.…”

Forging a symbiosis: transition metal delivery in symbiotic nitrogen fixation

“…This is suggested by having similar results when transforming the yeast mutants with Fe 2+ ‐transporting IRT1. Moreover, iron‐NA‐dependent complementation could not be achieved by other laboratories working on the same GmYSL7 or the M. truncatula orthologue (Castro‐Rodríguez et al ., 2021; Gavrin et al ., 2021; see below). Regardless of the specific role of GmYSL7, the overall involvement of YSL transporters in metal allocation to nodules is further supported by the need of NA synthesis in nodules by NA synthases (NAS).…”

“…The later reported localization in the vasculature (Wu et al ., 2023) is similar to that of the M. truncatula orthologue. MtYSL7 is located in the plasma membrane of nodule cortex cells and in roots, where a role in long‐distance signaling is more likely (Castro‐Rodríguez et al ., 2021). Further work on the identification of the peptide(s) transported by YSL7 is critical to ascertain whether YSL7 and its substrates are involved in regulating metal allocation to symbiotic nitrogen fixation.…”

“…In A. thaliana , it has been shown that functional YSL1 and YSL3 proteins participate in the long‐distance signaling of iron deficiency to roots by a yet‐to‐be‐defined mechanism (Kumar et al ., 2017). YSL7 is a candidate to mediate metal signaling in soybean and M. truncatula nodules (Castro‐Rodríguez et al ., 2021; Gavrin et al ., 2021). Arabidopsis, soybean, and M. truncatula YSL7 proteins transport short peptides (4–12 amino acid long) when expressed in yeast.…”

“…Mutation of soybean and M. truncatula YSL7 leads to reduced nitrogen fixation rates, as well as to an altered iron homeostasis response, in addition to dysregulation of other metabolic processes. In M. truncatula , ysl7 mutants accumulate more copper and iron in nodules, a likely consequence of the overexpression of the iron uptake machinery in roots (Castro‐Rodríguez et al ., 2021). Both MtYSL7 and GmYSL7 transport a similar substrate in vivo , since expressing GmYSL7 under the MtYSL7 promoter restores the WT phenotype in M. truncatula ysl7 mutants (Gavrin et al ., 2021).…”