Lotus japonicus Nuclear Factor YA1, a nodule emergence stage‐specific regulator of auxin signalling

Abstract

Organogenesis of legume root nodules begins with the nodulation factor-dependent stimulation of compatible root cells to initiate divisions, signifying an early nodule primordium formation event. This is followed by cellular differentiation, including cell expansion and vascular bundle formation, and we previously showed that Lotus japonicus NF-YA1 is essential for this process, presumably by regulating three members of the SHORT INTERNODES/STYLISH (STY) transcription factor gene family. In this study, we used combined genetics, genomics and cell biology approaches to characterize the role of STY genes during root nodule formation and to test a hypothesis that they mediate nodule development by stimulating auxin signalling. We show here that L. japonicus STYs are required for nodule emergence. This is attributed to the NF-YA1-dependent regulatory cascade, comprising STY genes and their downstream targets, YUCCA1 and YUCCA11, involved in a local auxin biosynthesis at the post-initial cell division stage. An analogous NF-YA1/STY regulatory module seems to operate in Medicago truncatula in association with the indeterminate nodule patterning. Our data define L. japonicus and M. truncatula NF-YA1 genes as important nodule emergence stage-specific regulators of auxin signalling while indicating that the inductive stage and subsequent formation of early nodule primordia are mediated through an independent mechanism(s).

Regulation of the Later Stages of Nodulation Stimulated by IPD3/CYCLOPS Transcription Factor and Cytokinin in Pea Pisum sativum L.

“…Moreover, up-regulation in wild type and cytokinin treated mutant was shown for a set of genes encoding auxin-regulated proteins. Since the SHI/STY may be the direct regulators of auxin biosynthesis, they are important for the early stages of nodule organogenesis but seem to be also required for subsequent nodule development [ 96 ]. In L. japonicus , the SHI/STY was found to promote the differentiation of nodule structure, including an increase in cell size and the formation of vascular bundles [ 97 ].…”

At the Root of Nodule Organogenesis: Conserved Regulatory Pathways Recruited by Rhizobia

“…In L. japonicus, the roles of the NF-YA1 and NF-YB1 genes in nodule development have also been reported, and these genes regulate LR development as well [37]. LjNF-YA1 stimulates the expression of the SHORT INTERNODES/STYLISH (STY) genes encoding transcription factors which are required for nodule emergence and differentiation and which activate the expression of auxin biosynthesis genes [89,90]. Moreover, the miR169-regulated AtNF-YA2 and AtNF-YA10 genes in A. thaliana are involved in root growth and LR development, suggesting that the miR169-NF-YA module is a basic regulator of the root developmental program [47].…”

Auxin Response Factor 2 (ARF2), ARF3, and ARF4 Mediate Both Lateral Root and Nitrogen Fixing Nodule Development in Medicago truncatula

“…Moreover, although both organs differ in the environmental stimuli and function, their developmental programs converged in the generation and interpretation of auxin maximum (Herrbach et al, 2014;Xiao et al, 2014;Schiessl et al, 2019). In addition, it was recently shown that Nuclear Factor YA (NF-YA) genes are important regulators of auxin signaling during nodule development via the direct control of SHORT INTERNODES/STYLISH (STY) transcription factor genes and their downstream targets, YUCCA1 and YUCCA11, involved in auxin biosynthesis (Shrestha et al, 2020). This implies that auxin biosynthesis, signaling, and responses must be integrated with the nodulation program, which is initiated by the LysM domain receptor kinases MtNFP (Nod Factor Perception, Amor et al, 2003) and MtLYK3 (Smit et al, 2007) in M. truncatula and followed by the activation of a number of transcription factors such as the ERF transcription factor MtERN1 (Ethylene response factor Required for Nodulation 1) (Middleton et al, 2007) and the three subunits of the NF-Y heterotrimeric complex (Combier et al, 2006;Laporte et al, 2014;Baudin et al, 2015).…”