The role of CLAVATA signalling in the negative regulation of mycorrhizal colonization and nitrogen response of tomato

Abstract

Plants form mutualistic nutrient acquiring symbioses with microbes, including arbuscular mycorrhizal fungi. The formation of these symbioses is costly and plants employ a negative feedback loop termed autoregulation of mycorrhizae (AOM) to limit arbuscular mycorrhizae (AM) formation. We provide evidence for the role of one leucine-rich-repeat receptor like kinase (FAB), a hydroxyproline O-arabinosyltransferase enzyme (FIN) and additional evidence for one receptor like protein (SlCLV2) in the negative regulation of AM formation in tomato. Reciprocal grafting experiments suggest that the FAB gene acts locally in the root, while the SlCLV2 gene may act in both the root and the shoot. External nutrients including phosphate and nitrate can also strongly suppress AM formation. We found that FAB and FIN are required for nitrate suppression of AM but are not required for the powerful suppression of AM colonisation by phosphate. This parallels some of the roles of legume homologs in the autoregulation of the more recently evolved symbioses with nitrogen-fixing bacteria leading to nodulation. This deep homology in the symbiotic role of these genes suggests that in addition to the early signalling events that lead to the establishment of AM and nodulation, the autoregulation pathway might also be considered part of the common symbiotic toolkit that enabled plants to form beneficial symbioses.

Systemic Optimization of Legume Nodulation: A Shoot-Derived Regulator, miR2111

“…In tomato, clv2 mutants exhibit increased mycorrhizal colonization rates (Wang et al, 2018). Moreover, grafting experiments using tomato clv2 demonstrated that CLV2 might act in both the shoot and roots to regulate AMF colonization (Wang et al, 2021). Since CLV2 physically interacts with shoot-acting LRR-RLK of legumes such as SUNN via CORYNE in M. truncatula (Crook et al, 2016), further investigation of the relationship between CLV2 and AM symbiosis in non-legumes is required.…”

A rulebook for peptide control of legume–microbe endosymbioses

“…By contrast, CLE peptides have been established as negative regulators of RN and AM symbiosis. Several genes encoding CLE peptides were found to be induced in roots in response to plant interactions with both AM fungi and rhizobia, as well as with macronutrients, such as N and P [9,10,[20][21][22][23][24]. Fully processed CLE peptides are 12-13-amino acids long and often posttranslationally modified by proline hydroxylation and arabinosylation [25].…”

“…These LRR-RLKs act as negative regulators of RN and AM symbiosis [29, [46][47][48][49][50][51][52]. Interestingly, this phenomenon does not appear to be only specific to legumes, because CLV1 orthologs in the non-legumes Brachypodium distachyon and tomato were recently reported to act as negative regulators of AM [9,23]. Although no functional connection to AM-induced CLE signaling was demonstrated in these species, these findings suggest that autoregulation of symbiosis is conserved across plant clades.…”

“…N 2 -fixing nodules are a major P sink and, therefore, nodule formation is inhibited when Pi availability to the plant is low; such inhibition was not observed in P. vulgaris nark mutants [58] (Figure 2B). Interestingly, recent evidence suggests that N regulation of AM symbiosis is also regulated by CLV1-type LRR-RLKs (Figure 2C): tomato FAB1 was shown to be involved in N regulation of AM symbiosis, although the cognate N-induced, AM-regulatory CLE peptide remains elusive [23]. The role of CLV1-type receptors in AM symbiosis regulation based on P is less clear (Figure 2D): although overexpression of the P-induced MtCLE33 negatively regulates AM symbiosis biosynthesis in a MtSUNN-dependent manner [9], clv1-like receptor mutants do not suppress AM inhibition by high P in legumes and non-legumes [9,23,58,59].…”

“…Interestingly, recent evidence suggests that N regulation of AM symbiosis is also regulated by CLV1-type LRR-RLKs (Figure 2C): tomato FAB1 was shown to be involved in N regulation of AM symbiosis, although the cognate N-induced, AM-regulatory CLE peptide remains elusive [23]. The role of CLV1-type receptors in AM symbiosis regulation based on P is less clear (Figure 2D): although overexpression of the P-induced MtCLE33 negatively regulates AM symbiosis biosynthesis in a MtSUNN-dependent manner [9], clv1-like receptor mutants do not suppress AM inhibition by high P in legumes and non-legumes [9,23,58,59]. This indicates that, in high P conditions, CLV1-independent mechanisms are mainly responsible for the suppression of AM symbiosis, although additional layers of regulation via CLE-SUNN modules may exist.…”