KIN3 impacts arbuscular mycorrhizal symbiosis and promotes fungal colonisation in Medicago truncatula

Abstract

Arbuscular mycorrhizal fungi help their host plant in the acquisition of nutrients, and this association is itself impacted by soil nutrient levels. High phosphorus levels inhibit the symbiosis, whereas high nitrogen levels enhance it. The genetic mechanisms regulating the symbiosis in response to soil nutrients are poorly understood. Here, we characterised the symbiotic phenotypes in four Medicago truncatula Tnt1-insertion mutants affected in arbuscular mycorrhizal colonisation. We located their Tnt1 insertions and identified alleles for two genes known to be involved in mycorrhization, RAM1 and KIN3. We compared the effects of the kin3-2 and ram1-4 mutations on gene expression, revealing that the two genes alter the expression of overlapping but not identical gene sets, suggesting that RAM1 acts upstream of KIN3. Additionally, KIN3 appears to be involved in the suppression of plant defences in response to the fungal symbiont. KIN3 is located on the endoplasmic reticulum of arbuscule-containing cortical cells, and kin3-2 mutants plants hosted significantly fewer arbuscules than the wild type. KIN3 plays an essential role in the symbiotic response to soil nitrogen levels, as, contrary to wild-type plants, the kin3-2 mutant did not exhibit increased root colonisation under high nitrogen.

ARBUSCULAR MYCORRHIZA-INDUCED KINASES AMK8 and AMK24 associate with the receptor-like kinase KINASE3 to regulate arbuscular mycorrhizal symbiosis in Lotus japonicus

“…S3, E and F ). In sum, KIN3 is required for the development of arbuscules in L. japonicus , similar to MtKIN3 and OsARK1 ( Bravo et al 2016 ; Roth et al 2018 ; Irving et al 2022 ).…”

“…2 and Supplemental Fig. S3 ), indicating the important role of KIN3 in arbuscule development from the beginning as in M. truncatula , probably in autoregulation of AM fungi in individual cells rather than in the initiation of AM colonization ( Irving et al 2022 ). Osark1 mutants displayed comparable mycorrhization to the wild type at 3 wpi but fewer fungal structures at 6 wpi, supporting the role of OsARK1 in maintaining AM symbiosis ( Roth et al 2018 ).…”

“…In addition to LysM RLKs, KINASE3 (KIN3) is required for arbuscule fine branching in M. truncatula ( Bravo et al 2016 ; Irving et al 2022 ). The KIN3 homolog ARBUSCULAR RECEPTOR-LIKE KINASE1 (ARK1) was previously identified as a PAM-specific RLK by membrane proteome analysis of mycorrhizal maize ( Zea mays ) and rice roots ( Roth et al 2018 ).…”

Walking on a tightrope: cell wall‐associated kinases act as sensors and regulators of immunity and symbiosis

“…In rice, the ARBUSCULAR RECEPTOR-LIKE KINASE 1 and 2, belonging to an undefined receptor-like kinase (RLK) subfamily, govern postarbuscule development and regulation of the AM association (Roth et al, 2018;Montero et al, 2021). In Medicago truncatula, KIN3, an active kinase, accumulates in the endoplasmic reticulum of arbusculated cells, exerting a partial suppression of the host immune response (Irving et al, 2022) and a similar phenotype has been shown for its orthologous protein in Lotus japonicus (Leng et al, 2023). Additionally, the rice kinase gene OsADK1, specifically induced in arbusculated cells, proves indispensable for arbuscular development during AM symbiosis, and the protein accumulates in the nucleus (Guo et al, 2022;Shi et al, 2022).…”

Microbe‐dependent and independent nitrogen and phosphate acquisition and regulation in plants

“…The expression of Kinase 3 (KIN3) is significantly induced during mycorrhizal interactions, and it appears to play an important role that depends on nutrient supply. Recent studies in M. truncatula showed that kin3 mutants display a much lower mycorrhizal infection rate than the wild-type under high-nitrogen conditions, while root colonization under low-nitrogen conditions was not affected, indicating that it plays a role in adjusting the symbiotic response according to soil nitrogen levels (Irving et al, 2022). Interestingly, Shi et al (2022), showed that the expression of the MtKIN3 homolog OsARK1 is regulated by PHRs in rice, further indicating crosstalk between nitrogen and Pi signaling.…”