Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant jasmonate/ethylene signaling

Abstract

 Ustilago maydis (U. maydis) is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins which suppress immune responses and redirect the host metabolism in favor of the pathogen. As effectors play a critical role during plant colonization, their identification and functional characterization is essential to understanding biotrophy and disease.  Using biochemical, molecular, and transcriptomic techniques, we performed a functional characterization of the U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1).  Jsi1 interacts with several members of the plant co-repressor family Topless/Topless related (TPL/TPR). Jsi1 expression in Zea mays (Z. mays) and Arabidopsis thaliana (A. thaliana) leads to transcriptional induction of the ethylene response factor (ERF) branch of the jasmonate/ethylene (JA/ET) signaling pathway. In A. thaliana, activation of the ERFbranch leads to biotrophic susceptibility. Jsi1 likely activates the ERF-branch via an EAR motif, which resembles EAR motifs from plant ERF transcription factors, that interacts with TPL/TPR proteins.  EAR motif-containing effector candidates were identified from different fungal species including Magnaporthe oryzae, Sporisorium scitamineum, and Sporisorium reilianum. Interaction between plant TPL proteins and these effector candidates from biotrophic and hemibiotrophic fungi indicates the convergent evolution of effectors modulating the TPL/TPR co-repressor hub.

mRNA Inventory of Extracellular Vesicles from Ustilago maydis

“…Biotrophic colonisation by U. maydis is accompanied by extensive reprogramming of metabolism, redox status, and hormone signalling in the infected plant tissues [ 79 ]. The fungus deploys effectors to divert metabolites away from biosynthesis of lignin [ 92 ] and salicylic acid (SA; [ 77 ]), and induces the jasmonate/ethylene signalling pathway to counter SA-mediated defence [ 93 ]. U. maydis also harbours metabolic enzymes lacking signal peptides that can synthesise [ 94 , 95 ], degrade [ 96 ], or potentially alter metabolic flux into biosynthesis of plant hormones [ 41 ].…”

TOPLESS promotes plant immunity by repressing auxin signaling and is targeted by the fungal effector Naked1

“…Jsi1 lacks any homology with Nkd1 but has a DLNxxPtype EAR motif that mediates its interaction with one of the C-terminal WD40 domains of TPL/TPRs. Deletion of jsi1 does not lead to virulence defects and its expression in planta induces an overlapping but different set of hormone-responsive genes, predominantly from the jasmonate/ethylene branch (Darino et al, 2021). Therefore, the different domains of TPL/TPR proteins seem to control different hormone-responsive gene sets.…”

mRNA inventory of extracellular vesicles from Ustilago maydis

“…Biotrophic colonisation by U. maydis is accompanied by extensive reprogramming of metabolism, redox status, and hormone signalling in the infected plant tissues [75]. The fungus deploys effectors to divert metabolites away from biosynthesis of lignin [88] and salicylic acid (SA; [73]), and induces the jasmonate/ethylene signalling pathway to counter SA-mediated defence [89]. U. maydis also harbours metabolic enzymes lacking signal peptides that can synthesise [90,91], degrade [92], or potentially alter metabolic flux into biosynthesis of plant hormones [41].…”