Fungal effector Jsi1 hijacks plant JA/ET signaling through Topless

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 hostmetabolism in favor of the pathogen. Here we describe a novel strategy by which U. maydis induces plant jasmonate/ethylene (JA/ET) hormone signaling and thereby biotrophic susceptibility. The U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1) possesses an ethylene-responsive element binding factor-associated amphiphilic repression (EAR) motif, DLNxxP, which interacts with the second WD40 domain of the conserved plant co-repressor family Topless/Topless related (TPL/TPR). Jsi1 interaction with TPL/TPRs leads to derepression of the ethylene response factor (ERF) branch of the JA/ET signaling pathway, supporting biotrophic susceptibility. Jsi1 likely activates the ERF branch by interfering with the binding of endogenous DLNxxP motif-containing ERF transcription factors to TPL/TPR proteins. The identification of effector proteins possessing a DLNxxP motif in different fungal species with biotrophic and hemibiotrophic lifestyles together with the validation of the interaction between such effectors from Magnaporthe oryzae (M. oryzae), Sporisorium scitamineum (S. scitamineum), and S. reilianum with TPL proteins indicates the convergent evolution of effectors for modulating the TPL/TPR co-repressor hub.

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

“…It is also in line with previous observations (Navarro et al, 2006) where auxin-mediated promotion of Pst susceptibility was not effective when R gene-mediated responses were activated. Our finding that the EAR-motif is conserved among most Nkd1 orthologs, as well as of other TPL-binding effectors in U. maydis and other pathogens (Darino et al, 2019, Petre et al, 2015, Gawehns, 2014, suggests that fungi widely exploit the antagonism between growth and defense by targeting the central co-repressor TOPLESS. The discovery of the post-transcriptional mechanism through which TOPLESS-dependent elevated auxin signaling inhibits PTI awaits further research.…”

“…10-25 μl of the extracts were analyzed by SDS-PAGE followed by western blot with α-HA or α-TPL (Eurogentec, Belgium). The latter (polyclonal) antibodies were developed in rabbit against the peptide CNEQLSKYGDTKSAR, that is conserved across TPL/TPR proteins (Darino et al, 2019). Experiments were repeated 2 times.…”

All Roads Lead to Susceptibility: The Many Modes of Action of Fungal and Oomycete Intracellular Effectors

“…Finally, the transcriptional repressor Topless (TPL), which interacted with the oomycete effector HaRXLR21 as that has been reported by Weßling et al. (2014) , is a target of the fungal effectors Jsi1 ( Darino et al., 2019 ) and MLP124017 ( Petre et al., 2015 ). There is thus increasingly compelling evidence that effectors from pathogenic microbes of different kingdoms have converged onto conserved, key regulators of immunity.…”

“…This leads to an induction of ET signaling by preventing the formation of the ethylene response factor (ERF)–TPL/TPR complex. Interestingly, several fungal effectors have been predicted to possess EAR motifs, suggesting their potential to also bind TPL/TPR proteins ( Darino et al., 2019 ). Recently, the P .…”

Engineering Smut Resistance in Maize by Site-Directed Mutagenesis of LIPOXYGENASE 3

“…Other effectors like the secreted chorismate mutase (Cmu1) converts chorismate to prephenate, by which a substrate for SA biosynthesis is removed (Djamei et al, 2011). Besides SA signaling, U. maydis has been shown to actively manipulate JA/ET signaling in maize by secretion of the Jsi1 effector that targets the c-terminal domain of TOPLESS (Darino et al, 2019). Furthermore, U. maydis directly produces auxin during infection (Reineke et al, 2008) and has also been shown to generate cytokinins, which indicates that it uses various phytohormone signaling pathways to manipulate its host (Morrison et al, 2015).…”