Many ways to TOPLESS – manipulation of plant auxin signalling by a cluster of fungal effectors

Abstract

Plant biotrophic pathogens employ secreted molecules, called effectors, to suppress the host immune system and redirect the host's metabolism and development in their favour. Putative effectors of the gall-inducing maize pathogenic fungus Ustilago maydis were analysed for their ability to induce auxin signalling in plants.Using genetic, biochemical, cell-biological, and bioinformatic approaches we functionally elucidate a set of five, genetically linked effectors, called Topless (TPL) interacting protein (Tips) effectors that induce auxin signalling.We show that Tips induce auxin signalling by interfering with central corepressors of the TPL family. CRISPR-Cas9 mutants and deletion strain analysis indicate that the auxin signalling inducing subcluster effectors plays a redundant role in virulence.Although none of the Tips seem to have a conserved interaction motif, four of them bind solely to the N-terminal TPL domain and, for Tip1 and Tip4, we demonstrate direct competition with auxin/indole-3-acetic acid transcriptional repressors for their binding to TPL class of corepressors. Our findings reveal that TPL proteins, key regulators of growth-defence antagonism, are a major target of the U. maydis effectome.

The fungal pathogen Ustilago maydis targets the maize corepressor RELK2 to modulate host transcription for tumorigenesis

“…Interestingly, despite their potential functional redundancy, individual knockouts of Tip6 and Nkd1 resulted in virulence deficiencies, indicating their unique roles during infection. However, the simultaneous deletion of multiple effectors led to a more pronounced virulence deficiency, highlighting the collective impact of these proteins on manipulating host responses (Bindics et al, 2022;Khan et al, 2023). It is worth noting that the maize RELK2 protein-interacting partners are located on different chromosomes, which may suggest a strategic evolution of effector-host interactions to target multiple TPL proteins effectively (Khan et al, 2023).…”

“…Moreover, the Nkd1‐TPL interaction hinders TPL recruitment by the Aux/IAA repressor, resulting in the derepression of auxin signaling (Navarrete et al ., 2022). The U. maydis cluster gene 6A encodes a family of five effector proteins known as Tips, which play a role in inducing auxin signaling (Bindics et al ., 2022). Although neither of them contains an EAR domain, Tip1 and Tip4 compete with the Aux/IAA repressor for TPL binding, ultimately promoting the expression of auxin‐responsive genes (Bindics et al ., 2022).…”

“…The U. maydis cluster gene 6A encodes a family of five effector proteins known as Tips, which play a role in inducing auxin signaling (Bindics et al ., 2022). Although neither of them contains an EAR domain, Tip1 and Tip4 compete with the Aux/IAA repressor for TPL binding, ultimately promoting the expression of auxin‐responsive genes (Bindics et al ., 2022). Additionally, the effector protein Jsi1, through its interaction with maize TPL, promotes the induction of jasmone/ethylene (JA/ET; Darino et al ., 2020).…”

A transcriptional activator effector ofUstilago maydisregulates hyperplasia in maize during pathogen-induced tumor formation

“…These effectors contain a nucleus localization signal, tandem repeat DNA binding domain and transcriptional activation domain, which can function independently as transcription factors to activate host gene expression. On the other hand, several effectors are not transcription factor themselves, but control host gene expression through interacting with host transcription factors 4 , recruit the suppressors of transcription factors [5][6][7][8] , or disrupt the assembly of transcription units 9,10 , eventually leading to the inhibition or activation of host gene expression, respectively.…”

Row1, a member of a new family of conserved fungal proteins involved in infection, is required for appressoria functionality in Ustilago maydis

“…In the plant pathogenic fungus U. maydis , many effectors and PCWDEs have been identified and characterized (for examples see Lanver et al, 2017; Zuo et al, 2019; Ludwig et al, 2021; Navarrete et al, 2021; Moreno-Sánchez et al, 2021; Ökmen et al, 2022; Bindics et al, 2022). When this fungus penetrates the plant, it interacts closely with the surrounding plant plasma (Doehlemann et al, 2008), where it secretes proteins that modify host cell structure and function (Win et al ., 2012; Lanver et al ., 2017).…”