A fungal effector hijacks conserved plant GSK3-like kinases to reprogram host cell identity
TL;DR
This work shows that the maize smut fungus Ustilago maydis deploys the effector Iag1 to reprogram host cell fate by targeting the conserved GSK3-like kinase BIN2, and indicates that short motifs provide an evolutionarily flexible strategy for targeting these central regulatory nodes.
Abstract
Stable developmental programs normally resist reprogramming, yet pathogens can override these constraints to induce profound tissue and cellular remodeling. How microbial pathogens access conserved developmental signaling networks to reprogram host growth and differentiation remains poorly understood. Here, we show that the maize smut fungus Ustilago maydis deploys the effector Iag1 to reprogram host cell fate by targeting the conserved GSK3-like kinase BIN2. Iag1 contains a PPNT short interaction motif found also in plant viral effectors that mediates its association with BIN2 and related maize GSK3-like kinases and is essential for effector activity and full fungal virulence. This interaction attenuates BIN2-dependent signaling, reduces phosphorylation of the BIN2 substrate BES1, and triggers extensive transcriptional reprogramming consistent with coordinated perturbation of brassinosteroid, auxin, and other BIN2-regulated developmental pathways. These changes result in extensive epidermal developmental reprogramming, including loss of stomatal identity, altered cell division orientation, and aberrant cell expansion. Together, our findings identify GSK3-like kinases as conserved developmental signaling hubs that pathogens can exploit to unlock host developmental plasticity and suggest that short motifs provide an evolutionarily flexible strategy for targeting these central regulatory nodes.