Cytokinin inhibits fungal development and virulence by targeting cellular trafficking
AbstractCytokinin (CK) is an important plant developmental regulator, having activities in many aspects of plant life and its response to the environment. CKs are involved in diverse processes in the plant, including stem-cell maintenance, vascular differentiation, growth and branching of roots and shoots, leaf senescence, nutrient balance and stress tolerance. In some cases, phytopathogens secrete CKs. It has been suggested that to achieve pathogenesis in the host, CK-secreting biotrophs manipulate CK signaling to regulate the host cell cycle and nutrient allocation. CK is known to induce host plant resistance to several classes of phytopathogens from a handful of works, with induced host immunity via salicylic acid signaling suggested to be the prevalent mechanism for this host resistance.Here, we show that CK directly inhibits the growth, development, and virulence of fungal phytopathogens. Focusing on Botrylis cinerea (Bc), we demonstrate that various aspects of fungal development can be reversibly inhibited by physiological concentrations of CK. We also found that CK affects both budding and fission yeast in a similar manner. Investigating the mechanism by which CK influences fungal development, we found that CK affects cellular trafficking in Bc, lowering endocytic rates and endomembrane compartment sizes, likely leading to reduced growth rates and arrested developmental programs. Mutant analyses in yeast confirmed that the endocytic pathway is a CK target.Our work uncovers a remarkably conserved role for a plant growth hormone in fungal biology, suggesting that co-evolution between pathogen and host resulted in fascinating molecular adaptations on fundamental processes in eukaryotic biology.ImportanceCytokinins (CKs), important plant growth/ developmental hormones, have previously been associated with host disease resistance. Here, we demonstrate that CK directly inhibits the growth, development, and virulence of B. cinerea (Bc) and many additional phytopathogenic fungi. Molecular and cellular analyses revealed that CK is not toxic to Bc, but rather, Bc likely recognizes CK and responds to it, resulting in cell cycle and individual cell growth retardation, via downregulation of endocytic trafficking. Mutant analyses in yeast confirmed that the endocytic pathway is a CK target. Our work demonstrates a conserved role for CK in yeast and fungal biology, suggesting that co-evolution between fungal pathogens and plant hosts caused molecular adaptations in cellular trafficking, a fundamental process in eukaryotic biology.
