Abstract
Plants produce cytokinin (CK) hormones for controlling key developmental processes like source/sink distribution, cell division or programmed cell-death. Some plant pathogens have been shown to produce CKs but the function of this mimicry production by non-tumor inducing pathogens, has yet to be established. Here we identify a gene required for CK biosynthesis, CKS1, in the rice blast fungus Magnaporthe oryzae. The fungal-secreted CKs are likely perceived by the plant during infection since the transcriptional regulation of rice CK-responsive genes is altered in plants infected by the mutants in which CKS1 gene was deleted. Although cks1 mutants showed normal in vitro growth and development, they were severely affected for in planta growth and virulence. Moreover, we showed that the cks1 mutant triggered enhanced induction of plant defenses as manifested by an elevated oxidative burst and expression of defense-related markers. In addition, the contents of sugars and key amino acids for fungal growth were altered in and around the infection site by the cks1 mutant in a different manner than by the control strain. These results suggest that fungal-derived CKs are key effectors required for dampening host defenses and affecting sugar and amino acid distribution in and around the infection site.
Highlights
Plant pathogens have evolved sophisticated strategies to manipulate host biological processes during infection [1,2]. (Hemi)biotrophic pathogens produce and secrete effector proteins and metabolites to hijack cellular metabolism of the infected tissues to their own benefit
The protein encoded by this gene presents all the features of a tRNA-Isopentenyl transferase (IPT) enzyme, the type of which is known in plants and yeast, and suspected in many fungi, to perform the first step of one of the CK biosynthesis pathways [25,40,45]
The Cytokinin Synthesis 1 (CKS1) protein is the only one found to contain an IPT domain in the rice blast fungal genome (S1 Table). These results suggest that the CK biosynthesis pathway controlled by CKS1 is probably the only one in the rice blast fungus
Summary
Plant pathogens have evolved sophisticated strategies to manipulate host biological processes during infection [1,2]. (Hemi)biotrophic pathogens produce and secrete effector proteins and metabolites to hijack cellular metabolism of the infected tissues to their own benefit. A first layer of plant defenses is induced by the perception of pathogen- or microbe-associated molecular patterns, like flagellin from bacteria or chitin from fungi [5]. These basal defense responses consist of an early accumulation of reactive oxygen species (ROS), a thickening of the cell wall, and production of metabolites/enzymes with antimicrobial activities. To limit these defenses triggered by chitin perception by the plant’s chitin receptor, fungal pathogens like Magnaporthe oryzae secrete chitin-binding effectors that enable escape from the host recognition system [6]. Pathogens interfere with other steps of plant immunity like signaling cascades following recognition and transcriptional regulators of host defenses [2,7]
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