A conserved fungal effector disturbs Ca2+ sensing and ROS homeostasis to induce plant cell death

Abstract

Acting as a major Ca2+ sensor, calmodulin (CaM) activates target proteins to regulate a variety of cellular processes. Here, we report that CaM–target binding is disturbed by a fungal virulence effector PdCDIE1 (Penicillium digitatum Cell Death-Inducing Effector 1), which results into reactive oxygen species (ROS)-dependent plant cell death. PdCDIE1 is an evolutionarily conserved fungal effector that exhibits plant cell death-inducing activity and contributes significantly to pathogen virulence. PdCDIE1 interacts with a plant heat shock protein Hsp70 that is antagonistic to ROS-dependent plant cell death. Hsp70 is a bona fide target of CaM and its CaM-binding domain also interacts with N-terminal PdCDIE1. The interaction between CaM and Hsp70 in citrus fruit is disturbed during pathogen infection but recovered during ΔPdCDIE1 mutant infection. Application of a CaM inhibitor and silencing of CaM genes induce plant cell death and high levels of ROS as PdCDIE1 does. These results reveal a molecular framework of effector-triggered susceptibility which integrates Ca2+ sensing and ROS homeostasis to induce plant cell death. Calmodulin (CaM) activates target proteins to regulate a variety of cellular processes. Here, the authors report that CaM–target binding is disturbed by a fungal effector PdCDIE1, leading to ROS-dependent plant cell death.