Large-Scale Identification and Characterization of Heterodera avenae Putative Effectors Suppressing or Inducing Cell Death in Nicotiana benthamiana

Abstract

<i>Heterodera avenae</i> is one of the most important plant pathogens and causes vast losses in cereal crops. As a sedentary endoparasitic nematode, <i>H. avenae</i> secretes effectors that modify plant defenses and promote its biotrophic infection of its hosts. However, the number of effectors involved in the interaction between <i>H. avenae</i> and host defenses remains unclear. Here, we report the identification of putative effectors in <i>H. avenae</i> that regulate plant defenses on a large scale. Our results showed that 78 of the 95 putative effectors suppressed programmed cell death (PCD) triggered by BAX and that 7 of the putative effectors themselves caused cell death in <i>Nicotiana benthamiana</i>. Among the cell-death-inducing effectors, three were found to be dependent on their specific domains to trigger cell death and to be expressed in esophageal gland cells by <i>in situ</i> hybridization. Ten candidate effectors that suppressed BAX-triggered PCD also suppressed PCD triggered by the elicitor PsojNIP and at least one R-protein/cognate effector pair, suggesting that they are active in suppressing both pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). Notably, with the exception of isotig16060, these putative effectors could also suppress PCD triggered by cell-death-inducing effectors from <i>H. avenae</i>, indicating that those effectors may cooperate to promote nematode parasitism. Collectively, our results indicate that the majority of the tested effectors of <i>H. avenae</i> may play important roles in suppressing cell death induced by different elicitors in <i>N. benthamiana</i>.