ClBeclin1 Positively Regulates Citrus Defence Against Citrus Yellow Vein Clearing Virus Through Mediating Autophagy-Dependent Degradation of ClAPX1

Mol Plant Pathol. 2024 Dec;25(12):e70041. doi: 10.1111/mpp.70041.

Abstract

Autophagy, one of the most widespread and highly conserved protein degradation systems in eukaryotic cells, plays an important role in plant growth, development and stress response. Beclin 1 is a core component of the phosphatidylinositol 3-kinase (PI3K) autophagy complex and positively regulates plant immunity against viruses. The upregulation of Eureka lemon ClBeclin1 was observed in response to citrus yellow vein clearing virus (CYVCV) infection. However, the function of ClBeclin1 and the underlying mechanism during CYVCV colonisation remain unclear. Here, the resistance evaluation of the overexpression and silencing of ClBeclin1 in Eureka lemon hairy roots revealed it as a positive regulator of citrus immunity against CYVCV. Transcriptomic profiling and metabolic analyses along with genetic evidence implied that the overexpression of ClBeclin1 positively triggered reactive oxygen species (ROS)- and jasmonic acid (JA)-mediated immunity in citrus. The accumulation of ROS and JA contents was attributed to the autophagic degradation of the ROS scavenger ClAPX1 via ClBeclin1 overexpression. Exogenous application of either H2O2 or JA significantly reduced CYVCV colonisation and vein-clearing symptoms on the host. Collectively, our findings indicate that ClBeclin1 activation contributes to citrus immunity against CYVCV through triggering ROS- and JA-mediated defence responses, and the accumulation of ROS and JA resulted from the autophagic degradation of ClAPX1 by ClBeclin1.

Keywords: Citrus yellow vein clearing virus; ClAPX1 protein; ClBeclin1 protein; autophagy; jasmonic acid (JA); reactive oxygen species (ROS).

MeSH terms

  • Autophagy*
  • Citrus* / immunology
  • Citrus* / metabolism
  • Citrus* / virology
  • Cyclopentanes / metabolism
  • Disease Resistance / genetics
  • Gene Expression Regulation, Plant
  • Hydrogen Peroxide / metabolism
  • Oxylipins / metabolism
  • Plant Diseases* / immunology
  • Plant Diseases* / virology
  • Plant Immunity
  • Plant Proteins* / genetics
  • Plant Proteins* / metabolism
  • Plant Viruses / pathogenicity
  • Plant Viruses / physiology
  • Reactive Oxygen Species* / metabolism

Substances

  • Plant Proteins
  • Reactive Oxygen Species
  • jasmonic acid
  • Cyclopentanes
  • Oxylipins
  • Hydrogen Peroxide