Phosphatidylinositol-phospholipase C3 negatively regulates the hypersensitive response via complex signaling with MAP kinase, phytohormones, and reactive oxygen species in Nicotiana benthamiana

J Exp Bot. 2023 Aug 17;74(15):4721-4735. doi: 10.1093/jxb/erad184.

Abstract

Phospholipid signaling plays important roles in plant immune responses. Here, we focused on two phospholipase C3 (PLC3) orthologs in the Nicotiana benthamiana genome, NbPLC3-1 and NbPLC3-2. We generated NbPLC3-1 and NbPLC3-2-double-silenced plants (NbPLC3s-silenced plants). In NbPLC3s-silenced plants challenged with Ralstonia solanacearum 8107, induction of hypersensitive response (HR)-related cell death and bacterial population reduction was accelerated, and the expression level of Nbhin1, a HR marker gene, was enhanced. Furthermore, the expression levels of genes involved in salicylic acid and jasmonic acid signaling drastically increased, reactive oxygen species production was accelerated, and NbMEK2-induced HR-related cell death was also enhanced. Accelerated HR-related cell death was also observed by bacterial pathogens Pseudomonas cichorii, P. syringae, bacterial AvrA, oomycete INF1, and TMGMV-CP with L1 in NbPLC3s-silenced plants. Although HR-related cell death was accelerated, the bacterial population was not reduced in double NbPLC3s and NbCoi1-suppressed plants nor in NbPLC3s-silenced NahG plants. HR-related cell death acceleration and bacterial population reduction resulting from NbPLC3s-silencing were compromised by the concomitant suppression of either NbPLC3s and NbrbohB (respiratory oxidase homolog B) or NbPLC3s and NbMEK2 (mitogen activated protein kinase kinase 2). Thus, NbPLC3s may negatively regulate both HR-related cell death and disease resistance through MAP kinase- and reactive oxygen species-dependent signaling. Disease resistance was also regulated by NbPLC3s through jasmonic acid- and salicylic acid-dependent pathways.

Keywords: Nicotiana benthamiana; Ralstonia solanacearum; Hypersensitive response; MAP kinase; jasmonic acid; phosphatidylinositol-phospholipase C3; reactive oxygen species; salicylic acid; virus-induced gene silencing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Disease Resistance
  • Gene Expression Regulation, Plant
  • Mitogen-Activated Protein Kinases / metabolism
  • Nicotiana* / metabolism
  • Plant Diseases / microbiology
  • Plant Growth Regulators* / metabolism
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Reactive Oxygen Species / metabolism
  • Salicylic Acid / metabolism

Substances

  • jasmonic acid
  • Plant Growth Regulators
  • Reactive Oxygen Species
  • Plant Proteins
  • Mitogen-Activated Protein Kinases
  • Salicylic Acid