MAPKs trigger antiviral immunity by directly phosphorylating a rhabdovirus nucleoprotein in plants and insect vectors

Zhi-Hang Ding1, Qiang Gao1,2, Xin Tong1,2

  • 1State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

The Plant Cell
|May 14, 2022
PubMed

Insights

Mitogen-activated protein kinase (MAPK) and extracellular signal-regulated kinase (ERK) directly phosphorylate the barley yellow striate mosaic virus (BYSMV) nucleoprotein, triggering immunity. This cross-kingdom signaling inhibits virus infection in both plants and insect vectors.

Area of Science:

  • Plant pathology
  • Virology
  • Molecular biology
  • Immunology

Background:

  • Mitogen-activated protein kinase (MAPK) and extracellular signal-regulated kinase (ERK) signaling pathways are crucial for converting external stimuli into immune responses.
  • The role of MAPK/ERK signaling in inducing virus immunity through direct phosphorylation of viral components is not well understood.
  • Barley yellow striate mosaic virus (BYSMV), a plant cytorhabdovirus, causes significant economic damage and is transmitted by the small brown planthopper (SBPH).

Purpose of the Study:

  • To investigate whether MAPK/ERK signaling directly phosphorylates viral effectors to induce immunity against BYSMV.
  • To elucidate the mechanism by which plant and insect MAPK/ERK pathways interact with BYSMV.
  • To determine the impact of this interaction on BYSMV infection in both barley plants and SBPH vectors.

Main Methods:

  • Identified interactions between barley MPK3 (HvMPK3), planthopper LsERK, and BYSMV nucleoprotein (N).
  • Utilized phosphorylation site analysis (serine 290) and phosphomimetic mutants (S290D).
  • Employed overexpression of HvMPK3, MAPK pathway inhibitor (U0126), and LsERK knockdown in SBPHs to assess BYSMV infection levels.

Main Results:

  • HvMPK3 and LsERK directly phosphorylate the BYSMV N protein at serine 290.
  • Overexpression of HvMPK3 inhibited BYSMV infection, while U0126 treatment increased susceptibility in barley.
  • Knockdown of LsERK enhanced BYSMV infection in SBPHs.
  • A phosphomimetic mutant (S290D) abolished BYSMV infection by disrupting N self-interaction and N-RNA complex formation.

Conclusions:

  • The conserved MAPK and ERK signaling pathways directly phosphorylate the BYSMV nucleoprotein, initiating immunity against this virus.
  • This direct phosphorylation mechanism represents a cross-kingdom immune response in both host plants and insect vectors.
  • The findings reveal a novel strategy for controlling BYSMV by targeting the conserved MAPK/ERK-mediated phosphorylation of the viral nucleoprotein.

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