Ferredoxin 1 is downregulated by the accumulation of abscisic acid in an ABI5-dependent manner to facilitate rice stripe virus infection in Nicotiana benthamiana and rice

Plant J. 2021 Aug;107(4):1183-1197. doi: 10.1111/tpj.15377. Epub 2021 Jul 10.

Abstract

Ferredoxin 1 (FD1) accepts and distributes electrons in the electron transfer chain of plants. Its expression is universally downregulated by viruses and its roles in plant immunity have been brought into focus over the past decade. However, the mechanism by which viruses regulate FD1 remains to be defined. In a previous report, we found that the expression of Nicotiana benthamiana FD1 (NbFD1) was downregulated following infection with potato virus X (PVX) and that NbFD1 regulates callose deposition at plasmodesmata to play a role in defense against PVX infection. We now report that NbFD1 is downregulated by rice stripe virus (RSV) infection and that silencing of NbFD1 also facilitates RSV infection, while viral infection was inhibited in a transgenic line overexpressing NbFD1, indicating that NbFD1 also functions in defense against RSV infection. Next, a RSV-derived small interfering RNA was identified that contributes to the downregulation of FD1 transcripts. Further analysis showed that the abscisic acid (ABA) which accumulates in RSV-infected plants also represses NbFD1 transcription. It does this by stimulating expression of ABA insensitive 5 (ABI5), which binds the ABA response element motifs in the NbFD1 promoter, resulting in negative regulation. Regulation of FD1 by ABA was also confirmed in RSV-infected plants of the natural host rice. The results therefore suggest a mechanism by which virus regulates chloroplast-related genes to suppress their defense roles.

Keywords: ABA; ABI5; ferredoxin 1; rice stripe virus; transcription repression; virus-derived small interfering RNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abscisic Acid
  • Arabidopsis / genetics
  • Disease Resistance / genetics
  • Down-Regulation
  • Ferredoxins / genetics*
  • Ferredoxins / metabolism
  • Gene Expression Regulation, Plant
  • Host-Pathogen Interactions / physiology
  • Nicotiana / genetics
  • Nicotiana / metabolism
  • Nicotiana / virology*
  • Oryza / genetics
  • Oryza / metabolism
  • Oryza / virology*
  • Plant Diseases / virology
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Plants, Genetically Modified
  • Promoter Regions, Genetic
  • RNA, Small Interfering
  • Tenuivirus / genetics
  • Tenuivirus / pathogenicity*

Substances

  • Ferredoxins
  • Plant Proteins
  • RNA, Small Interfering
  • Abscisic Acid