Maize Phenylalanine Ammonia-Lyases Contribute to Resistance to Sugarcane Mosaic Virus Infection, Most Likely Through Positive Regulation of Salicylic Acid Accumulation

Mol Plant Pathol. 2019 Oct;20(10):1365-1378. doi: 10.1111/mpp.12817. Epub 2019 Sep 5.

Abstract

Sugarcane mosaic virus (SCMV) is a pathogen of worldwide importance that causes dwarf mosaic disease on maize (Zea mays). Until now, few maize genes/proteins have been shown to be involved in resistance to SCMV. In this study, we characterized the role of maize phenylalanine ammonia-lyases (ZmPALs) in accumulation of the defence signal salicylic acid (SA) and in resistance to virus infection. SCMV infection significantly increased SA accumulation and expression of SA-responsive pathogenesis-related protein genes (PRs). Interestingly, exogenous SA treatment decreased SCMV accumulation and enhanced resistance. Both reverse transcription-coupled quantitative PCR and RNA-Seq data confirmed that expression levels of at least four ZmPAL genes were significantly up-regulated upon SCMV infection. Knockdown of ZmPAL expression led to enhanced SCMV infection symptom severity and virus multiplication, and simultaneously resulted in decreased SA accumulation and PR gene expression. Intriguingly, application of exogenous SA to SCMV-infected ZmPAL-silenced maize plants decreased SCMV accumulation, showing that ZmPALs are required for SA-mediated resistance to SCMV infection. In addition, lignin measurements and metabolomic analysis showed that ZmPALs are also involved in SCMV-induced lignin accumulation and synthesis of other secondary metabolites via the phenylpropanoid pathway. In summary, our results indicate that ZmPALs are required for SA accumulation in maize and are involved in resistance to virus infection by limiting virus accumulation and moderating symptom severity.

Keywords: Sugarcane mosaic virus; ligin; phenylalanine ammonia-lyase; phenylpropanoid biosynthesis; resistance; salicylic acid; virus-induced gene silencing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology
  • Gene Silencing
  • Phenylalanine Ammonia-Lyase / genetics
  • Phenylalanine Ammonia-Lyase / metabolism*
  • Plant Diseases / virology*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Potyvirus / pathogenicity*
  • Salicylic Acid / metabolism*
  • Zea mays / enzymology*
  • Zea mays / virology*

Substances

  • Plant Proteins
  • Phenylalanine Ammonia-Lyase
  • Salicylic Acid

Supplementary concepts

  • Sugarcane mosaic virus