Elicitor hydrophobin Hyd1 interacts with Ubiquilin1-like to induce maize systemic resistance

J Integr Plant Biol. 2020 Apr;62(4):509-526. doi: 10.1111/jipb.12796. Epub 2019 May 17.

Abstract

Trichoderma harzianum is a plant-beneficial fungus that secretes small cysteine-rich proteins that induce plant defense responses; however, the molecular mechanism involved in this induction is largely unknown. Here, we report that the class II hydrophobin ThHyd1 acts as an elicitor of induced systemic resistance (ISR) in plants. Immunogold labeling and immunofluorescence revealed ThHyd1 localized on maize (Zea mays) root cell plasma membranes. To identify host plant protein interactors of Hyd1, we screened a maize B73 root cDNA library. ThHyd1 interacted directly with ubiquilin 1-like (UBL). Furthermore, the N-terminal fragment of UBL was primarily responsible for binding with Hyd1 and the eight-cysteine amino acid of Hyd1 participated in the protein-protein interactions. Hyd1 from T. harzianum (Thhyd1) and ubl from maize were co-expressed in Arabidopsis thaliana, they synergistically promoted plant resistance against Botrytis cinerea. RNA-sequencing analysis of global gene expression in maize leaves 24 h after spraying with Curvularia lunata spore suspension showed that Thhyd1-induced systemic resistance was primarily associated with brassinosteroid signaling, likely mediated through BAK1. Jasmonate/ethylene (JA/ET) signaling was also involved to some extent in this response. Our results suggest that the Hyd1-UBL axis might play a key role in inducing systemic resistance as a result of Trichoderma-plant interactions.

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Sequence
  • Cloning, Molecular
  • Curvularia / physiology
  • Disease Resistance / immunology*
  • Fungal Proteins / chemistry
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism*
  • Gene Expression Regulation, Plant
  • Genes, Fungal
  • Hypocreales / genetics
  • Phylogeny
  • Plant Diseases / immunology*
  • Plant Leaves / genetics
  • Plant Proteins / chemistry
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Plant Roots / metabolism
  • Protein Binding
  • Protein Domains
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Saccharomyces cerevisiae / metabolism
  • Zea mays / genetics
  • Zea mays / immunology*
  • Zea mays / microbiology

Substances

  • Fungal Proteins
  • Plant Proteins
  • RNA, Messenger

Supplementary concepts

  • Curvularia lunata
  • Trichoderma harzianum