Tomato Sl3-MMP, a member of the Matrix metalloproteinase family, is required for disease resistance against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000

BMC Plant Biol. 2015 Jun 14:15:143. doi: 10.1186/s12870-015-0536-z.

Abstract

Background: Matrix metalloproteinases (MMPs) are a family of zinc-dependent endopeptidases. MMPs have been characterized in detail in mammals and shown to play key roles in many physiological and pathological processes. Although MMPs in some plant species have been identified, the function of MMPs in biotic stress responses remains elusive.

Results: A total of five MMP genes were identified in tomato genome. qRT-PCR analysis revealed that expression of Sl-MMP genes was induced with distinct patterns by infection of Botrytis cinerea and Pseudomonas syringae pv. tomato (Pst) DC3000 and by treatment with defense-related hormones such as salicylic acid, jasmonic acid and ethylene precursor 1-amino cyclopropane-1-carboxylic acid. Virus-induced gene silencing (VIGS)-based knockdown of individual Sl-MMPs and disease assays indicated that silencing of Sl3-MMP resulted in reduced resistance to B. cinerea and Pst DC3000, whereas silencing of other four Sl-MMPs did not affect the disease resistance against these two pathogens. The Sl3-MMP-silenced tomato plants responded with increased accumulation of reactive oxygen species and alerted expression of defense genes after infection of B. cinerea. Transient expression of Sl3-MMP in leaves of Nicotiana benthamiana led to an enhanced resistance to B. cinerea and upregulated expression of defense-related genes. Biochemical assays revealed that the recombinant mature Sl3-MMP protein had proteolytic activities in vitro with distinct preferences for specificity of cleavage sites. The Sl3-MMP protein was targeted onto the plasma membrane of plant cells when transiently expressed in onion epidermal cells.

Conclusion: VIGS-based knockdown of Sl3-MMP expression in tomato and gain-of-function transient expression of Sl3-MMP in N. benthamiana demonstrate that Sl3-MMP functions as a positive regulator of defense response against B. cinerea and Pst DC3000.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Botrytis / drug effects
  • Botrytis / physiology*
  • Cell Death / drug effects
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Disease Resistance / drug effects
  • Disease Resistance / immunology*
  • Gene Expression Regulation, Plant / drug effects
  • Gene Silencing / drug effects
  • Genes, Plant
  • Hydrogen Peroxide / metabolism
  • Matrix Metalloproteinases / chemistry
  • Matrix Metalloproteinases / metabolism*
  • Molecular Sequence Data
  • Multigene Family
  • Nicotiana / drug effects
  • Nicotiana / genetics
  • Onions / cytology
  • Phylogeny
  • Plant Diseases / genetics
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Plant Epidermis / cytology
  • Plant Epidermis / drug effects
  • Plant Epidermis / metabolism
  • Plant Growth Regulators / pharmacology
  • Plant Proteins / chemistry
  • Plant Proteins / metabolism*
  • Plants, Genetically Modified
  • Protein Transport / drug effects
  • Proteolysis / drug effects
  • Pseudomonas syringae / drug effects
  • Pseudomonas syringae / physiology*
  • Sequence Alignment
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Solanum lycopersicum / enzymology*
  • Solanum lycopersicum / genetics
  • Solanum lycopersicum / immunology
  • Solanum lycopersicum / microbiology*
  • Subcellular Fractions / drug effects
  • Subcellular Fractions / metabolism

Substances

  • Plant Growth Regulators
  • Plant Proteins
  • Hydrogen Peroxide
  • Matrix Metalloproteinases

Associated data

  • GENBANK/KR081423
  • GENBANK/KR081424
  • GENBANK/KR081425
  • GENBANK/KR081426
  • GENBANK/KR081427