Silencing of miR156 confers enhanced resistance to brown planthopper in rice

Planta. 2018 Oct;248(4):813-826. doi: 10.1007/s00425-018-2942-6. Epub 2018 Jun 22.

Abstract

Silencing of miR156 in rice confers enhanced resistance to brown planthopper through reducing JA and JA-Ile biosynthesis. Rice brown planthopper (BPH, Nilaparvata lugens Stål) threatens the sustainability of rice production and global food security. Due to the rapid adaptation of BPH to current germplasms in rice, development of novel types of resistant germplasms becomes increasingly important. Plant ontogenetic defense against pathogen and herbivores offers a broad spectrum and durable resistance, and has been experimentally tested in many plants; however, the underlying molecular mechanism remains unclear. miR156 is the master regulator of ontogeny in plants; modulation of miR156 is, therefore, expected to cause corresponding changes in BPH resistance. To test this hypothesis, we silenced miR156 using a target mimicry method in rice, and analyzed the resistance of miR156-silenced plants (MIM156) to BPH. MIM156 plants exhibited enhanced resistance to BPH based on analyses of honeydew excretion, nymph survival, fecundity of BPH, and the survival ratio of rice plants after BPH infestation. Molecular analysis indicated that the expression of MPK3, MPK6, and WRKY70, three genes involved in BPH resistance and jasmonic acid (JA) signaling, was altered in MIM156 plants. The JA and bioactive jasmonoyl-isoleucine levels and the expression of genes involved in JA biosynthesis were significantly reduced in MIM156 plants. Restoration of JA level by exogenous application increased the number of BPH feeding on MIM156 plants and reduced its resistance to BPH. Our findings suggest that miR156 negatively regulates BPH resistance by increasing JA level in rice; therefore, modulation of miR156-SPLs' pathway may offer a promising way to breed rice varieties with enhanced resistance against BPH and elite agronomically important traits.

Keywords: Brown planthopper (Nilaparvata lugens Stål); Defense; Herbivory; Jasmonic acid; miR156.

MeSH terms

  • Animals
  • Cyclopentanes / metabolism
  • Cyclopentanes / pharmacology
  • Down-Regulation
  • Female
  • Gene Expression Regulation, Plant
  • Gene Silencing
  • Hemiptera / physiology*
  • Isoleucine / analogs & derivatives
  • Isoleucine / metabolism
  • MicroRNAs / genetics*
  • Oryza / drug effects
  • Oryza / genetics*
  • Oryza / physiology
  • Oxylipins / metabolism
  • Oxylipins / pharmacology
  • Plant Breeding
  • Plants, Genetically Modified

Substances

  • Cyclopentanes
  • MicroRNAs
  • Oxylipins
  • jasmonoyl-isoleucine
  • Isoleucine
  • jasmonic acid