A frameshift mutation in JAZ10 resolves the growth versus defense dilemma in rice

Proc Natl Acad Sci U S A. 2024 Dec 24;121(52):e2413564121. doi: 10.1073/pnas.2413564121. Epub 2024 Dec 18.

Abstract

CRISPR-Cas9 genome editing systems have revolutionized plant gene functional studies by enabling the targeted introduction of insertion-deletions (INDELs) via the nonhomologous end-joining (NHEJ) pathway. Frameshift-inducing INDELs can introduce a premature termination codon and, in other instances, can lead to the appearance of new proteins. Here, we found that mutations in the rice jasmonate (JA) signaling gene OsJAZ10 by CRISPR-Cas9-based genome editing did not affect canonical JA signaling. However, a type of mutant with an INDEL that yielded a novel frameshift protein named FJ10 (Frameshift mutation of JAZ10), exhibited enhanced rice growth and increased resistance to brown planthopper attacks. Overexpression of FJ10 in wild-type plants phenocopies OsJAZ10 frameshift mutants. Further characterization revealed that FJ10 interacts with Slender Rice 1 (OsSLR1) and F-box/Kelch 16 (OsFBK16). These interactions disrupt the function of OsSLR1 in suppressing gibberellin-mediated growth and the function of OsFBK16 in repressing lignin-mediated defense responses, respectively. Field experiments with FJ10-expressing plants demonstrate that this protein uncouples the growth-defense tradeoff, opening broad avenues to obtain cultivars with enhanced yield without compromised defenses.

Keywords: brown planthopper; frameshift mutation; growth–defense tradeoff; jasmonate; rice.

MeSH terms

  • Animals
  • CRISPR-Cas Systems
  • Cyclopentanes* / metabolism
  • Disease Resistance / genetics
  • Frameshift Mutation*
  • Gene Editing
  • Gene Expression Regulation, Plant
  • Gibberellins / metabolism
  • Hemiptera / genetics
  • Hemiptera / growth & development
  • Hemiptera / metabolism
  • Oryza* / genetics
  • Oryza* / growth & development
  • Oryza* / metabolism
  • Oryza* / parasitology
  • Oxylipins* / metabolism
  • Plant Diseases / genetics
  • Plant Diseases / parasitology
  • Plant Proteins* / genetics
  • Plant Proteins* / metabolism
  • Plants, Genetically Modified / genetics
  • Signal Transduction

Substances

  • Cyclopentanes
  • Plant Proteins
  • jasmonic acid
  • Oxylipins
  • Gibberellins