Key message <p><i>NLR</i><sub><i>4DS−1</i></sub> confers stripe rust resistance by enhancing multilayer physical and chemical defenses. This finding illuminates strategies for engineering durable resistance in wheat.</p> Abstract <p>Wheat stripe rust (<i>Puccinia striiformis</i> f. sp. <i>tritici</i>, <i>Pst</i>) is a major threat to global wheat production. The <i>Yr28</i> locus for <i>Pst</i> resistance is derived from <i>Aegilops tauschii</i> subsp. <i>strangulata</i>. <i>NLR</i><sub><i>4DS−1</i></sub> has been identified as the stripe rust resistance gene at the <i>Yr28</i> locus, which encodes a coiled-coil nucleotide-binding leucine-rich repeat (NLR) protein, however, its molecular mode of action remains largely unknown. Here, we introduced the full-length genomic <i>NLR</i><sub><i>4DS−1</i></sub> into the <i>Pst</i> susceptible wheat ‘Fielder’ by <i>Agrobacterium</i>-mediated transformation. Transgenic plants were resistant to <i>Pst</i>, with significantly reduced fungal biomass and elevated expression of pathogenesis-related genes. Integrated transcriptomic and metabolomic analysis revealed that <i>NLR</i><sub><i>4DS−1</i></sub> orchestrates a multifaceted defense program involving a burst of reactive oxygen species, chlorophyll reduction, lignin accumulation, and the induction of flavonoid and terpenoid phytoalexins. In vitro, either the flavonoid quercetin or the terpenoid borneol can suppress spore germination and hyphal growth of <i>Pst</i>. Notably, <i>NLR</i><sub><i>4DS−1</i></sub> expression did not compromise seedling growth or agronomic performance at the adult stage. Together, these findings identify <i>NLR</i><sub><i>4DS−1</i></sub> as the stripe rust resistance gene for <i>Yr28</i> locus, demonstrate its role in activating defensive pathways, and highlight its potential for engineering durable <i>Pst</i> resistance through gene stacking.</p>

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NLR4DS−1 enhances wheat resistance to stripe rust by upregulating multiple defense responses

  • Jicheng Qu,
  • Hongyun Kou,
  • Zhenghan Chen,
  • Muhammmad Waqas,
  • Hao Wang,
  • Fengchang Ye,
  • Mingzhu Lyu,
  • Heng Tang,
  • Jiajie Wu,
  • Daolin Fu

摘要

Key message

NLR4DS−1 confers stripe rust resistance by enhancing multilayer physical and chemical defenses. This finding illuminates strategies for engineering durable resistance in wheat.

Abstract

Wheat stripe rust (Puccinia striiformis f. sp. tritici, Pst) is a major threat to global wheat production. The Yr28 locus for Pst resistance is derived from Aegilops tauschii subsp. strangulata. NLR4DS−1 has been identified as the stripe rust resistance gene at the Yr28 locus, which encodes a coiled-coil nucleotide-binding leucine-rich repeat (NLR) protein, however, its molecular mode of action remains largely unknown. Here, we introduced the full-length genomic NLR4DS−1 into the Pst susceptible wheat ‘Fielder’ by Agrobacterium-mediated transformation. Transgenic plants were resistant to Pst, with significantly reduced fungal biomass and elevated expression of pathogenesis-related genes. Integrated transcriptomic and metabolomic analysis revealed that NLR4DS−1 orchestrates a multifaceted defense program involving a burst of reactive oxygen species, chlorophyll reduction, lignin accumulation, and the induction of flavonoid and terpenoid phytoalexins. In vitro, either the flavonoid quercetin or the terpenoid borneol can suppress spore germination and hyphal growth of Pst. Notably, NLR4DS−1 expression did not compromise seedling growth or agronomic performance at the adult stage. Together, these findings identify NLR4DS−1 as the stripe rust resistance gene for Yr28 locus, demonstrate its role in activating defensive pathways, and highlight its potential for engineering durable Pst resistance through gene stacking.