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<p>Polyphenol oxidase (PPO) is a critical enzyme involved in fruit browning, plant defense, and various physiological processes during plant growth and development. Nonetheless, the extent to which selective inhibition of PPO genes can mitigate fruit browning without adversely affecting stress resilience remains unclear. Herein, fresh in-hull walnut (<i>Juglans regia</i>), a fruit prone to browning, was selected to investigate the distinct roles in stress responses between its two PPO genes, <i>JrPPO1</i> and <i>JrPPO2</i>, through fruit storage assays and heterologous overexpression in <i>Arabidopsis thaliana</i>. <i>JrPPO1</i> expression was suppressed under modified atmosphere packaging (MAP) but induced by H₂O₂ treatment, mirroring PPO activity levels and inversely correlating with browning severity. In contrast, <i>JrPPO2</i> displayed inconsistent expression patterns. Upon anthracnose pathogen inoculation, transient silencing of <i>JrPPO2</i> resulted in significantly larger lesions at 3 dpi than both <i>JrPPO1</i>-silenced and control fruits. Following assessment of homozygous T3-generation transgenic <i>Arabidopsis</i> lines, <i>JrPPO2</i>-overexpressing (OE- <i>JrPPO2</i>) lines exhibited significantly higher germination rates (81.95–95.57%) and longer root elongation compared to WT and <i>JrPPO1</i>-overexpressing lines (OE- <i>JrPPO1</i>) under 250 mM NaCl. Upon <i>Pst</i> DC3000 infection, OE-<i>JrPPO2</i> showed lower O₂·⁻ and MDA accumulation, elevated SOD, POD, and PPO activities, higher Fv/Fm values, and significantly reduced bacterial titers, whereas OE-<i>JrPPO1</i> exhibited compromised photosynthetic capacity and higher pathogen loads. Moreover, <i>JrPPO2</i> overexpression upregulated <i>AtNPR1</i>, <i>PR1</i>, <i>PDF1.2</i>, and <i>LOX3</i>, reinforcing its broader role in defense regulation. These the findings revealed functional specialization between <i>JrPPO1</i> and <i>JrPPO2</i>, with <i>JrPPO1</i> mainly governing fruit browning and <i>JrPPO2</i> integrating abiotic and biotic stress resilience. Targeted manipulation of <i>JrPPO2</i> offers a promising strategy to enhance walnut stress tolerance without compromising fruit quality.</p>

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Distinct Roles of Walnut JrPPO1 and JrPPO2 in Plant Stress Responses Revealed Through Fruit Assays and Heterologous Expression in Arabidopsis thaliana

  • 期刊论文

  • 发表日期：

    2025年12月23日

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  • Yifan Wang,
  • Md Rasel,
  • Yan Tang,
  • Zhipeng Guo,
  • Nan Wang,
  • Niu Ye,
  • Huiling Ma

摘要

Polyphenol oxidase (PPO) is a critical enzyme involved in fruit browning, plant defense, and various physiological processes during plant growth and development. Nonetheless, the extent to which selective inhibition of PPO genes can mitigate fruit browning without adversely affecting stress resilience remains unclear. Herein, fresh in-hull walnut (Juglans regia), a fruit prone to browning, was selected to investigate the distinct roles in stress responses between its two PPO genes, JrPPO1 and JrPPO2, through fruit storage assays and heterologous overexpression in Arabidopsis thaliana. JrPPO1 expression was suppressed under modified atmosphere packaging (MAP) but induced by H₂O₂ treatment, mirroring PPO activity levels and inversely correlating with browning severity. In contrast, JrPPO2 displayed inconsistent expression patterns. Upon anthracnose pathogen inoculation, transient silencing of JrPPO2 resulted in significantly larger lesions at 3 dpi than both JrPPO1-silenced and control fruits. Following assessment of homozygous T3-generation transgenic Arabidopsis lines, JrPPO2-overexpressing (OE- JrPPO2) lines exhibited significantly higher germination rates (81.95–95.57%) and longer root elongation compared to WT and JrPPO1-overexpressing lines (OE- JrPPO1) under 250 mM NaCl. Upon Pst DC3000 infection, OE-JrPPO2 showed lower O₂·⁻ and MDA accumulation, elevated SOD, POD, and PPO activities, higher Fv/Fm values, and significantly reduced bacterial titers, whereas OE-JrPPO1 exhibited compromised photosynthetic capacity and higher pathogen loads. Moreover, JrPPO2 overexpression upregulated AtNPR1, PR1, PDF1.2, and LOX3, reinforcing its broader role in defense regulation. These the findings revealed functional specialization between JrPPO1 and JrPPO2, with JrPPO1 mainly governing fruit browning and JrPPO2 integrating abiotic and biotic stress resilience. Targeted manipulation of JrPPO2 offers a promising strategy to enhance walnut stress tolerance without compromising fruit quality.