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Key message <p>Our results highlight the key role of NaMYC2a/b in regulating trypsin protease inhibitor activity after insect feeding by controlling the expression of <i>NaPI, NaKTI2</i>, and NaPI-like.</p> Abstract <p>When attacked by insect herbivores, <i>Nicotiana attenuata</i> plants activate jasmonate (JA) signaling, and increase trypsin protease inhibitor (TPI) activities by switching on the transcription of various protease inhibitor (PI) genes, such as <i>NaPI</i> and <i>NaKTI2</i>. However, how PI genes are regulated during insect feeding remains unclear. Here we identified a new PI, NaPI-like, that confers <i>Spodoptera litura</i> resistance. NaPI-like shares low sequence identity to NaPI. However, its expression could be specifically and highly induced by <i>S. litura</i> oral secretion (OS). TPI activity was increased by <i>NaPI-like</i> overexpression, and was reduced by silencing <i>NaPI-like</i>. Accordingly, the generalist <i>S. litura</i> performed better in <i>NaPI-like</i>-silenced plants. Further study revealed that the expression levels of <i>NaPI</i>, <i>NaPI-like</i>, and <i>NaKTI2</i> were all strongly elicited by treatment with methyl JA or wounding plus <i>S. litura</i> oral secretion (W + OS) in wild-type (WT) plants. However, they were induced to a much lesser extent in JA-deficient ir<i>AOC</i> plants with W + OS treatment, suggesting that these three <i>PI</i> genes are regulated by JA signaling. Finally, we demonstrated that co-silencing <i>NaMYC2a</i> and <i>NaMYC2b</i> significantly reduced TPI activity, resulting in decreased insect resistance in <i>N. attenuata</i>. EMSA and Dual-LUC assays revealed that NaMYC2a/b regulates the expression of <i>NaPI</i> and <i>NaKTI</i> directly, and <i>NaPI-like</i> indirectly. Our results highlight the diversity of PI genes elicited by insect, and the key role of NaMYC2a/b in regulating TPI activity after insect feeding by controlling <i>NaPI</i>, <i>NaPI-like</i>, and <i>NaKTI2</i> expression. Thus, our data provide new insights into the regulation of PIs during insect feeding. <i>Key message</i>: Our results highlight the key role of NaMYC2a/b in regulating trypsin protease inhibitor activity after insect feeding by controlling the expression of <i>NaPI</i>, <i>NaKTI2</i>, and <i>NaPI-like</i>.</p>

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MYC2a/b-regulated protease inhibitors in defense against Spodoptera litura in Nicotiana attenuata

  • 期刊论文

  • 发表日期：

    2025年12月5日

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  • Luyan Zhao,
  • Junzhong Liu,
  • Lei Wang,
  • Jinsong Wu

摘要

Key message

Our results highlight the key role of NaMYC2a/b in regulating trypsin protease inhibitor activity after insect feeding by controlling the expression of NaPI, NaKTI2, and NaPI-like.

Abstract

When attacked by insect herbivores, Nicotiana attenuata plants activate jasmonate (JA) signaling, and increase trypsin protease inhibitor (TPI) activities by switching on the transcription of various protease inhibitor (PI) genes, such as NaPI and NaKTI2. However, how PI genes are regulated during insect feeding remains unclear. Here we identified a new PI, NaPI-like, that confers Spodoptera litura resistance. NaPI-like shares low sequence identity to NaPI. However, its expression could be specifically and highly induced by S. litura oral secretion (OS). TPI activity was increased by NaPI-like overexpression, and was reduced by silencing NaPI-like. Accordingly, the generalist S. litura performed better in NaPI-like-silenced plants. Further study revealed that the expression levels of NaPI, NaPI-like, and NaKTI2 were all strongly elicited by treatment with methyl JA or wounding plus S. litura oral secretion (W + OS) in wild-type (WT) plants. However, they were induced to a much lesser extent in JA-deficient irAOC plants with W + OS treatment, suggesting that these three PI genes are regulated by JA signaling. Finally, we demonstrated that co-silencing NaMYC2a and NaMYC2b significantly reduced TPI activity, resulting in decreased insect resistance in N. attenuata. EMSA and Dual-LUC assays revealed that NaMYC2a/b regulates the expression of NaPI and NaKTI directly, and NaPI-like indirectly. Our results highlight the diversity of PI genes elicited by insect, and the key role of NaMYC2a/b in regulating TPI activity after insect feeding by controlling NaPI, NaPI-like, and NaKTI2 expression. Thus, our data provide new insights into the regulation of PIs during insect feeding. Key message: Our results highlight the key role of NaMYC2a/b in regulating trypsin protease inhibitor activity after insect feeding by controlling the expression of NaPI, NaKTI2, and NaPI-like.