Nitric Oxide Boosts Bemisia tabaci Performance Through the Suppression of Jasmonic Acid Signaling Pathway in Tobacco Plants

Yanan Xu, Cheng Qu, Xia Sun, Zhifei Jia, Ming Xue, Haipeng Zhao, Xuguo Zhou

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

The intimate relationships between plants and insects start with herbivory, which can be traced back to approximately 420 million year ago. Like many other relationships, a plant–insect interaction can be mutualistic, commensalistic, or antagonistic. Within antagonistic relationships, plants deploy inducible defense to insect phytophagy. Insects, however, can evade/suppress effectual plant defenses by manipulating plant defense signaling. Previously, we showed that the sweet potato whitefly, Bemisia tabaci, a global invasive insect pest, can suppress jasmonic acid (JA)-dependent defenses, thereby enhancing their performance on host plants. Given that nitric oxide (NO), a multifunctional signaling molecule, interacts closely with JA signaling pathway, we hypothesized that NO is involved in the suppression of JA defensive responses. Equipped with an integrated approach, we comprehensively examined this overarching hypothesis. We showed that: (1) tobacco plants responded to B. tabaci infestation by accumulating high levels of NO, (2) the exogenous application of sodium nitroprusside, a NO donor, in tobacco plants attracted B. tabaci adults and accelerated nymphal development, whereas plants treated with 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO), a NO scavenger, repelled B. tabaci adults and prolonged nymphal development, and, more importantly, (3) silencing of NO-associated protein 1, a gene associated with NO accumulation, and cPTIO application disrupted the B. tabaci-mediated suppression of JA in plants. Collectively, these results suggest that: (1) NO signaling is activated by B. tabaci infestation, (2) NO is involved in the suppression of JA-dependent plant defense, and, consequently, (3) NO improves B. tabaci performance on host plants. Our study reflects the remarkable arm race that co-evolved for millions of years between plants and insects and offers a potential novel target (nitric oxide) for the long-term sustainable management of this global invasive pest.

Original languageEnglish
Article number847
JournalFrontiers in Physiology
Volume11
DOIs
StatePublished - Jul 22 2020

Bibliographical note

Funding Information:
The authors are grateful to the Department of Plant Pathology, Nanjing Agricultural University, for providing tobacco seeds and gene silencing vectors and all the members of the Plant Disease Prevention Laboratory for technical assistance. The authors also thank the reviewers for their constructive comments and suggestions. Funding. This work was financially supported by the National Natural Science Foundation of China (31701799) and Shandong Modern Agricultural Industry Technology System (SDAIT05-022-08).

Publisher Copyright:
© Copyright © 2020 Xu, Qu, Sun, Jia, Xue, Zhao and Zhou.

Keywords

  • Bemisia tabaci
  • jasmonic acid
  • nitric oxide
  • plant defense
  • tobacco

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

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