TY - JOUR
T1 - Nitric Oxide Boosts Bemisia tabaci Performance Through the Suppression of Jasmonic Acid Signaling Pathway in Tobacco Plants
AU - Xu, Yanan
AU - Qu, Cheng
AU - Sun, Xia
AU - Jia, Zhifei
AU - Xue, Ming
AU - Zhao, Haipeng
AU - Zhou, Xuguo
N1 - Publisher Copyright:
© Copyright © 2020 Xu, Qu, Sun, Jia, Xue, Zhao and Zhou.
PY - 2020/7/22
Y1 - 2020/7/22
N2 - 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.
AB - 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.
KW - Bemisia tabaci
KW - jasmonic acid
KW - nitric oxide
KW - plant defense
KW - tobacco
UR - http://www.scopus.com/inward/record.url?scp=85089065418&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85089065418&partnerID=8YFLogxK
U2 - 10.3389/fphys.2020.00847
DO - 10.3389/fphys.2020.00847
M3 - Article
AN - SCOPUS:85089065418
SN - 1664-042X
VL - 11
JO - Frontiers in Physiology
JF - Frontiers in Physiology
M1 - 847
ER -