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

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)-4,4,5,5tetramethylimidazoline-1-oxyl-3-oxide (cPTIO), a NO scavenger, repelled B. tabaci adults and prolonged nymphal development, and, more importantly, (3) silencing of NOassociated 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.

Nitric Oxide, an Essential Intermediate in the Plant–Herbivore Interaction

“…Some publications have described the rapid accumulation and participation of NO as a common feature to insect-infested plants ( Table 1 ). Different arthropods including hemipteran ( Smith and Boyko, 2007 ; Moloi and van der Westhuizen, 2009 ; Liu et al, 2011 ; Mai et al, 2014 ; Wozniak et al, 2017 ; Li et al, 2019 ; Xu et al, 2020 ) and lepidopteran species ( Arimura et al, 2008 ; Bricchi et al, 2010 ) cause a rapid and transient increase of NO levels in insect-damaged tissues. However, its physiological significance remains to be established.…”

“…These results were probably due to the role of NOA1 in plant chloroplast functions and in the allocation of carbon resources within phenylpropanoid pathway ( Wünsche et al, 2011b ). Very recently, Xu et al (2020) have demonstrated that the hemipteran Bemisia tabaci infestation activated NO signaling in tobacco, leading to suppression of JA-dependent defenses and improving nymph performance. Additionally, they have confirmed the NOA1 involvement in the JA-mediated responses to B. tabaci .…”

Oxylipins From Different Pathways Trigger Mitochondrial Stress Signaling Through Respiratory Complex III

“…13-LOX-derived jasmonic acid is by far the most studied oxylipin. As a key hormone controlling both developmental and stress-related processes, its receptor, co-receptors, and downstream-regulated transcription factors and target genes are well defined (Chini et al, 2009 ; Ruan et al, 2019 ). In addition to jasmonates, oxylipins from the 9-LOX and non-enzymatic pathways are also implicated in plant stress responses.…”

Data_Sheet_1.docx

“…These results were probably due to the role of NOA1 in plant chloroplast functions and in the allocation of carbon resources within phenylpropanoid pathway (Wünsche et al, 2011b). Very recently, Xu et al (2020) have demonstrated that the hemipteran Bemisia tabaci infestation activated NO signaling in tobacco, leading to suppression of JA-dependent defenses and improving nymph performance. Additionally, they have confirmed the NOA1 involvement in the JA-mediated responses to B. tabaci.…”

“…Some publications have described the rapid accumulation and participation of NO as a common feature to insect-infested plants ( Table 1). Different arthropods including hemipteran (Smith and Boyko, 2007;Moloi and van der Westhuizen, 2009;Liu et al, 2011;Mai et al, 2014;Wozniak et al, 2017;Li et al, 2019;Xu et al, 2020) and lepidopteran species (Arimura et al, 2008;Bricchi et al, 2010) cause a rapid and transient increase of NO levels in insect-damaged tissues. However, its physiological significance remains to be established.…”