Dataset Information

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)-4,4,5,5-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.

SUBMITTER: Xu Y

PROVIDER: S-EPMC7387647 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Nitric Oxide Boosts <i>Bemisia tabaci</i> Performance Through the Suppression of Jasmonic Acid Signaling Pathway in Tobacco Plants.

Xu Yanan Y Qu Cheng C Sun Xia X Jia Zhifei Z Xue Ming M Zhao Haipeng H Zhou Xuguo X

Frontiers in physiology 20200722

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, <i> ...[more]

PMID: 32792979

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Project description:The whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), and the viruses it transmits, are a major constraint to vegetable crops, worldwide. Although the whitefly is usually controlled using chemical pesticides, biological control agents constitute an important component in integrated pest management programs. One of these agents is the wasp Eretmocerus mundus (Mercet) (Hymenoptera: Aphelinidae). E. mundus lays its egg on the leaf underneath the pupa of B. tabaci. First instars of the wasp hatch and penetrate the whitefly larvae. Initiation of parasitization induces the host to form a cellular capsule around the parasitoid. Around this capsule, epidermal cells multiply and thick layers of cuticle are deposited. The physiological and molecular processes underlying B. tabaci-E. mundus interactions have not been investigated so far. We have used a cDNA microarray containing 6,000 expressed sequence tags (ESTs) from the whitefly genome to study the parasitoid-whitefly interaction. We compared RNA samples collected across two time points of the parasitization process: when the parasitoid first instar started the penetration process and once it had fully penetrated the host. The results clearly indicated that genes known to be part of the defense pathways described in other insects are also involved in the response of B. tabaci to parasitization by E. mundus. Some of the responses observed included the repression of a serine protease inhibitor (serpin) and the induction of a melanization cascade. A second set of genes that strongly responded to parasitization included bacterial genes encoded by whitefly symbionts. Quantitative real-time PCR and FISH analyses showed that proliferation of Rickettsia, a facultative secondary symbiont, was strongly induced following the initiation of the parasitization process, a result that supported previous reports suggesting that endosymbionts may be involved in the insect host resistance to various environmental stresses. This is the first study examining the transcriptional response of a hemipteran insect to the attack of a biological control agent (Hymenopterous parasitoid), using a new genomic approach developed for this insect pest. The defense response in B. tabaci seems to resemble that of model organisms such as Drosophila melanogaster. Moreover, endosymbionts of B. tabaci seem to play a role in the response to parasitization, and this is supported by previously published results from aphids. Keywords: time course

Project description:Nitric oxide (NO.) is a well-established signal in mammalian cells regulating e.g. smooth muscle tone, neurotransmission and apoptosis. NO interacts with superoxide (O2-) to derive the highly reactive peroxynitrite (ONOO-) radical leading to the generation of lipid hydroxy-peroxides (ROO.) and cell death. Thus the recent reports implicating of .NO in the Hypersensitive Response (HR) a form of programmed cell death elicited by pathogens in plantsis suggestive of parallel roles in animals and plants. As part of BBSRC funded programmes which are investigating oxidative signaling and cell death in Arabidopsis we have collaborated with the Trace Gas Detection facility at the University of Nijmegen to be the first to measure NO in planta from a developing HR (Mur et al.paper in prep). The challenge remains to understand the spatio-temporal role(s) of .NO during the HR and disease development. In line with other groups e.g. Klessig et al.(2000) PNAS 978849-55 we have observed that .NO mediated event are both SA- dependent and independent. We propose a two-stage programme to investigate NO events which will lead to subsequent BBSRC grant bids. Firstly to exploit the GARNET Affymetrix transcriptomic service to identify genes which are upregulated by .NO (see programme below). These will be compared with similar data generated by other members of the consortium; Dr. Steve Neill for oxidative stress (Desikan et al. (2001). Plant Physiol 127(1): 159-72; Clarke et al.2000 Plant J.; 24:667-77); Dr. Paul Kenton who is mainly interested in signaling by the oxylipid Jasmonic acid (Kentonet al. (1999). MPMI 12(1): 74-78) as well as from other sources. Though these data in themselves will suggest modes of NO action. However as a second approach we will clone the promoter of a strongly NO-responsive gene which will be fused to positive and negative selectable markers as well as reporter genes e.g. LUC. to identify Arabidopsis EMS mutants which are perturbed in NO-mediated events. Programme. Our in planta measurement show that from a baseline production of 1nl.g fwt-1h-1 NO levels rise to 6nl. g fwt-h-1 (_plus/- 1.1 SE) prior to cell death and to 25nl g fwt-h-1 (_plus/- 4.2 SE) at cell death following which the concentration falls. At this juncture we will intend to gas Arabidopsis to ~75ppb (the head-space concentration when NO production was at 6nl. g fwt-h-1). Prior to using the DNA RNA will establish that this does not elicit cell death over the proposed treatment period and that both PR1 (SA-dependent) and PAL1 (SA-independent) genes are induced. We will compare this plant with sealed but non-treated Arabidopsis. Future targets for DNA RNAs analysis induce plant treated with both NO (Sodium Nitro Prusside) and O2- (Xanthine oxidase) generators and depending on their effectiveness (to be assessed by NO measurement) HR lesions treated with Nitric Oxide Synthase inhibitors. Keywords: compound_treatment_design

Dataset Information

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

Publications

Nitric Oxide Boosts <i>Bemisia tabaci</i> Performance Through the Suppression of Jasmonic Acid Signaling Pathway in Tobacco Plants.

Similar Datasets

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