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      Bensulfuron-Methyl Treatment of Soil Affects the Infestation of Whitefly, Aphid, and Tobacco Mosaic Virus on Nicotiana tabacum

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          Abstract

          Bensulfuron-methyl (BSM) is widely used in paddy soil for weed control. BSM residue in the soil has been known to inhibit the growth of sensitive crop plants. However, it is unknown whether BSM residue can affect the agrosystem in general. In this study, we have found significant effects of BSM on the infestation of Bemisia tabaci, Myzus persicae, and Tobacco mosaic virus (TMV) in Nicotiana tabacum. The soil was treated with BSM before the pest inoculation. The herbicide-treated tobaccos showed resistance to B. tabaci, but this resistance could not be detected until 15-day post-infestation when smaller number of adults B. tabaci appeared. In M. persicae assay, the longevity of all development stages of insects, and the fecundity of insects were not significantly affected when feeding on BSM-treated plants. In TMV assay, the BSM treatment also reduced virus-induced lesions in early infection time. However, the titer of TMV in BSM treated plants increased greatly over time and was over 40-fold higher than the mock-infected control plants after 20 days. Further studies showed that BSM treatment increased both jasmonic acid (JA) and salicylic acid (SA) levels in tobacco, as well as the expression of target genes in the JA and SA signaling pathways, such as NtWIPK, NtPR1a, and NtPAL. NtPR1a and NtPAL were initially suppressed after virus-inoculation, while NtRDR1 and NtRDR6, which play a key role in fighting virus infection, only showed up- or were down-regulated 20 days post virus-inoculation. Taken together, our results suggested that BSM residue in the soil may affect the metabolism of important phytohormones such as JA and SA in sensitive plants and consequently affect the plant immune response against infections such as whitefly, aphids, and viruses.

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          Most cited references43

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          The salicylic acid loop in plant defense.

          Jyoti Shah (2003)
          Salicylic acid is an important signal molecule in plant defense. In the past two years, significant progress has been made in understanding the mechanism of salicylic-acid biosynthesis and signaling in plants. A pathway similar to that found in some bacteria synthesizes salicylic acid from chorismate via isochorismate. Salicylic-acid signaling is mediated by at least two mechanisms, one requiring the NON-EXPRESSOR OF PR1 (NPR1) gene and a second that is independent of NPR1. Feedback loops involving salicylic acid modulate upstream signals. These feedback loops may provide a point for integrating developmental, environmental and other defense-associated signals, and thus fine-tune the defense responses of plants.
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            The jasmonate signal pathway.

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              Salicylic acid and jasmonic acid are essential for systemic resistance against tobacco mosaic virus in Nicotiana benthamiana.

              Systemic resistance is induced by pathogens and confers protection against a broad range of pathogens. Recent studies have indicated that salicylic acid (SA) derivative methyl salicylate (MeSA) serves as a long-distance phloem-mobile systemic resistance signal in tobacco, Arabidopsis, and potato. However, other experiments indicate that jasmonic acid (JA) is a critical mobile signal. Here, we present evidence suggesting both MeSA and methyl jasmonate (MeJA) are essential for systemic resistance against Tobacco mosaic virus (TMV), possibly acting as the initiating signals for systemic resistance. Foliar application of JA followed by SA triggered the strongest systemic resistance against TMV. Furthermore, we use a virus-induced gene-silencing-based genetics approach to investigate the function of JA and SA biosynthesis or signaling genes in systemic response against TMV infection. Silencing of SA or JA biosynthetic and signaling genes in Nicotiana benthamiana plants increased susceptibility to TMV. Genetic experiments also proved the irreplaceable roles of MeSA and MeJA in systemic resistance response. Systemic resistance was compromised when SA methyl transferase or JA carboxyl methyltransferase, which are required for MeSA and MeJA formation, respectively, were silenced. Moreover, high-performance liquid chromatography-mass spectrometry analysis indicated that JA and MeJA accumulated in phloem exudates of leaves at early stages and SA and MeSA accumulated at later stages, after TMV infection. Our data also indicated that JA and MeJA could regulate MeSA and SA production. Taken together, our results demonstrate that (Me)JA and (Me)SA are required for systemic resistance response against TMV.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                26 December 2016
                2016
                : 7
                : 1970
                Affiliations
                [1] 1Key Laboratory of Plant Virology of Fujian Province, Institute of Plant Virology, Fujian Agriculture and Forestry University Fuzhou, China
                [2] 2Key laboratory of Biopesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University Fuzhou, China
                Author notes

                Edited by: Gero Benckiser, University of Giessen, Germany

                Reviewed by: Zonghua Wang, Fujian Agriculture and Forestry University, China; Javier Veloso, University of Giessen, Germany

                *Correspondence: Zujian Wu, wuzujian@ 123456126.com Xiujuan Ye, xiujuanye2004@ 123456gmail.com

                This article was submitted to Plant Biotic Interactions, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2016.01970
                5183605
                ab7bb47d-a1a0-476b-bf4d-eb371d446a00
                Copyright © 2016 Li, Islam, Wu and Ye.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 August 2016
                : 12 December 2016
                Page count
                Figures: 5, Tables: 2, Equations: 1, References: 52, Pages: 10, Words: 0
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                herbicide,bemisia tabaci,myzus persicae,tobacco mosaic virus,jasmonic acid,salicylic acid

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