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      Transmission of Xanthomonas albilineans by the spittlebug, Mahanarva fimbriolata (Hemiptera: Cercopidae), in Brazil: first report of an insect vector for the causal agent of sugarcane leaf scald

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          Abstract

          Leaf scald is a destructive sugarcane disease caused by the bacterium Xanthomonas albilineans (Ashby) Dowson. This pathogen presents the gene cluster SPI-1 T3SS, a conserved feature in pathogens vectored by animals. In this study, the competence of Mahanarva fimbriolata (Stål), a spittlebug commonly found in sugarcane fields in Brazil, was evaluated for the transmission of X. albilineans. Artificial probing assays were conducted to investigate the ability of M. fimbriolata adults to acquire X. albilineans from artificial diets containing the pathogen with subsequent inoculation of X. albilineans into pathogen-free diets. Plant probing assays with M. fimbriolata adults were conducted to evaluate the acquisition of X. albilineans from diseased source plants and subsequent inoculation of healthy recipient sugarcane plants. The presence of X. albilineans DNA in saliva/diet mixtures of the artificial probing assays and both insects and plants of the plant probing assays were checked using TaqMan assays. The artificial probing assays showed that M. fimbriolata adults were able to acquire and inoculate X. albilineans in diets. Plant probing assays confirmed the competence of M. fimbriolata to transmit X. albilineans to sugarcane. Over the entire experiment, 42% of the insects had acquired the pathogen and successful inoculation of the pathogen occurred in 18% of the recipient-susceptible sugarcane plants at 72 or 96 h of inoculation access period. Assays evidenced the vector competence of M. fimbriolata for transmission of X. albilineans, opening new pathways for investigating the biology and the economic impacts of the interaction between X. albilineans and M. fimbriolata.

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          Vector-Borne Bacterial Plant Pathogens: Interactions with Hemipteran Insects and Plants

          Hemipteran insects are devastating pests of crops due to their wide host range, rapid reproduction, and ability to transmit numerous plant-infecting pathogens as vectors. While the field of plant–virus–vector interactions has flourished in recent years, plant–bacteria–vector interactions remain poorly understood. Leafhoppers and psyllids are by far the most important vectors of bacterial pathogens, yet there are still significant gaps in our understanding of their feeding behavior, salivary secretions, and plant responses as compared to important viral vectors, such as whiteflies and aphids. Even with an incomplete understanding of plant–bacteria–vector interactions, some common themes have emerged: (1) all known vector-borne bacteria share the ability to propagate in the plant and insect host; (2) particular hemipteran families appear to be incapable of transmitting vector-borne bacteria; (3) all known vector-borne bacteria have highly reduced genomes and coding capacity, resulting in host-dependence; and (4) vector-borne bacteria encode proteins that are essential for colonization of specific hosts, though only a few types of proteins have been investigated. Here, we review the current knowledge on important vector-borne bacterial pathogens, including Xylella fastidiosa, Spiroplasma spp., Liberibacter spp., and ‘Candidatus Phytoplasma spp.’. We then highlight recent approaches used in the study of vector-borne bacteria. Finally, we discuss the application of this knowledge for control and future directions that will need to be addressed in the field of vector–plant–bacteria interactions.
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            Insects as alternative hosts for phytopathogenic bacteria.

            Phytopathogens have evolved specialized pathogenicity determinants that enable them to colonize their specific plant hosts and cause disease, but their intimate associations with plants also predispose them to frequent encounters with herbivorous insects, providing these phytopathogens with ample opportunity to colonize and eventually evolve alternative associations with insects. Decades of research have revealed that these associations have resulted in the formation of bacterial-vector relationships, in which the insect mediates dissemination of the plant pathogen. Emerging research, however, has highlighted the ability of plant pathogenic bacteria to use insects as alternative hosts, exploiting them as they would their primary plant host. The identification of specific bacterial genetic determinants that mediate the interaction between bacterium and insect suggests that these interactions are not incidental, but have likely arisen following the repeated association of microorganisms with particular insects over evolutionary time. This review will address the biology and ecology of phytopathogenic bacteria that interact with insects, including the traditional role of insects as vectors, as well as the newly emerging paradigm of insects serving as alternative primary hosts. Also discussed is one case where an insect serves as both host and vector, which may represent a transitionary stage in the evolution of insect-phytopathogen associations. © 2011 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.
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              Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas

              Xanthomonas is a well-studied genus of bacterial plant pathogens whose members cause a variety of diseases in economically important crops worldwide. Genomic and functional studies of these phytopathogens have provided significant understanding of microbial-host interactions, bacterial virulence and host adaptation mechanisms including microbial ecology and epidemiology. In addition, several strains of Xanthomonas are important as producers of the extracellular polysaccharide, xanthan, used in the food and pharmaceutical industries. This polymer has also been implicated in several phases of the bacterial disease cycle. In this review, we summarise the current knowledge on the infection strategies and regulatory networks controlling virulence and adaptation mechanisms from Xanthomonas species and discuss the novel opportunities that this body of work has provided for disease control and plant health. Here, we discuss the current knowledge surrounding regulatory networks and systems that control virulence and adaption mechanisms in Xanthomonas species. Additionally, we detail how study of these pathogens has provided novel opportunities for disease control and plant health.
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                Author and article information

                Contributors
                Role: Subject Editor
                Journal
                J Insect Sci
                J Insect Sci
                jis
                Journal of Insect Science
                Oxford University Press (US )
                1536-2442
                November 2023
                18 December 2023
                18 December 2023
                : 23
                : 6
                : 28
                Affiliations
                Instituto Agronômico (IAC), Centro de Cana , Ribeirão Preto, SP 14032-800, Brazil
                Instituto Agronômico (IAC), Centro de Cana , Ribeirão Preto, SP 14032-800, Brazil
                Instituto Agronômico (IAC), Centro de Cana , Ribeirão Preto, SP 14032-800, Brazil
                Instituto Agronômico (IAC), Centro de Cana , Ribeirão Preto, SP 14032-800, Brazil
                Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (Unesp) , Jaboticabal, SP 14884-900, Brazil
                Escola Superior de Agricultura ‘Luiz de Queiroz’, Universidade de São Paulo (USP) , Piracicaba, SP 13418-900, Brazil
                Escola Superior de Agricultura ‘Luiz de Queiroz’, Universidade de São Paulo (USP) , Piracicaba, SP 13418-900, Brazil
                Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo (USP) , São Paulo, SP 05508-090, Brazil
                Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (Unesp) , Jaboticabal, SP 14884-900, Brazil
                Instituto Agronômico (IAC), Centro de Cana , Ribeirão Preto, SP 14032-800, Brazil
                Author notes
                Corresponding authors, mail: silvana.creste@ 123456sp.gov.br (S.C.)
                Author information
                https://orcid.org/0000-0001-7290-9801
                https://orcid.org/0000-0002-8979-3320
                https://orcid.org/0009-0008-5248-5755
                https://orcid.org/0009-0005-0301-8673
                https://orcid.org/0000-0002-5650-5695
                https://orcid.org/0000-0002-1238-9354
                https://orcid.org/0000-0002-6506-2734
                https://orcid.org/0000-0002-4249-5561
                https://orcid.org/0000-0002-3315-3332
                Article
                iead116
                10.1093/jisesa/iead116
                10727476
                38109489
                2f541694-35d9-4825-95b7-018fdd34d8f9
                © The Author(s) 2023. Published by Oxford University Press on behalf of Entomological Society of America.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 06 September 2023
                : 21 November 2023
                : 29 November 2023
                Page count
                Pages: 8
                Funding
                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo, DOI 10.13039/501100001807;
                Award ID: 2016/17545-8
                Funded by: Paul and Daisy Soros Fellowships for New Americans, DOI 10.13039/100006063;
                Award ID: 2018/07615-4
                Funded by: TT3 fellowship;
                Award ID: 2018/21693-8
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil;
                Award ID: Finance Code 001
                Categories
                Research
                AcademicSubjects/SCI01382

                Entomology
                pathogen transmission,plant disease,hemipteran,qpcr diagnostics,insect vector
                Entomology
                pathogen transmission, plant disease, hemipteran, qpcr diagnostics, insect vector

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