Insect Transmission of Plant Pathogens: a Systems Biology Perspective

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Abstract

ABSTRACT

Insect-vectored pathogens pose one of the greatest threats to plant and animal, including human, health on a global scale. Few effective control strategies have been developed to thwart the transmission of any insect-transmitted pathogen. Most have negative impacts on the environment and human health and are unsustainable. Plant pathogen transmission by insect vectors involves a combination of coevolving biological players: plant hosts, insect vectors, plant pathogens, and bacterial endosymbionts harbored by the insect. Our ability to help growers to control vector-borne disease depends on our ability to generate pathogen- and/or disease-resistant crops by traditional or synthetic approaches and to block pathogen transmission by the insect vector. Systems biology studies have led to the reexamination of existing paradigms on how pathogens interact with insect vectors, including the bacterial symbionts, and have identified vector-pathogen interactions at the molecular and cellular levels for the development of novel transmission interdiction strategies.

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Plant viruses alter insect behavior to enhance their spread

Laura L. Ingwell, Sanford Eigenbrode, Nilsa A. Bosque-Pérez (2012)

Pathogens and parasites can induce changes in host or vector behavior that enhance their transmission. In plant systems, such effects are largely restricted to vectors, because they are mobile and may exhibit preferences dependent upon plant host infection status. Here we report the first evidence that acquisition of a plant virus directly alters host selection behavior by its insect vector. We show that the aphid Rhopalosiphum padi, after acquiring Barley yellow dwarf virus (BYDV) during in vitro feeding, prefers noninfected wheat plants, while noninfective aphids also fed in vitro prefer BYDV-infected plants. This behavioral change should promote pathogen spread since noninfective vector preference for infected plants will promote acquisition, while infective vector preference for noninfected hosts will promote transmission. We propose the “Vector Manipulation Hypothesis” to explain the evolution of strategies in plant pathogens to enhance their spread to new hosts. Our findings have implications for disease and vector management.

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The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

Wenbo Chen, Daniel K. Hasegawa, Navneet Kaur … (2016)

Background The whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is among the 100 worst invasive species in the world. As one of the most important crop pests and virus vectors, B. tabaci causes substantial crop losses and poses a serious threat to global food security. Results We report the 615-Mb high-quality genome sequence of B. tabaci Middle East-Asia Minor 1 (MEAM1), the first genome sequence in the Aleyrodidae family, which contains 15,664 protein-coding genes. The B. tabaci genome is highly divergent from other sequenced hemipteran genomes, sharing no detectable synteny. A number of known detoxification gene families, including cytochrome P450s and UDP-glucuronosyltransferases, are significantly expanded in B. tabaci. Other expanded gene families, including cathepsins, large clusters of tandemly duplicated B. tabaci-specific genes, and phosphatidylethanolamine-binding proteins (PEBPs), were found to be associated with virus acquisition and transmission and/or insecticide resistance, likely contributing to the global invasiveness and efficient virus transmission capacity of B. tabaci. The presence of 142 horizontally transferred genes from bacteria or fungi in the B. tabaci genome, including genes encoding hopanoid/sterol synthesis and xenobiotic detoxification enzymes that are not present in other insects, offers novel insights into the unique biological adaptations of this insect such as polyphagy and insecticide resistance. Interestingly, two adjacent bacterial pantothenate biosynthesis genes, panB and panC, have been co-transferred into B. tabaci and fused into a single gene that has acquired introns during its evolution. Conclusions The B. tabaci genome contains numerous genetic novelties, including expansions in gene families associated with insecticide resistance, detoxification and virus transmission, as well as numerous horizontally transferred genes from bacteria and fungi. We believe these novelties likely have shaped B. tabaci as a highly invasive polyphagous crop pest and efficient vector of plant viruses. The genome serves as a reference for resolving the B. tabaci cryptic species complex, understanding fundamental biological novelties, and providing valuable genetic information to assist the development of novel strategies for controlling whiteflies and the viruses they transmit. Electronic supplementary material The online version of this article (doi:10.1186/s12915-016-0321-y) contains supplementary material, which is available to authorized users.

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The Wolbachia endosymbiont as an anti-filarial nematode target

Barton E Slatko, Mark Taylor, Jeremy M Foster (2010)

Human disease caused by parasitic filarial nematodes is a major cause of global morbidity. The parasites are transmitted by arthropod intermediate hosts and are responsible for lymphatic filariasis (elephantiasis) or onchocerciasis (river blindness). Within these filarial parasites are intracellular alpha-proteobacteria, Wolbachia, that were first observed almost 30 years ago. The obligate endosymbiont has been recognized as a target for anti-filarial nematode chemotherapy as evidenced by the loss of worm fertility and viability upon antibiotic treatment in an extensive series of human trials. While current treatments with doxycycline and rifampicin are not practical for widespread use due to the length of required treatments and contraindications, anti-Wolbachia targeting nevertheless appears a promising alternative for filariasis control in situations where current programmatic strategies fail or are unable to be delivered and it provides a superior efficacy for individual therapy. The mechanisms that underlie the symbiotic relationship between Wolbachia and its nematode hosts remain elusive. Comparative genomics, bioinfomatic and experimental analyses have identified a number of potential interactions, which may be drug targets. One candidate is de novo heme biosynthesis, due to its absence in the genome sequence of the host nematode, Brugia malayi, but presence in Wolbachia and its potential roles in worm biology. We describe this and several additional candidate targets, as well as our approaches for understanding the nature of the host-symbiont relationship.

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Author and article information

Journal

Journal ID (nlm-ta): mSystems

Journal ID (iso-abbrev): mSystems

Journal ID (hwp): msys

Journal ID (pmc): msys

Journal ID (publisher-id): mSystems

Title: mSystems

Publisher: American Society for Microbiology (1752 N St., N.W., Washington, DC )

ISSN (Electronic): 2379-5077

Publication date (Electronic): 20 March 2018

Publication date Collection: Mar-Apr 2018

Volume: 3

Issue: 2

Electronic Location Identifier: e00168-17

Affiliations

[a ]USDA Agricultural Research Service, Emerging Pests and Pathogens Research Unit, Robert W. Holley Center for Agriculture and Health, Ithaca, New York, USA

[b ]Boyce Thompson Institute, Ithaca, New York, USA

[c ]Plant Pathology and Plant Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, New York, USA

Author notes

Address correspondence to mlc68@ 123456cornell.edu .

Conflict of Interest Disclosures: M.H. has nothing to disclose.

Citation Heck M. 2018. Insect transmission of plant pathogens: a systems biology perspective. mSystems 3:e00168-17. https://doi.org/10.1128/mSystems.00168-17.

Author information

Michelle Heck https://orcid.org/0000-0003-0921-4489

Article

Publisher ID: mSystems00168-17

DOI: 10.1128/mSystems.00168-17

PMC ID: 5881024

PubMed ID: 29629417

SO-VID: fe5d202b-d89a-4464-a7f2-774ab3fdfa21

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This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply.

History

Date received : 2 November 2017

Date accepted : 2 January 2018

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Figures: 0, Tables: 0, Equations: 0, References: 32, Pages: 5, Words: 3628

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cover-date March/April 2018

Keywords: aphids,citrus greening,plant virus,proteomics,psyllids,transcriptomics,vector biology

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Keywords: aphids, citrus greening, plant virus, proteomics, psyllids, transcriptomics, vector biology

Insect Transmission of Plant Pathogens: a Systems Biology Perspective

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Vector Biology

Most cited references 18

Plant viruses alter insect behavior to enhance their spread

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

The Wolbachia endosymbiont as an anti-filarial nematode target

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