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| Back to Basics: Are Begomoviruses Whitefly Pathogens? |
| Henryk Czosnek , Murad Ghanim |
1.Institute of Plant Science and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, Israel
2.Department of Entomology, Agricultural Research Organization, Volcani Center, Bet Dagan 50250, Israel |
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摘要 Begomoviruses and whiteflies have interacted for geological times. An assumed long-lasting virus-vector intimate relationship of this magnitude implies that the partners have developed co-evolutionary mechanisms that insure on one hand the survival and the efficient transmission of the virus, and on the other hand the safeguard of the insect host from possible deleterious effects of the virus. Several studies have indicated that viruses belonging to the Tomato yellow leaf curl virus (TYLCVs) family from China, Israel and Italy are reminiscent of insect pathogens. TYLCVs like all begomoviruses are transmitted in a circulative manner by the whitefly Bemisia tabaci. The survival of the virus in the haemolymph of B. tabaci is ensured by a GroEL homologue produced by a whitefly secondary endosymbiont. Following acquisition and transfer to non-host plants, the virus may remain associated with the insect for its entire 4-5 wk-long adult life. During this period, the ability of the insects to inoculate plants steadily decreased, but did not disappear. The long-term presence of TYLCVs in B. tabaci was associated with a decrease in the insect longevity and fertility. Viral DNA was transmitted to progeny, but seldom infectivity. TYLCV transcripts were found associated with the insects, raising the possibility of replication and expression in the vector. TYLCVs may spread amidst whiteflies during copulation. Functional genomics tools such as microarrays, deep sequencing, quantitative PCR and gene silencing allow revisiting the proposition that TYLCVs have retained, or acquired, some characteristics of an insect pathogen.
Abstract Begomoviruses and whiteflies have interacted for geological times. An assumed long-lasting virus-vector intimate relationship of this magnitude implies that the partners have developed co-evolutionary mechanisms that insure on one hand the survival and the efficient transmission of the virus, and on the other hand the safeguard of the insect host from possible deleterious effects of the virus. Several studies have indicated that viruses belonging to the Tomato yellow leaf curl virus (TYLCVs) family from China, Israel and Italy are reminiscent of insect pathogens. TYLCVs like all begomoviruses are transmitted in a circulative manner by the whitefly Bemisia tabaci. The survival of the virus in the haemolymph of B. tabaci is ensured by a GroEL homologue produced by a whitefly secondary endosymbiont. Following acquisition and transfer to non-host plants, the virus may remain associated with the insect for its entire 4-5 wk-long adult life. During this period, the ability of the insects to inoculate plants steadily decreased, but did not disappear. The long-term presence of TYLCVs in B. tabaci was associated with a decrease in the insect longevity and fertility. Viral DNA was transmitted to progeny, but seldom infectivity. TYLCV transcripts were found associated with the insects, raising the possibility of replication and expression in the vector. TYLCVs may spread amidst whiteflies during copulation. Functional genomics tools such as microarrays, deep sequencing, quantitative PCR and gene silencing allow revisiting the proposition that TYLCVs have retained, or acquired, some characteristics of an insect pathogen.
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Received: 01 March 2011
Accepted:
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| Fund: Supported by grant IS-4062-07 from the United States-Israel Binational Agricultural Research and Development Fund (BARD) to Czosnek H and Ghanim M, by research grant 887/07 from the Israel Science Foundation (ISF) to C. H. and G. M., and by research grant 42-204.2/2006 from the German-Israel Foundation (GIF) to C. H. and G. M. |
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Corresponding Authors:
Correspondence Henryk Czosnek, E-mail: czosnek@agri.huji.ac.il
E-mail: czosnek@agri.huji.ac.il
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Cite this article:
Henryk Czosnek , Murad Ghanim.
2012.
Back to Basics: Are Begomoviruses Whitefly Pathogens?. Journal of Integrative Agriculture, 11(2): 225-234.
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| [1]de Assis Filho F M, Naidu R A, Deom C M, Sherwood J L. 2002. Dynamics of Tomato spotted wilt virus replication in the alimentary canal of two thrips species. Phytopathology, 92, 729-733. [2]Ammar E D, Khlifa E A, Mahmoud A, Abol-Ela S E, Peterschmitt M. 2007. Evidence for multiplication of the leafhopper-borne maize yellow stripe virus in its vector using ELISA and dot-blot hybridization. Archives of Virology, 152, 489-494. [3]Bauman P, Munson M A, Lai C Y, Clark M A, Baumann L, Moran N A, Campbell B C. 1993. Origin and properties of bacterial endosymbionts of aphids, whiteflies, and mealybugs. ASM News, 5, 21-24. [4]Bejarano E R, Khashoggi A, Witty M, Lichtenstein C P. 1996. Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution. Proceedings of the National Academy of Sciences of the USA, 93, 759-764. [5]Bellés X. 2010. Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annual Review of Entomology, 55, 111-128. [6]Black L M. 1950. A plant virus that multiplies in its insect vector. Nature, 166, 852-853. [7]Bosco D, Mason G, Accotto G P. 2004. TYLCSV DNA, but not infectivity, can be transovarially inherited by the progeny of the whitefly vector Bemisia tabaci (Gennadius). Virology, 323, 276-283. [8]Bouvaine S, Boonham N, Douglas A E. 2011. Interactions between a luteovirus and the GroEL chaperonin protein of the symbiotic bacterium Buchnera aphidicola of aphids. Journal of General Virology, 92, 1467-1674. [9]Brown J K, Czosnek H. 2002. Whitefly transmission of plant viruses. In: Plumb R T, ed., Advances in Botanical Research. Plant Virus Vector Interactions. Academic Press, New York, USA. vol. 36. pp. 65-100. [10]Caciagli P, Bosco D. 1997. Quantitation over time of tomato yellow leaf curl geminivirus DNA in its whitefly vector. Phytopathology, 87, 610-613. [11]Caciagli P, Bosco D, Al-Bitar L. 1995. Relationships of the Sardinian isolate of tomato yellow leaf curl geminivirus with its whitefly vector Bemisia tabaci Gen. European Journal of Plant Pathology, 101, 163-170. [12]Caciagli P, Medina Piles V, Marian D, Vecchiati M, Masenga V, Mason G, Falcioni T, Noris E. 2009. Virion stability is important for the circulative transmission of Tomato yellow leaf curl sardinia virus by Bemisia tabaci, but virion access to salivary glands does not guarantee transmissibility. Journal of Virology, 83, 5784-5795. [13]Cilia M, Howe K, Fish T, Smith D, Mahoney J, Tamborindeguy C, Burd J, Thannhauser T W, Gray S. 2011a. Biomarker discovery from the top down: Protein biomarkers for efficient virus transmission by insects (Homoptera: Aphididae) discovered by coupling genetics and 2-D DIGE. Proteomics, 11, 2440-2458. [14]Cilia M, Tamborindeguy C, Fish T, Howe K, Thannhauser T W, Gray S. 2011b. Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission. Journal of Virology, 85, 2148- 2166. [15]Czosnek H, Brown J. 2010. The whitefly genome - white paper. Proposal to sequence multiple genomes of Bemisia tabaci (Gennadius). In: Stansly P A, Natanjo S E, eds., Bemisia: Bionomics and Management of a Global Pest. Springer, Dordrecht, The Netherlands. pp. 503-532. [16]Czosnek H, Ghanim M, Ghanim M. 2002. Circulative pathway of begomoviruses in the whitefly vector Bemisia tabaci - insights from studies with Tomato yellow leaf curl virus. Annals of Applied Biology, 140, 215-231. [17]Czosnek H, Ghanim M, Rubinstein G, Morin S, Fridman V, Zeidan M. 2001. Whiteflies: Vectors, and victims (?), of geminiviruses. In: Maramorosch K, ed., Advances in Virus Research. Academic Press, New York, USA. vol. 57. pp. 291-322. [18]Dasgupta R, Garcia B H II, Goodman R M. 2000. Systemic spread of an RNA insect virus in plants expressing plant viral movement protein genes. Proceedings of the National Academy of Sciences of the USA, 98, 4910- 4915. [19]Ghanim M, Kontsedalov S. 2007. Gene expression in pyriproxyfen-resistant Bemisia tabaci Q biotype. Pest Management Science, 63, 776-783. [20]Ghanim M, Medina V. 2007. Localization of Tomato yellow leaf curl virus in its whitefly vector Bemisia tabaci. In: Czosnek H, ed., Tomato Yellow Leaf Curl Virus Disease: Management, Molecular Biology, Breeding for Resistance. Springer, The Netherlands. pp. 171-183. [21]Ghanim M, Brumin M, Popovski S. 2009. A simple, rapid and inexpensive method for localization of Tomato yellow leaf curl virus and Potato leafroll virus in plant and insect vectors. Journal of Virological Methods, 159, 311-314. [22]Ghanim M, Kontsedalov S, Czosnek H. 2007. Tissue-specific gene silencing by RNA interference in the whitefly Bemisia tabaci (Gennadius). Insect Biochemistry and Molecular Biology, 37, 732-738. [23]Ghanim M, Morin S, Zeidan M, Czosnek H. 1998. Evidence for transovarial transmission of tomato yellow leaf curl virus by its vector the whitefly Bemisia tabaci. Virology, 240, 295-303. [24]Ghanim M, Morin S, Czosnek H. 2001. Rate of Tomato yellow leaf curl virus (TYLCV) translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology, 91, 188-196. [25]Ghanim M, Sobol I, Ghanim M, Czosnek H. 2007. Horizontal transmission of begomoviruses between Bemisia tabaci biotypes. Arthropod-Plant Interactions, 1, 195- 204. [26]Gibbs M J, Cooper J I. 1995. A recombinational event in the history of luteoviruses probably induced by basepairing between the genomes of two distinct viruses. Virology, 206, 1129-1132. [27]Gibbs M J, Weiller G F. 1999. Evidence that a plant virus switched hosts to infect a vertebrate and then recombined with a vertebrate-infecting virus. Proceedings of the National Academy of Sciences of the USA, 96, 8022-8027. [28]Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M, Brumin N, Sobol I, Czosnek H, Vavre F, Fleury F, Ghanim M. 2010. The transmission efficiency of Tomato yellow leaf curl virus is correlated with the presence of a specific symbiotic bacterium species. Journal of Virology, 84, 9310-9317. [29]van den Heuvel J F J M, Verbeek M, van der Wilk F. 1994. Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. Journal of General Virology, 75, 2559-2565. [30]Höfer P, Bedford I D, Markham P G, Jeske H, Frischmuth T. 1997. Coat protein gene replacement results in whitefly transmission of an insect nontransmissible geminivirus isolate. Virology, 236, 288-295. [31]Höhnle M, Höfer P, Bedford I D, Briddon R W, Markham P G, Frischmuth T. 2001. Exchange of three amino acids in the coat protein results in efficient whitefly transmission of a nontransmissible Abutilon mosaic virus isolate. Virology, 290, 164-171. [32]Hu J, De Barro P, Zhao H, Wang J, Nardi F, Liu S H. 2011. An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE, 6, e16061. Hunter W B, Hiebert E, Webb S E, Tsai J H, Polston J E. 1998. Location of geminiviruses in the whitefly Bemisia tabaci (Homoptera: Aleyrodidae). Plant Disease, 82, 1147-1151. [33]Jiu M, Zhou X P, Tong L, Xu J, Yang X, Wan F H, Liu S S. 2007. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE, 2, e182. Katagiri F, Tsuda K. 2010. Understanding the plant immune system. Molecular Plant Microbe Interactions, 23, 1531-1536. [34]Kheyr-Pour A, Bananej K, Dafalla G A, Caciagli P, Noris E, Ahoonmanesh A, Lecoq H, Gronenborn B. 2000. Watermelon chlorotic stunt virus from the Sudan and Iran: Sequence comparisons and identification of a whitefly-transmission determinant. Phytopathology, 90, 629-635. [35]Kunik T, Palanichelvam K, Czosnek H, Citovsky V, Gafni Y. 1998. Nuclear import of a geminivirus capsid protein in plant and insect cells: Implications for the viral nuclear entry. The Plant Journal, 13, 121-129. [36]Lapidot M, Friedmann M, Pilowsky M, Ben-Joseph R, Cohen S. 2001. Effect of host plant resistance to Tomato yellow leaf curl virus (TYLCV) on virus acquisition a n d t r a n s m i s s i o n b y i t s w h i t e f l y v e c t o r . Phytopathology, 91, 1209-1213. [37]Lefeuvre P, Martin D P, Harkins G, Lemey P, Gray A J A, Meredith S, Lakay F, Monjane A, Lett J M, Varsani A, Heydarnejad J. 2010. The spread of Tomato yellow leaf curl virus from the Middle East to the world. PLoS Pathogens, 6, e1001164. [38]Leshkowitz D, Gazit S, Reuveni E, Ghanim M, Czosnek H, McKenzie C, Shatters Jr R G, Brown J K. 2006. Whitefly (Bemisia tabaci) genome project: analysis of sequenced clones from egg, instar, and adult (viruliferous and nonviruliferous) cDNA libraries. BMC Genomics, 7, 79. [39]Liu J, Zhao H, Jiang K, Zhou X P and Liu S S. 2009. Differential indirect effects of two plant viruses on an invasive and an indigenous whitefly vector: implications for competitive displacement. Annals of Applied Biology, 155, 439-448. [40]Luan J B, Li J M, Varela N, Wang Y L, Li F F, Bao Y Y, Zhang C X, Liu S S, Wang X W. 2011. Global analysis of the transcriptional response of whitefly to tomato yellow leaf curl China virus reveals the relationship of coevolved adaptations. Journal of Virology, 85, 3330- 3340. [41]Mahadav A, Gerling D, Gottlieb Y, Czosnek H, Ghanim M. 2008. Parasitization by the wasp Eretmocerus mundus induces transcription of genes related to immune response and symbiotic bacteria proliferation in the whitefly Bemisia tabaci. BMC Genomics, 9, 342. Mahadav A, Kontsedalov S, Czosnek H, Ghanim M. 2009. Thermotolerance and gene expression following heat stress in the whitefly Bemisia tabaci B and Q biotypes. Insect Biochemistry and Molecular Biology, 39, 668- 676. [42]Matsuura S, Hoshino S. 2009. Effect of tomato yellow leaf curl disease on reproduction of Bemisia tabaci Q biotype (Hemiptera: Aleyrodidae) on tomato plants. Applied Entomology and Zoology, 44, 143-148. [43]McGrath P F, Harrison B D. 1995. Transmission of tomato leaf curl geminiviruses by Bemisia tabaci: effects of virus isolate and vector biotype. Annals of Applied Biology, 126, 307-316. [44]McKenzie C L. 2002. Effect of tomato mottle virus (ToMoV) on Bemisia tabaci biotype B (Homoptera: Aleyrodidae) oviposition and adult survivorship on healthy tomato. Florida Entomologist, 85, 367-368. [45]Medina V, Pinner M S, Bedford I D, Achon M A, Gemeno C, Markham P G. 2006. Immunolocalization of Tomato yellow leaf curl Sardinia virus in natural host plants and its vector Bemisia tabaci. Journal of Plant Pathology, 88, 299-308. [46]Mehta P, Wyman J A, Nakhla M K, Maxwell D P. 1994. Transmission of tomato yellow leaf curl geminivirus by Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology, 87, 1291-1297. [47]Miller L K, Ball L A. 1998. The Insect Viruses. Plenum Press, New York, USA. Morin S, Ghanim M, Zeidan M, Czosnek H, Verbeek M, van den Heuvel J F J M. 1999. A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of Tomato yellow leaf curl virus. Virology, 30, 75-84. [48]Morin S, Ghanim M, Sobol I, Czosnek H. 2000. The GroEL protein of the whitefly Bemisia tabaci interacts with the coat protein of transmissible and non-transmissible begomoviruses in the yeast two-hybrid system. Virology, 276, 404-416. [49]Noris E, Vaira A M, Caciagli P, Masenga V, Gronenborn B, Accotto G P. 1998. Amino acids in the capsid protein of tomato yellow leaf curl virus that are crucial for systemic infection, particle formation, and insect transmission. Journal of Virology, 72, 10050-10057. [50]Ohnesorge S, Bejarano E R. 2009. Begomovirus coat protein interacts with a small heatshock protein of its transmission vector (Bemisia tabaci). Insect Molecular Biology, 18, 693-703. [51]Oliver K M, Degnan P H, Burke G R, Moran N A. 2010. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology, 55, 247-266. [52]Padidam M, Sawyer S, Fauquet C M. 1999. Possible emergence of new geminiviruses by frequent recombination. Virology, 265, 218-225. [53]Pascual S, Callejas C. 2004. Intra- and interspecific competition between biotypes B and Q of Bemisia tabaci (Hemiptera: Aleyrodidae) from Spain. Bulletin of Entomological Research, 94, 369-375. [54]Polston J E, Al-Musa A, Perring T M, Dodds J A. 1990. Association of the nucleic acid of squash leaf curl geminivirus with the whitefly Bemisia tabaci. Phytopathology, 80, 850-856. [55]Rosell R C, Torres-Jerez I, Brown J K. 1999. Tracing the geminivirus-whitefly transmission pathway by polymerase chain reaction in whitefly extracts, saliva, hemolymph, and honeydew. Phytopathology, 89, 239- 246. [56]Roth B M, Pruss G J, Vance V B. 2004. Plant viral suppressors of RNA silencing. Virus Research, 102, 97-108. [57]Rubinstein G, Czosnek H. 1997. Long-term association of tomato yellow leaf curl virus (TYLCV) with its whitefly vector Bemisia tabaci: effect on the insect transmission capacity, longevity and fecundity. Journal of General Virology, 78, 2683-2689. [58]Schlee D. 1970. Verwandtschaftsforschung an fossilen und rezenten Aleyrodina (Insectas, Hemiptera). Stuttgarter Beiträge zur Naturkunde, 213, 1-74. [59]Sinisterra X H, McKenzie C L, Hunter W B, Powell C A, Shatters Jr. R G. 2005. Differential transcriptional activity of plant-pathogenic begomoviruses in their whitefly vector (Bemisia tabaci, Gennadius: Hemiptera Aleyrodidae). Journal of General Virology, 86, 1525- 1532. [60]Sylvester E S. 1969. Evidence of transovarial passage of the sowthistle yellow vein virus in the aphid Hyperomyzus lactucae. Virology, 38, 440-446. [61]Sylvester E S. 1973. Reduction of excretion, reproduction, and survival in Hyperomyzus lactucae fed on plants infected with isolates of sowthistle yellow vein virus. Virology, 56, 632-635. [62]Wang J, Zhao H, Jian L, Jiu M, Qian Y J, Liu S S. 2010. Low frequency of horizontal and vertical transmission of two begomoviruses through whitefly Bemisia tabaci biotype B and Q. Annals of Applied Biology, 157, 125- 133. [63]Wang X W, Luan J B, Li J M, Bao Y Y, Zhang C X, Liu S S. 2010. De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics, 11, 400. |
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