Abstract
We have previously shown that the monopartite Tomato yellow leaf curl virus (TYLCV), a begomovirus (family Geminiviridae, genus Begomovirus) infecting tomato plants can be transmitted in a gender-dependent manner among its insect vector the whitefly Bemisia tabaci type B (Gennaduis) (Aleyrodidae: Hemiptera) during mating. Viruliferous females were able to transmit the virus to non-viruliferous males and vice versa, in the absence of any other virus source. The recipient insects were able to infect tomato plants. In this communication, we present evidence that two bipartite begomoviruses infecting cucurbits, Squash leaf curl virus (SLCV) and Watermelon chlorotic stunt virus (WmCSV) can be transmitted in a gender-dependent manner among whiteflies. In addition we show that TYLCV can be transmitted during mating among individuals from the same biotype (from B-males to B-females and vice versa; and from Q-males to Q-females and vice versa). However, viruliferous males of the B biotype are unable to transmit the virus to females of the Q biotype (and vice versa); similarly, viruliferous males of the Q biotype are unable to transmit the virus to females of the B biotype (and vice versa). These findings support the hypothesis that a pre-zygotic mating barrier between the Q and B biotypes is the cause for the absence of gene flow between the two biotypes, and that virus transmission can be used as a marker for inter-biotype mating. To be transmitted during mating, the virus needs to be present in the haemolymph of the donor insect. Abutilon mosaic virus (AbMV), a bipartite begomovirus that can be ingested but not transmitted by B. tabaci, is absent in the whitefly haemolymph, and cannot be transmitted during mating. Mating was a precondition for horizontal virus transfer from male to female, or female to male. Virus was not transmitted when viruliferous B. tabaci were caged with the non-vector non-viruliferous whitefly Trialeurodes vaporariorum (Westwood) (Aleyrodidae: Hemiptera) and vice versa.
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References
Antignus Y, Lachman O, Pearlsman M (2004) Squash leaf curl virus (SLCV) and watermelon chlorotic stunt virus (WmCSV), newly emerging begomoviruses in Israel. Second European Whitefly Symposium, 5–9 October 2004, Cavtat, Croatia. Abstratc 31L, p 29
Antignus Y, Lachman O, Pearlsman M, Omer S, Yunis H, Messika Y, Uko O, Koren A (2003) Squash leaf curl geminivirus–a new illegal immigrant from the Western Hemisphere and a threat to cucurbit crops in Israel. Phytoparasitica 31:415
Bedford ID, Markham PG, Brown JK, Rosell RC (1994) Geminivirus transmission and biological characterization of whitefly (Bemisia tabaci) types from different world regions. Ann Appl Biol 125:311–325
Bosco D, Mason G, Accotto GP (2004) TYLCSV DNA, but not infectivity, can be transovarially inherited by the progeny of the whitefly vector Bemisia tabaci (Gennadius). Virology 323:276–283
Brown J (2000) Molecular markers for the identification and global tracking of whitefly vector: begomovirus complexes. Virus res 71:233–260
Brown JK, Caballero R, Rogan D, Bird J (2001) Evidence for Bemisia tabaci species complex: mitochondria cytochrome oxidase I gene complex sequence analysis confirms one group comprising all B. tabaci, and mating between AZA, AZB and Jatropha biotypes corroborate a single biological species. In: Proceedings, European Whitefly Symposium, 27 February–3 March 2001, Ragusa, Sicily, Italy. European Whitefly Studies Network, Norwich, United Kingdom, p 23
Butlin R (1995) Genetic variation in mating signals and responses. In: Lambert DM, Spencer HG (eds) Speciation and the recognition concept, theory and application. The Johns Hopkins University Press, Baltimore, MD, pp 327–366
Byrne FJ, Cahill M, Denholm I, Devonshire AL (1995) Biochemical identification of interbreeding between B-type and non B-type strains of the tobacco whitefly Bemisia tabaci. Biochem Genet 33:13–23
Chapman RF (1991) The Insects. Structure and function. Edward Arnold, London, 919 pp
Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N, Inbar M, Ghanim M (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull Entomol Res 97:407–413
Cohen S (1990) Epidemiology of whitefly-transmitted viruses. In: Gerling D (ed) Whiteflies: their bionomics, pest status and management. Intercept Ltd, Andover, Hans, UK, pp 211–225
Costa HS, Brown JK, Sivasupramaniam S, Bird J (1993) Regional distribution, insecticide resistance, and reciprocal crosses between the ‘A’ and ‘B’ biotypes of Bemisia tabaci. Insect Sci Applic 14:127–138
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. Ann Appl Biol 140:215–231
DeBarro PJ, Hart PJ (2000) Mating interactions between two biotypes of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae) in Australia. Bull Entomol Res 90:103–112
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
Ghanim M, Czosnek H (2000) Tomato yellow leaf curl geminivirus (TYLCV-Is) is transmitted among whiteflies (Bemisia tabaci) in a sex-related manner. J Virol 74:4738–4745
Ghanim M, Morin S, Czosnek H (2001a) 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
Ghanim M, Rosell RC, Campbell LR, Czosnek H, Brown JK, Ullman DE (2001b) Digestive, Salivary and Reproductive Organs of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Biotype B. J Morphol 248:22–40
Gunning RV, Byrne FJ, Devonshire AL (1997) Electrophoretic analysis of non-B and B-biotype Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in Australia. Aust J Entomol 36:245–249
Hohnle M, Hofer P, Bedford ID, Briddon RW, Markham PG, 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
Horowitz AR, Denholm I, Gorman K, Cenis JL, Kontsedalov S, Ishaaya I (2003) Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 31:94–98
Horowitz AR, Kontsedalov S, Khasdan V, Ishaaya I (2005) Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Arch Insect Biochem Physiol 58:216–225
Maruthi MN, Colvin J, Thwaites RM, Banks GK, Gibson G, Seal SE (2004) Reproductive incompatibility and cytochrome oxidase I gene sequence variability amongst host-adapted and geographically separate Bemisia tabaci populations (Hemiptera: Aleyrodidae). Syst Entomol 29:560–568
Morin S, Elbaz M (2006) Mating behavior and its effect on reproductive potential of the B and Q biotypes of Bemisia tabaci. The Fourth International Bemisia Workshop, Duck Key, FL, USA, p 49, Abstract
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
Navot N, Pichersky E, Zeidan M, Zamir D, Czosnek H (1991) Tomato yellow leaf curl virus: a whitefly-transmitted geminivirus with a single genomic component. Virology 185:151–161
Perring TM, Cooper AD, Rodriguez RJ, Farrar CA, Bellows TS (1993) Identification of a whitefly species by genomic and behavioral studies. Science 259:74–77
Perring TM (2001) The Bemisia tabaci species complex. Crop Prot 20:725–737
Perring TM Symmes EJ (2006) Courtship behavior of Bemisia argentifolii (Hemiptera: Aleyrodidae) and whitefly mate recognition. Ann Entomol Soc Am 99:598–606
Polston JE, Al-Musa A, Perring TM, Dodds JA (1990) Association of the nucleic acid of Squash leaf curl geminivirus with the whitefly Bemisia tabaci. Phytopathology 80:850–856
Ronda M, Adán A, Beitia DF, Cifuentes D, Cenis JL (2000). Interbreeding between biotypes of Bemisia tabaci. European Whitefly Studies Network Newsletter, #3 (http://www.whitefly.org/EWSN-NewDownLds-pdf/EWSN_Newsletter03.pdf)
Rosell RC, Torres-Jerez I, Brown JK (1999) Tracing the geminivirus-whitefly transmission pathway by polymerase chain reaction in whitefly extracts, hemolymph, and honeydew. Phytopathology 89:239–246
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. J Gen Vir 78:2683–2689
Sanchez-Campos S, Navas-Castillo J, Camero R, Soria C, Diaz JA, Moriones E (1999). Displacement of Tomato Yellow Leaf Curl Virus (TYLCV)-Sr by TYLCV-Is in tomato epidemics in Spain. Phytopathology 89:1038–1043
Sinisterra XH, McKenzie CL, Hunter WB, Powell CA, Shatters RG Jr (2005) Differential transcriptional activity of plant pathogenic begomoviruses in their whitefly vector (Bemisia tabaci, Gennadius: Hemiptera Aleyrodidae) J Gen Virol 86:1525–1532
Zeidan M, Czosnek H (1991) Acquisition of Tomato yellow leaf curl virus by the whitefly Bemisia tabaci. J Gen Virol 72:2607–2614
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Ghanim, M., Sobol, I., Ghanim, M. et al. Horizontal transmission of begomoviruses between Bemisia tabaci biotypes. Arthropod-Plant Interactions 1, 195–204 (2007). https://doi.org/10.1007/s11829-007-9018-z
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DOI: https://doi.org/10.1007/s11829-007-9018-z