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Journal of Integrative Agriculture  2015, Vol. 14 Issue (9): 1786-1795    DOI: 10.1016/S2095-3119(14)60931-X
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Cryptic species composition and genetic diversity within Bemisia tabaci complex in soybean in India revealed by mtCOI DNA sequence
 Prasanna H C, Kanakala S, Archana K, Jyothsna P, Varma R K, Malathi V G
1、Division of Vegetable Improvement, Indian Institute of Vegetable Research, Varanasi, Uttar Pradesh 221305, India
2、Advanced Centre for Plant Virology, Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi 110012, India
3、Department of Plant Pathology, Jawaharlal Nehru Krishi Vishwavidyalaya, Jabalpur 482004, India
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摘要  Bemisia tabaci is a cryptic species complex, causing significant loss on many agriculturally important crops worldwide. Knowledge on species composition and diversity within B. tabaci complex is critical for evolving sustainable pest management strategies. Here we investigate the whitefly species complex in soybean in major soybean growing states of India. The mitochondrial cytochrome oxidase gene subunit-1 (mtCOI) based phylogenetic relationships established using Bayesian methods indicated the existence of three cryptic species namely Asia I, Asia II 1, and Asia II 7. All the haplotypes detected in the study could be assigned to these three cryptic species following the species demarcation criteria of 3.5% divergence threshold. Of these, Asia II 1 was found to be predominant with wide spread distribution across the surveyed regions from cool temperate zones to hot and humid tropical plains. On the contrary, cryptic species Asia II 7 showed localized distribution. The Asia II 1 exhibited the highest haplotype diversity and Asia I showed high level of nucleotide diversity. There was a significantly high genetic differentiation among these three cryptic species. The MEAM 1, a dreadful invasive species was not detected in the specimens tested in the current study. The diversity and distribution of three cryptic species is discussed in the light of current knowledge on distribution of whitefly species in India and yellow mosaic disease observed during sampling survey.

Abstract  Bemisia tabaci is a cryptic species complex, causing significant loss on many agriculturally important crops worldwide. Knowledge on species composition and diversity within B. tabaci complex is critical for evolving sustainable pest management strategies. Here we investigate the whitefly species complex in soybean in major soybean growing states of India. The mitochondrial cytochrome oxidase gene subunit-1 (mtCOI) based phylogenetic relationships established using Bayesian methods indicated the existence of three cryptic species namely Asia I, Asia II 1, and Asia II 7. All the haplotypes detected in the study could be assigned to these three cryptic species following the species demarcation criteria of 3.5% divergence threshold. Of these, Asia II 1 was found to be predominant with wide spread distribution across the surveyed regions from cool temperate zones to hot and humid tropical plains. On the contrary, cryptic species Asia II 7 showed localized distribution. The Asia II 1 exhibited the highest haplotype diversity and Asia I showed high level of nucleotide diversity. There was a significantly high genetic differentiation among these three cryptic species. The MEAM 1, a dreadful invasive species was not detected in the specimens tested in the current study. The diversity and distribution of three cryptic species is discussed in the light of current knowledge on distribution of whitefly species in India and yellow mosaic disease observed during sampling survey.
Keywords:  whitefly       mitochondrial cytochrome oxidase gene subunit-1       Asia I       Asia II 1       Asia II 7       begomovirus and yellow mosaic disease  
Received: 19 August 2014   Accepted:
Fund: 

We are thankful to Department of Biotechnology, Government of India for liberal funding (Functional Genomics of Yellow Mosaic Viruses of Soybean and Development of Transgenic Resistance in Soybean: BT/PR9631/AGR/02/468/2007).

Corresponding Authors:  Malathi V G, Tel: +91-8110996093, Fax: +91-11-25843123, E-mail: vgmalathi@rediffmail.com     E-mail:  vgmalathi@rediffmail.com
About author:  * These authors contributed equally to this work.

Cite this article: 

Prasanna H C, Kanakala S, Archana K, Jyothsna P, Varma R K, Malathi V G. 2015. Cryptic species composition and genetic diversity within Bemisia tabaci complex in soybean in India revealed by mtCOI DNA sequence. Journal of Integrative Agriculture, 14(9): 1786-1795.

Ahmed M Z, De Barro P J, Greeff J M, Ren S X, Naveed M, QiuB L. 2011. Genetic identity of the Bemisia tabacis peciescomplex and association with high cotton leaf curl disease(CLCuD) incidence in Pakistan. Pest Management Science67, 307-317

Ahmed M Z, Ren S X, Mandour N S, Maruthi, M N, NaveedM, Qiu B L. 2009. Phylogenetic analysis of Bemisiatabaci(Hemiptera: Aleyrodidae) populations from cotton plantsin Pakistan, China, and Egypt. Journal of Pest Science,83, 135-141

Alemandri V, De Barro P, Bejerman N, Argüello Caro EB, Dumón A D, Mattio M F, Rodriguez S M, Truoli G. 2012.Species within the Bemisia tabaci (Hemiptera: Aleyrodidae)complex in soybean and bean crops in Argentina. Journalof Economic Entomology, 105, 48-53

Amari K, Gonzalez-Ibeas D, Gomez P, Sempere R N, Sanchez-Pina M A, Aranda M A, Diaz-Pendon J A, Navas-Castillo J,Moriones E, Blanca J, Hernandez-Gallardo M D, AnastasioG. 2008. Tomato torrado virus is transmitted by Bemisiatabaci and infects pepper and eggplant in addition to tomato.Plant Disease, 92, 1139.

Banks G K, Colvin J, Chowda R V, Maruthi M N, MuniyappaV, Venkatesh H M, Kiran Kumar M, Padma A S, Beitia F J,Seal S E. 2001. First report of the Bemisia tabaci B biotypein India and an associated tomato leaf curl virus diseaseepidemic. Plant Disease, 85, 231.

De Barro P J, Liu S S, Boykin L M, Dinsdale A B. 2011. Bemisiatabaci: A statement of species status. Annual Review ofEntomology, 56, 1-19

Bedford I D, Briddon R W, Brown J K, Rosell R C, MarkhamP G. 1994. Geminivirus transmission and biologicalcharacterization of Bemisia tabaci (Gennadius) biotypesfrom different geographic regions. Annals of AppliedBiology, 125, 311-325

Bing X L, Ruan Y M, Rao Q, Wang X W, Liu S S. 2013. Diversity ofsecondary endosymbionts among different putative speciesof the whitefly Bemisia tabaci. Insect Science, 20, 194-206

Boykin L M. 2014. Bemisia tabaci nomenclature: Lessonslearned. Pest Management Science. doi, 10.1002/ps.3709Boykin L M, Armstrong K F, Kubatko L, De Barro P. 2012.Species delimitation and global biosecurity. EvolutionaryBioinformatics, 8, 1-37

Brown J K. 2000. Molecular markers for the identification andglobal tracking of whitefly vector-Begomovirus complexes.Virus Research, 71, 233-260

Brown J K, Costa H S, Laemmlen F. 1992. First report ofwhitefly-associated squash silverleaf disorder of Cucurbitain Arizona and of white streaking disorder of Brassicaspecies in Arizona and California. Plant Disease, 76, 426.

Chowda-Reddy R V, Kirankumar M, Seal S E , Muniyappa V,Valand G B, Govindappa M R, Colvin J. 2012. Bemisiatabaci phylogenetic groups in India and relative transmissionefficacy of tomato leaf curl Bangalore virus by an indigenousand an exotic population. Journal of Integrative Agriculture,11, 235-248

Crowder D W, Horowitz A R, De Barro P J. 2010. Matingbehaviour, life history and adaptation to insecticidesdetermine species exclusion between whiteflies. Journalof Animal Ecology, 79, 563-570

Dinsdale A, Cook L, Riginos C, Buckley Y M, De Barro P. 2010.Refined global analysis of Bemisia tabaci (Hemiptera:Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrialcytochrome oxidase 1 to identify species level geneticboundaries. Annals of the Entomological Society ofAmerica, 103, 196-208

Elbaz M, Lahav N, Morin S. 2010. Evidence for pre-zygoticreproductive barrier between the B and Q biotypes ofBemisia tabaci (Hemiptera: Aleyrodidae). Bulletin ofEntomological Research, 100, 581-590

Excoffier L, Laval G, Schneider S. 2005. Arlequin (ver. 3.0): Anintegrated software package for population genetics dataanalysis. Evolutionary Bioinformatics Online, 1, 47-50

Frohlich, D R, Torres-Jerez I, Bedford I D, Markham P G, BrownJ K. 1999. A phylogeographical analysis of the Bemisiatabaci species complex based on mitochondrial DNAmarkers. Molecular Ecology, 8, 1683-1691

Gorman K, Slater R, Blande J D, Clarke A, Wren J, McCafferyA, Denholm I. 2010. Cross-resistance relationshipsbetween neonicotinoids and pymetrozine in Bemisia tabaci(Hemiptera: Aleyrodidae). Pest Management Science, 66,1186-1190

Horowitz A R, Kontsedalov S, Khasdan V, Kontsedalov S,Ishaaya I. 2005. Biotypes B and Q of Bemisia tabaci andtheir relevance to neonicotinoid and pyriproxyfen resistance.Archives of Insect Biochemistry and Physiology, 58,216-225

Hu J, De Barro P, Zhao H, Wang J, Nardi F. 2011. An extensivefield survey combined with a phylogenetic analysis revealsrapid and widespread invasion of two alien whiteflies inChina. PLoS ONE, 6, e16061.

Hu J, Chen Y D, Jian Z L, Nardi F, Yang T Y, Jin J, Zhang Z K.2014. Global analysis of the whitefly Bemisia tabaci crypticspecies Asia I in Asia. Motochondrial DNA, 2, 232-241. doi,10.3109/19401736.2013.830289

Jiu M, Zhou X P, Tong L, Xu J, Yang X, Wan F H, Liu S S. 2007.Vector-virus mutualism accelerates population increase ofan invasive whitefly. PLoS ONE, 2, e182.

Jones D R. 2003. Plant viruses transmitted by whiteflies.European Journal of Plant Pathology, 109, 195-219

Jukes T H, Cantor C R. 1996. Evolution of protein molecules.In: Munroled H N, ed., Mammalian Protein Metabolis.Academic Press, New York. pp. 31-132

Legg J P, French R, Rogan D, Okao-Okuja G, Brown J K.2002. A distinct Bemisia tabaci (Gennadius) (Hemiptera:Sternorrhynca: Aleyrodidae) genotype cluster is associatedwith the epidemic of severe cassava mosaic virus diseasein Uganda. Molecular Ecology, 11, 1219-1229

Liu S S, De Barro P J, Xu J, Luan J B, Zang L S, Ruan Y M, Wan F H. 2007. Asymmetric mating interactions drive widespreadinvasion and displacement in a whitefly. Science, 318,1769-1772

Liu S S, Colvin J, De Barro P J. 2012. Species concepts asapplied to the whitefly Bemisia tabaci systematics: Howmany species are there? Journal of Integrative Agriculture,11, 176-186

McKenzie C L, Bethke J A, Byrne F J, Chamberlin J R, DennehyT J, Dickey A M, Gilrein D, Hall P M, Ludwig S, Oetting R D,Osborne L S, Schmale L, Shatters Jr R G. 2012. Distributionof Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes inNorth America after the Q invasion. Journal of EconomicEntomology, 105, 753-766

Nei M, Tajima F. 1983. Maximum likelihood estimation of thenumber of nucleotide substitutions from restriction sitesdata. Genetics, 105, 207-217

Nene Y L. 1972. A Survey of Viral Diseases of Pulse Crops inUttar Pradesh. Govind Ballabh Pant University of Agricultureand Technology. Pantnagar, Uttaranchal, India. p. 191.

Polston J E, De Barro P, Boykin L M. 2014. Transmissionspecificities of plant viruses with the newly identified speciesof the Bemisia tabaci species complex. Pest ManagementScience. doi, 10.1002/ps.3738

Pond S L K, Frost S D, Muse S V. 2005. HyPhy: hypothesistesting using phylogenies. Bioinformatics, 21, 676-679

Posada D, Crandall K A. 1998. Modeltest: Testing the model ofDNA substitution. Bioinformatics, 14, 817-818

Pospieszny H, Borodynko N, Obrepalska-Steplowska A, HasiowB. 2007. The first report of Tomato torrado virus in Poland.Plant Disease, 91, 1364.

Ramappa H K, Muniyappa V, Colvin J. 1998. The contributionof tomato and alternative host plants to tomato leaf curl virusinoculum pressure in different areas of south India. Annalsof Applied Biology, 133, 187-198

Rao Q, Wang S, Su Y L, Bing X L, Liu S S, Wang X W. 2012.Draft genome sequence of ‘Candidatus Hamiltonelladefensa’, an endosymbiont of the whitefly Bemisia tabaci.Journal of Bacteriology, 194, 3558.

Rekha A R, Maruthi M N, Muniyappa V, Colvin J. 2005.Occurrence of three genotypic clusters of Bemisia tabaciand the rapid spread of the B biotype in south India.Entomologia Experimentalis et Applicata, 117, 221-233

Ronquist F, Teslenko M, van der Mark P, Ayres D L, DarlingA, Höhna S, Larget B, Liu L, Suchard M A, HuelsenbeckJ P. 2012. MrBayes 3.2: Efficient Bayesian phylogeneticinference and model choice across a large model space.Systematic Biology, 61, 539-542

Rozas J, Sanchez-Delbarrio J C, Messegeuer X, Rozas R.2003. DnaSP, DNA polymorphism analyses by coalescentand other methods. Bioinformatics, 19, 2496-2497

Saleem H M, Bedford I D, Evans A A F, Markham P G. 2003.Geminivirus transmission by different biotypes of thewhitefly Bemisia tabaci (Gennadius). Pakistan Journal ofZoology, 35, 343-351

Schuster D J, Mueller T F, Kring J B, Priece J F. 1990.Relationship of the sweetpotato whitefly to a new tomatofruit disorder in Florida. Hort Science, 25, 1618-1620

Shankarappa K S, Rangaswamy K T, Narayana D S A, Rekha AR, Raghavendra N. 2007. Development of silverleaf assay,protein and nucleic acid-based diagnostic techniques forthe quick and reliable detection and monitoring of biotypeB of the whitefly, Bemisia tabaci (Gennadius). Bulletin ofEntomological Research, 97, 503-513

Simon B, Cenis J L, Beitia F, Khalid S, Moreno I M, Fraile A. 2003.Genetic structure of field populations of begomoviruses andof their vector Bemisia tabaci in Pakistan. Phytopathology,93, 1422-1422

Su Y, He W B, Wang J, Li J M, Liu S S, Wang X W. 2013.Selection of endogenous reference genes for geneexpression analysis in the Mediterranean species of theBemisia tabaci (Hemiptera: Aleyrodidae) complex. Journalof Economic Entomology, 106, 1446-1455

Sun D B, Xu J, Luan J B, Liu S S. 2011. Reproductiveincompatibility between the B and Q biotypes of the whiteflyBemisia tabaci: genetic and behavioural evidence. Bulletinof Entomological Research, 101, 211-220

Suteri B D. 1974. Occurrence of soybean yellow mosaic virusin Uttar Pradesh. Current Science, 43, 689-690

Varma A, Mandal B, Manoj K S. 2011. Global emergenceand spread of whitefly (Bemisia tabaci) transmittedgeminiviruses. In: Thompson, Winston M O, ed., TheWhitefly, Bemisia tabaci (Homoptera: Aleyrodidae)Interaction with Geminivirus-Infected Host Plants. Springer,pp. 205-292

Wang H L, Yang J, Boykin L M, Zhao Q Y, Li Q, Wang X W,Liu S S. 2013. The characteristics and expression profilesof the mitochondrial genome for the Mediterranean speciesof the Bemisia tabaci complex. BMC Genomics, 14, 401.

Wang P, Crowder D W, Liu S S. 2012. Roles of matingbehavioural interactions and life history traits in thecompetition between alien and indigenous whiteflies.Bulletin of Entomological Research, 102, 1-11

Wang P, Ruan Y M, Liu S S. 2010. Crossing experiments andbehavioural observations reveal reproductive incompatibilityamong three putative species of the whitefly Bemisia tabaci.Insect Science, 17, 508-516

Wang X W, Luan J B, Li J M, Su Y L, Xia J, Liu S S. 2011.Transcriptome analysis and comparison reveal divergencebetween two invasive whitefly cryptic species. BMCGenomics, 12, 458.

Wrather A, Shannon G, Balardin R, Carregal L, Escobar R,Gupta G K, Ma Z, Morel W, Ploper D, Tenuta A. 2010. Effectof diseases on soybean yield in the top eight producingcountries in 2006. Plant Health Progress. doi,10.1094/PHP-2010-0125-01-RS

Wright S. 1951. The genetical structure of populations. Annalsof Eugenics, 15, 323-354.

Xu J, De Barro P J, Liu S S. 2010. Reproductive incompatibilityamong genetic groups of Bemisia tabaci supports theproposition that the whitefly is a cryptic species complex.Bulletin of Entomological Research, 100, 359–366.
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