Skip to main content

Advertisement

SpringerLink
Log in

Comparative transmission of Bhendi yellow vein mosaic virus by two cryptic species of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae)

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

The leaf sample from okra plants showing prominent yellow vein mosaic symptoms and healthy plant without any virus symptoms were collected from farmer’s field. The presence of begomovirus in the infected sample was confirmed by polymerase chain reaction (PCR) and the amplicons were cloned and sequenced. The genome analysis showed that the isolate in the present study had 99% nucleotide identity with Bhendi yellow vein mosaic virus (BYVMV) revealing it as BYVMV variant. The genetic species of Bemisia tabaci collected from fields were identified as Asia-1 and MEAM-1 genetic species based on silver leaf assay, sequence characterized amplified region marker, and mtCOI gene sequence. The comparative virus–vector relationship of both genetic species of B. tabaci indicates a minimum of two and three B. tabaci in MEAM-1 and Asia-1 genetic species, respectively, per plant were required to transmit the disease. The minimum acquisition access period and inoculation access period of 15 (MEAM-1) and 20 min (Asia-1) were required to transmit the YVMD; it was further confirmed by nucleic acid hybridization using coat protein gene-specific probe of BYVMV. With respect to the sex, the female B. tabaci were more efficient in transmitting the disease as compared to male ones in both the genetic species of B. tabaci. The MEAM-1 to transmit the BYVMV more efficiently than Asia-1 genetic species of B. tabaci.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  Google Scholar 

  • Arguello-Astorga GR, Ruiz-Medrano R (2001) An iteron-related domain is associated to motif 1 in the replication proteins of geminiviruses: identification of potential interacting amino acid-base pairs by a comparative approach. Arch Virol 146:1465–1485

    Article  CAS  Google Scholar 

  • Atzmon G, Hadassa VO, Czosnek H (1998) PCR amplification of tomato yellow leaf curl virus (TYLCV) DNA from squashes of plants and whitefly vectors: application to study of TYLCV acquisition and transmission. Eur J Plant Pathol 104:189–194

    Article  CAS  Google Scholar 

  • Banks GK, Colvin J, Chowda Reddy RK, Maruthi MN, Muniyappa V, Venkatesh HM, Kirankumar M, Padmaja AS, Beitia FJ, Seal SF (2001) First report of B. tabaci, B-biotype in India and an associated tomato leaf curl virus disease epidemic. Plant Dis 85:231

    Article  Google Scholar 

  • Bedford ID, Briddon RW, Brown JK, Rossel RC, Markham PG (1994) Geminivirus transmission and biological characterisation of Bemisia tabaci (Genn.) biotypes from different geographic regions. Ann App Biol 125:311–325

    Article  Google Scholar 

  • Botstein DRL, White M, Skolnick DR (1980) Construction of a genetic map in man using restriction fragment length polymorphism. Am J Human Gen 32:314–331

    CAS  Google Scholar 

  • Boykin LM, Bell CD, Evans G, Small I, Barro PJD (2013) Is agriculture driving the diversification of the Bemisia tabaci species complex (Hemiptera: sternorrhyncha: Aleyrodidae)? Dating, diversification and biogeographic evidence revealed. BMC Evol Biol 13:228–238

    Article  Google Scholar 

  • Briddon RW, Stanley J (2006) Subviral agents associated with plant single-stranded DNA viruses. Virology 344:198–210

    Article  CAS  Google Scholar 

  • Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG (2002) Universal primers for the PCR-mediated amplification of DNA beta: a molecule associated with some monopartite begomoviruses. Mol Biotechnol 20:315–318

    Article  CAS  Google Scholar 

  • Brown JK, Bird J, Frohlich DR, Russell RC, Bedford ID, Markham PG (1995) The relevance of variability within the Bemisia tabaci species complex to epidemics caused by sub-group–III geminiviruses. In: Gerling D and Mayer RT (eds) Bemisia, taxonomy, biology, damage, control and management. Intercept Ltd., UK, pp 77–89

  • Brown JK, Zerbini FM, Navas-Castillo J, Moriones E, Ramos-Sobrinho R, Jose CF, Silva Fiallo-Olive E, Briddon RW, Hernandez-Zepeda C, Idris A, Malathi VG, Martin DP, Rivera-Bustamante R, Ueda S, Varsani A (2015) Revision of begomovirus taxonomy based on pairwise sequence comparisons. Arch Virol 160(6):1593–1619

    Article  CAS  Google Scholar 

  • Capoor SP, Varma PM (1950) Yellow vein mosaic of H. esculentus L. Indian J Agric Sci 20:217–230

    Google Scholar 

  • Cervera MT, Cabezas JA, Simon B, Martinez-Zapater JM, Beitia F, Cenis JL (2000) Genetic relationships among biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae) based on AFLP analysis. Bull Entomol Res 90:391–396

    Article  CAS  Google Scholar 

  • Chenulu VV, Venkateswarlu V, Rangaraju R (1979) Studies on yellow mosaic disease of mungbean. Indian Phytopath 32:230–235

    Google Scholar 

  • Chowda-Reddy RV, Kirankumar M, Seal SE, Muniyappa V, Girish B, Valand GM, Colvin J (2012) Bemisia tabaci phylogenetic groups in India and the relative transmission efficacy of tomato leaf curl Bangalore virus by an indigenous and an exotic population. J Integr Agric 11(2):235–248

    Article  Google Scholar 

  • Czosnek H, Ber R, Navot N, Zamir D, Antignus Y, Cohen S (1988) Detection of tomato yellow leaf curl virus in lysates of plants and insects by hybridization with a viral DNA probe. Plant Dis 72:949–951

    Article  Google Scholar 

  • Czosnek H, Ghanim M, Ghanim M (2002) The 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

    Article  Google Scholar 

  • De Barro PJ, Driver F (1997) Use of RAPD-PCR to distinguish the B-biotype from other biotypes of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Aust J Entomol 36:149–152

    Article  Google Scholar 

  • De Barro PJ, Liu SS, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19

    Article  Google Scholar 

  • Dinsdale A, Cook L, Riginos C, Buckley Y, De Barro PJ (2010) Refined global analysis of Bemisia tabaci (Gennadius) (Hemiptera: Sternorrhyncha: Aleyrodoidea) mitochondrial CO1 to identify species level genetic boundaries. Ann Entomol Soc Am 103:196–208

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Frohlich DR, Torres-Jerez I, Bedford ID, Markham PG, Brown JK (1999) A phylogeographical analysis of Bemisia tabaci species complex based on mitochondrial DNA markers. Mol Ecol 8:1683–1691

    Article  CAS  Google Scholar 

  • Hanley-Bowdoin L, Settleage SB, Orozco BM, Nagar S, Robertson D (1999) Geminivirus: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Plant Sci 18:71–106

    Article  CAS  Google Scholar 

  • Idris AM, Brown JK (1998) Sinaloa tomato leaf curl geminivirus: biological and molecular evidence for a new subgroup III virus. Phytopathology 88:648–657

    Article  CAS  Google Scholar 

  • Kumar J, Kumar A, Roy JK, Tuli R, Khan JA (2010) Identification and molecular characterization of begomovirus and associated satellite DNA molecules infecting Cyamopsis tetragonoloba. Virus Genes 41:118–125

    Article  CAS  Google Scholar 

  • Lee W, Park J, Lee GS, Lee S, Akimoto S (2013) Taxonomic status of the Bemisia tabaci complex (Hemiptera: Aleyrodidae) and reassessment of the number of its constituent species. PLoS ONE 8:e63817

    Article  CAS  Google Scholar 

  • Lefeuvre P, Martin DP, Harkins G, Lemey P, Gray AJA, 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 Pathog 6:e1001164

    Article  Google Scholar 

  • Li SF, Onodera S, Sano T, Yoshida K, Wang GP, Shikata E (1995) Gene diagnosis of viroid: comparisons of return-PAGE and hybridization using DIG-labelled DNA and RNA probes for practical diagnosis of hop stunt, citrus exocortis and apple scar skin viroids in their natural host plants. Ann Phytopatol Soc Jpn 61:381–390

    Article  CAS  Google Scholar 

  • Mahesh YS, Shankarappa KS, Rangaswamy KT, Prameela HA, Aswathanarayana DS, Nagesha N, Maruthi MN (2010) Detection and characterisation of a begomovirus associated with leaf curl disease of ornamental croton (Codiaeum variegatum). J Hortic Sci Biotech 85(2):101–105

    Article  CAS  Google Scholar 

  • Mandal B, Muniyappa V (1991) Transmission of Croton yellow vein mosaic virus by Bemisia tabaci: virus-vector relationship. Fitopatol Bras 16:260–262

    Google Scholar 

  • Maruthi MN, Rekha R, Muniyappa V (2007) Pumpkin yellow vein mosaic disease is caused by two distinct begomoviruses: complete viral sequences and comparative transmission by an indigenous Bemisia tabaci and the introduced B-biotype. EPPO Bull 37:412–419

    Article  Google Scholar 

  • Mathew AV, Muniyappa V (1991) Transmission of Indian cassava mosaic virus by Bemisia tabaci. Fitopatol Brarileira 16:46–49

    Google Scholar 

  • Morales FJ, Anderson PK (2001) The emergence and dissemination of whitefly transmitted viruses in Latin America. Arch Virol 146:415–441

    Article  CAS  Google Scholar 

  • Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9(9):1–8

    Article  Google Scholar 

  • Muniyappa V, Reddy HR (1976) Studies on the yellow mosaic disease of horsegram (Dolichos biflorus L.)—virus vector relationships. Mysore J Agric Sci 10:605–610

    Google Scholar 

  • Murugesan S, Chellaiah S (1977) Transmission of greengram yellow mosaic virus by the whitefly, Bemisia tabaci. Madras Agric J 64:437–438

    Google Scholar 

  • Nakahara KHT, Hataya T, Sugimoto T, Kimura I, Shigata E (1998) A mixture of synthetic probes labelled with biotin for the sensitive detection of potato spindle tuber viroid. J Virol Methods 71:219–227

    Article  CAS  Google Scholar 

  • Narayana DSA, Shankarappa KS, Govindappa MR, Prameela HA, Gururaj Rao MR, Rangaswamy KT (2006) Natural occurrence of jatropha mosaic virus disease in India. Curr Sci 91:585–586

    Google Scholar 

  • Narayana DSA, Rangaswamy KT, Shankarappa KS, Maruthi MN, Reddy CNL, Rekha AR, Murthy KVK (2007) Distinct begomovirus closely related to cassava mosaic viruses cause Indian jatropha mosaic disease. Int J Virol 3:1–11

    Article  CAS  Google Scholar 

  • Nateshan HM, Muniyappa V, Swanson MM, Harrison BD (1996) Host range, vector relations and serological relationships of cotton leaf curl virus from southern India. Ann Appl Biol 128:233–244

    Article  Google Scholar 

  • Padidam M, Beachy RN, Fauquet M (1995) Classification and identification of geminivirus using sequence comparison. J Gen Virol 76:249–263

    Article  CAS  Google Scholar 

  • Pan HP, Chu D, Yan WQ, Su Q, Liu BM, Wang SL, Wu QJ, Xie W, Jiao XG, Li RM, Yang N, Yang X, Xu BY, Zhang YJ (2012) Rapid spread of tomato yellow leaf curl virus in China is aided differentially by two invasive whiteflies. PLoS ONE 7:e34817

    Article  CAS  Google Scholar 

  • Perring TM, Cooper AD, Rodriguez RJ, Farrar CA, Bellows TS (1993) Identification of a whitefly species by genomic and behavioural studies. Science 259:74–77

    Article  CAS  Google Scholar 

  • Polston JE, Anderson PK (1997) The emergence of whitefly-transmitted geminiviruses in tomato in the Western hemisphere. Plant Dis 81:358–1369

    Article  Google Scholar 

  • 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 80:851–856

    Article  Google Scholar 

  • Power GP (2000) Insect transmission of plant viruses: a constraint on virus variability. Biotic Interact 2:336–340

    Google Scholar 

  • Pun KB, Doraiswamy S (1999) Effect of age of okra plants on susceptibility to okra yellow vein mosaic virus. Indian J Virol 15:57–58

    Google Scholar 

  • Rathi YPS, Nene YL (1974) Some aspects of the relationship between mungbean yellow mosaic virus and its vector Bemisia tabaci. Indian Phytopath 27:459–462

    Google Scholar 

  • Rekha AR, Maruthi MN, Muniyappa V, Colvin J (2005) Occurrence of three genotypic clusters of Bemisia tabaci and the rapid spread of the B biotype in south India. Entomol Exp Appl 117:221–233

    Article  Google Scholar 

  • Rodriguez R, Ramos PL, Vivian D, Velazquez K, Rudy P, Fuentes A, Pujol M (2003) Establishment of a non-radioactive nucleic acid hybridization technique for begomovirus detection. Biotechnol Apl 20:164–169

    CAS  Google Scholar 

  • Rojas MR, Gilbertson RL, Russel DR, Maxwell DP (1993) Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Dis 77:340–347

    Article  CAS  Google Scholar 

  • Romero-Durban JC, Cambra M, Vila DN (1995) A simple imprint-hybridization method for detection of viroids. J Virol Methods 55:37–47

    Article  CAS  Google Scholar 

  • Saunders K, Bedford ID, Briddon RW, Markham PG, Wong SM, Stanley J (2000) A unique virus complex causes Ageratum yellow vein disease. Proc Natl Acad Sci USA 97:6890–6895

    Article  CAS  Google Scholar 

  • Shankarappa KS, Rangaswamy KT, Aswatha Narayana DS, Rekha AR, Raghavendra N, Lashminarayanareddy CN, Chancellor TCB, Maruthi MN (2007) Development of silver leaf assay, protein and nucleic acid-based diagnostic techniques for the quick and reliable detection and monitoring of biotype B of the whitefly, Bemisia tabaci (Gennadius). Bull Entomol Res 97(5):503–511

    Article  CAS  Google Scholar 

  • Simmons AM, Ling KS, Harrison HF, Jackson DM (2009) Sweet potato leaf curl virus: efficiency of acquisition, retention and transmission by Bemisia tabaci (Hemiptera: Aleyrodidae). Crop Prot 28:1007–1011

    Article  CAS  Google Scholar 

  • Simon C, Frati F, Beckembach A, Crespi B, Liu B, Flook P (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    Article  CAS  Google Scholar 

  • Singh SJ (1980) Studies on epidemiology of yellow vein mosaic virus of okra. Indian J Mycol Plant Path 10:35–39

    Google Scholar 

  • Singh RP, Boucher A, Laksman DK, Tavantzis SM (1994) Multimeric non-radioactive cRNA probes improve detection of potato spindle tuber viroid (PSTVd). J Virol Methods 49:221–234

    Article  Google Scholar 

  • Singh ST, Priya NG, Kumar J, Rana VS, Ellango R, Joshi A, Priyadarshini G, Asokan R, Rajagopal R (2012) Diversity and phylogenetic analysis of endosymbiotic bacteria from field caught Bemisia tabaci from different locations of north India based on 16S rDNA library screening. Infect Genet Evol 12:411–419

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Molecular Evolutionary genetics analysis verison 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Varma A, Malathi VG (2003) Emerging geminivirus problems: a serious threat to crop production. Ann Appl Biol 142:145–164

    Article  CAS  Google Scholar 

  • Venkataravanappa V, Reddy CNL, Swaranalatha P, Jalali S, Briddon RW, Krishna Reddy M (2011) Diversity and phylogeography of begomovirus-associated beta satellites of okra in India. Virol J 8:555

    Article  CAS  Google Scholar 

  • Venkataravanappa V, Reddy CNL, Jalali S, Krishna Reddy M (2012) Molecular characterization of distinct bipartite begomovirus infecting bhendi (Abelmoschus esculentus L.) in India. Virus Genes 44:522–535

    Article  CAS  Google Scholar 

  • Venkataravanappa V, Reddy CNL, Krishna Reddy M (2013) Begomovirus characterization and development of phenotypic and DNA-based diagnostics for screening of okra genotype resistance against Bhendi yellow vein mosaic virus. 3 Biotech 3:461–470

    Article  CAS  Google Scholar 

  • Venkataravanappa V, Reddy CNL, Jalali S, Briddon RW, Krishna Reddy M (2015a) Molecular identification and biological characterization of a begomovirus associated with okra enation leaf curl disease in India. Eur J Plant Pathol 141:217–235

    Article  CAS  Google Scholar 

  • Venkataravanappa V, Reddy CNL, Jalali S, Krishna Reddy M (2015b) Association of tomato leaf curl New Delhi virus DNA-B with bhendi yellow vein mosaic virus in okra showing yellow vein mosaic disease symptoms. Acta Virol 59:125–139

    Article  CAS  Google Scholar 

  • Venkataravanappa V, Prasannaa HC, Reddy CNL, Krishna Reddy M (2014) Evidence for two predominant viral lineages, recombination and subpopulation structure in begomoviruses associated with yellow vein mosaic disease of okra in India. Plant Pathol 64(3):508–518

    Article  Google Scholar 

Download references

Acknowledgements

The research was supported by the project title “Establishment of association of begomovirus species with yellow vein mosaic disease (YVMD) in wild and cultivated species of okra and identification of source of resistance to the most predominant virus” funded by the National Fund for Basic and Strategic Research in Agricultural Sciences (NFBSFARA), Indian Council of Agricultural Research, Government of India, New Delhi, India.

Author information

Authors and Affiliations

  1. Division of Plant Pathology, Central Horticultural Experimental Station, ICAR-Institute of Horticultural Research, Hessaraghatta Lake PO, Chettalli, Bangalore, 571248, India

    V. Venkataravanappa

  2. ICAR-Indian Institute of Vegetable Research, Varanasi, 221305, Uttar Pradesh, India

    M. H. Kodandaram

  3. Department of Plant Pathology, College of Sericulture, University of Agricultural Sciences, Chintamani, Bangalore, 563125, Karnataka, India

    C. N. Lakshminarayana Reddy

  4. Department of Plant Pathology, College of Horticulture, University of Horticultural Sciences, Bagalkot, Bengaluru, 560065, Karnataka, India

    K. S. Shankarappa

  5. Division of Plant Pathology, Plant Virology Laboratory, ICAR-Indian Institute of Horticultural Research, Hessaraghatta Lake PO, Bangalore, 560089, Karnataka, India

    M. Krishna Reddy

Authors
  1. V. Venkataravanappa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. H. Kodandaram
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. N. Lakshminarayana Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. S. Shankarappa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Krishna Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to V. Venkataravanappa or M. Krishna Reddy.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Venkataravanappa, V., Kodandaram, M.H., Lakshminarayana Reddy, C.N. et al. Comparative transmission of Bhendi yellow vein mosaic virus by two cryptic species of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). 3 Biotech 7, 331 (2017). https://doi.org/10.1007/s13205-017-0970-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-017-0970-8

Keywords

Search

Navigation