Neotropical Entomology

, Volume 48, Issue 2, pp 207–218 | Cite as

Genetic Status and Endosymbionts Diversity of Bemisia tabaci (Gennadius) on Hosts Belonging to Family Malvaceae in India

  • T R HashmiEmail author
  • S R Devi
  • A Ahmad
  • N M Meshram
  • R Prasad
Ecology, Behavior and Bionomics


A study was instigated to examine the genetic status and distribution of known endosymbionts namely Portiera, Rickettsia, Wolbachia, Cardinium, and Arsenophonus in the populations of Bemisia tabaci (Gennadius) from three host plants: cotton (Gossypium herbaceum), okra (Abelmoschus esculentus L.), and China rose (Hibiscus rosa-sinensis) belonging to the family Malvaceae. The presence of four secondary endosymbionts Rickettsia, Wolbachia, Cardinium, and Arsenophonus was checked in Bemisia tabaci populations. Phylogenetic analyses grounded on the mitochondrial cytochrome oxidase I gene (mtCO1) unveiled the presence of Asia 1, Asia II 1, and Asia II 7 genetic groups for Bemisia tabaci on abovementioned crops. Individuals were examined for symbiotic bacterial infection with specific primers amplifying the 16S rRNA gene for Portiera, Rickettsia, Cardinium, and Wolbachia, and the 23S rRNA gene for Arsenophonus. The results show that Portiera was present in all the Bemisia tabaci samples. However, variations were noted in the circulation frequencies of secondary endosymbionts among the Bemisia tabaci populations. A significant difference was noticed in the distribution frequency of Rickettsia between cotton and China rose or okra with their p values as 0.016 and 0.033 respectively. The uneven incidence of secondary endosymbionts ropes the assumption that each endosymbiotic bacterium not only has a role in the endurance but may contribute to the polyphagous nature of Bemisia tabaci. It also brings an uncomplicated evidence for progressive studies on control measures of this notorious insect pest.


Host diversity endosymbionts genetic group insect 



The authors are very grateful to Dr. V. V. Ramamurthy [Rtd. Professor] of the Division of Entomology at I.A.R.I, New Delhi, India, and Mrs. Asha Gaur [Chief Technical Officer] at I.A.R.I, New Delhi, India, for their helpful comments, suggestions, and discussion to accomplish this research work.

Authors’ contributions

TRH and NMM conceived and designed experiments. TRH and SRD contributed to field work, performed the experiment, and analyzed data. NMM and RP contributed reagents/materials/analysis tools/editing of the manuscript. TRH and AA wrote the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169Google Scholar
  2. Baumann P (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189CrossRefGoogle Scholar
  3. Baumann P, Baumann L, Lai CY, Rouhbakhsh D, Moran NA, Clark MA (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49:55–94. CrossRefGoogle Scholar
  4. Baumann L, Thao ML, Funk CJ, Ng JCK, Baumann P, Falk BW (2004) Sequence analysis of DNA fragments from the genome of the primary endosymbiont of the whitefly Bemisia tabaci. Curr Microbiol 48(1):77–81CrossRefGoogle Scholar
  5. Bing XL, Yang J, Zchori-Fein E, Xiao-We W, Shu-Sheng L (2013) Characterization of a newly discovered symbiont in the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Entomol Zool 79(2):569Google Scholar
  6. Boykin LM, Shatters RGJ, Rosell RC, McKenzie CL, Bagnall RA, De Barro PJ, Frohlich DR (2007) Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Mol Phylogenet Evol 44:1306–1319CrossRefGoogle Scholar
  7. Boykin LM, Armstrong KF, Kubatko L, De Barro P (2012) Species delimitation and global biosecurity. Evol Bioinforma 8:1–37CrossRefGoogle Scholar
  8. Brune A, Ohkuma M (2001) Role of the termite gut microbiota in symbiotic digestion. In: Biology of termites: a modern synthesis. Springer Netherlands, Dordrecht, pp 439–475Google Scholar
  9. Cahill M, Denholm I, Bryne FJ, Devonshire AL (1996) Insecticide resistance in Bemisia tabaci status and implications for management. Proceeding of Brighton Crop Protection Conference. Pests and Diseases 1:75–80Google Scholar
  10. 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 97:407–413CrossRefGoogle Scholar
  11. Chu D, Gao C, De Barro PJ, Zhang Y, Wan F, Khan I (2011) Further insights into the strange role of bacterial endosymbionts in whitefly, Bemisia tabaci: comparison of secondary symbionts from biotypes B and Q in China. Bull Entomol Res 101:477–486CrossRefGoogle Scholar
  12. Dalton R (2006) The Christmas invasion. Nature 443:898–900CrossRefGoogle Scholar
  13. De Barro PJ, Liu SS, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19CrossRefGoogle Scholar
  14. Dedeine F, Bouletreau M, Vavre F (2005) Wolbachia requirement for oogenesis: occurrence within the genus Asobara (Hymenoptera, Braconidae) and evidence for intraspecific variation in A. tabida. Heredity 95:394–400CrossRefGoogle Scholar
  15. Dinsdale A, Cook L, Riginos C, Buckley YM, De Barro PJ (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidae: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am 103:196–208CrossRefGoogle Scholar
  16. Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–27CrossRefGoogle Scholar
  17. Elbaz M, Lahav N, Morin S (2010) Evidence for prezygotic reproductive barrier between the B and Q biotypes of Bemisia tabaci. Bull Entomol Res 100:581–590CrossRefGoogle Scholar
  18. Ellango R, Singh ST, Rana VS, Gayatri Priya N, Raina H, Chaubey R, Naveen NC, Mahmood R, Ramamurthy VV, Asokan R, Rajagopal R (2015) Distribution of Bemisia tabaci genetic groups in India. Environ Entomol 44(4):1258–1264CrossRefGoogle Scholar
  19. Everett KDE, Thao M, Horn M, Dyszynski GE, Baumann P (2005) Novel chlamydiae in whiteflies and scale insects: endosymbionts “Candidatus Fritschea bemisiae” strain Falk and “Candidatus Fritschea eriococci” strain Elm. Int J Syst Evol Microbiol 55(Pt 4):1581–1587CrossRefGoogle Scholar
  20. Ferrari J, Darby AC, Daniell TJ, Godfray HCJ, Douglas AE (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol Entomol 29:60–65CrossRefGoogle Scholar
  21. Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR, Mandelco L, Brenner DJ (1991) NOTES: Arsenophonus nasoniae gen. nov, sp. nov, the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int J Syst Evol Microbiol 41:563–565Google Scholar
  22. Gnankiné O, Mouton L, Henri H, Terraz G, Houndeté T, Martin T, Vavre F, Fleury F (2013) Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv Divers 6(3):411–421CrossRefGoogle Scholar
  23. Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl Environ Microbiol 72(5):3646–3652CrossRefGoogle Scholar
  24. Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D, Chiel E, Gottlieb Y, Ghanim M, Zchori-Fein E, Fleury F (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol Ecol 19:4365–4378CrossRefGoogle Scholar
  25. Hashmi TR, Dey D, Prasad R (2016a) Diversity of associated endosymbionts of Bemisia tabaci (Gennadius) on solanaceous host plants in India. Indian J Sci Technol 9(40):1–7Google Scholar
  26. Hashmi TR, Naveen NC, Dey D, Meshram NM, Prasad R (2016b) Evaluation of endosymbionts in different developmental stages of three population of Bemisia tabaci. Int J Innov Res Adv Stud 3(10):272–275Google Scholar
  27. Hashmi TR, Dey D, Prasad R (2017) Distribution frequency of endosymbionts and genetic characterisation of Bemisia tabaci (Hemiptera: Aleyrodidae) on fabaceous host plants in India. Orient Insects 52:1–15. Google Scholar
  28. Hashmi TR, Devi SR, Meshram NM, Prasad R (2018) Assessment of bacterial endosymbionts and the host, Bemisia tabaci (Hemiptera: Aleyrodidae), using rRNA and mitochondrial cytochrome oxidase I gene sequences. Commun Integr Biol (11):1, e1433442Google Scholar
  29. Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P (1999) Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci U S A 96:6814–6819CrossRefGoogle Scholar
  30. Hongoh Y, Ohkuma M, Kudo T (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 44:231–242CrossRefGoogle Scholar
  31. 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 58:216–225CrossRefGoogle Scholar
  32. Hosokawa T, Kikuchi Y, Meng XY, Fukatsu T (2005) The making of symbiont capsule in the plataspid stinkbug Megacopta punctatissima. FEMS Microbiol Ecol 54:471–477CrossRefGoogle Scholar
  33. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23(10):403–405CrossRefGoogle Scholar
  34. Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219CrossRefGoogle Scholar
  35. Kaltenpoth M, Goettler W, Dale C, Stubblefield JW, Herzner G, Roeser-Mueller K et al (2006) ‘Candidatus Streptomyces philanthi’, an endosymbiotic streptomycete in the antennae of Philanthus digger wasps. Int J Syst Evol Microbiol 56:1403–1411CrossRefGoogle Scholar
  36. Khasdan V, Levin I, Rosner A, Levin I, Rosner A, Morin S, Kontsedalov S, Maslenin L, Horowitz AR (2005) DNA markers for identifying biotypes B and Q of Bemisia tabaci (Hemiptera: Aleyrodidae) and studying population dynamics. Bull Entomol Res 95:605–613CrossRefGoogle Scholar
  37. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120CrossRefGoogle Scholar
  38. Liu SS, Colvin J, De Barro PJ (2012) Species concepts as applied to the whitefly Bemisia tabaci systematics: how many species are there? J Integr Agric 11:176–186CrossRefGoogle Scholar
  39. Marubayashi JM, Kliot A, Yuki VA, Rezende JAM, Krause-Sakate R, Pavan MA, Ghanim M (2014) Diversity and localization of bacterial endosymbionts from whitefly species collected in Brazil. PLoS One 9(9):e108363. CrossRefGoogle Scholar
  40. Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195CrossRefGoogle Scholar
  41. Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A 104:8627–8633CrossRefGoogle Scholar
  42. Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H (2005) The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci U S A 102(47):16919–16926CrossRefGoogle Scholar
  43. Moya A, Peretó J, Gil R, Latorre A (2008) Learning how to live together: genomic insights into prokaryote–animal symbioses. Nat Rev Genet 9(3):218–229CrossRefGoogle Scholar
  44. Muyzer G, Hottentrager S, Teske A, Wawer C (1996) Denaturing gradient gel electrophoresis of PCR amplified 16s rDNA—a new molecular approach to analyze the genetic diversity of mixed microbial communities. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual 3.4.4. Kluwer Academic Publishers, Dordrecht, pp 1–23Google Scholar
  45. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 100:1803–1807CrossRefGoogle Scholar
  46. Pascual S, Callejas C (2004) Intra- and interspecific competition between biotypes B and Q of Bemisia tabaci (Hemiptera: Aleyrodidae) from Spain. Bull Entomol Res 94:369–375CrossRefGoogle Scholar
  47. Roopa HK, Rebijith KB, Asokan R, Mahmood R, Krishna Kumar NK (2014) Isolation and identification of culturable bacteria from honeydew of whitefly, Bemisia tabaci (G.) (Hemiptera: Aleyrodidae). Meta Gene 2:114–122CrossRefGoogle Scholar
  48. Sasaki-Fukatsu K, Koga R, Nikoh N, Yoshizawa K, Kasai S, Mihara M (2006) Symbiotic bacteria associated with stomach discs of human lice. Appl Environ Microbiol 72:7349–7352CrossRefGoogle Scholar
  49. 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(2):411–419CrossRefGoogle Scholar
  50. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729CrossRefGoogle Scholar
  51. Tay WT, Evans GA, Boykin LM, De Barro PJ (2012) Will the real Bemisia tabaci please stand up? PLoS One 7:e50550CrossRefGoogle Scholar
  52. Thao ML, Baumann P (2004) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol 70(6):3401–3406CrossRefGoogle Scholar
  53. Wang P, Ruan YM, Liu SS (2010) Crossing experiments and behavioral observations reveal reproductive incompatibility among three putative species of the whitefly Bemisia tabaci. Insect Sci 17:508–516CrossRefGoogle Scholar
  54. Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex ratio distorting endosymbiotic bacterium among arthropods. Proc Biol Sci 270(1526):1857–1865CrossRefGoogle Scholar
  55. Xu J, De Barro PJ, Liu SS (2010) Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex. Bull Entomol Res 100:359–366CrossRefGoogle Scholar
  56. Zchori-fein AE, Brown JK (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Ann Entomol Soc Am 95(6):711–718CrossRefGoogle Scholar

Copyright information

© Sociedade Entomológica do Brasil 2018

Authors and Affiliations

  1. 1.Division of EntomologyIndian Agricultural Research InstituteNew DelhiIndia
  2. 2.Amity Institute of Microbial TechnologyAmity UniversityNoidaIndia

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