Abstract
Bemisia tabaci species complex (whitefly) is one of the most dangerous pests that destroy many important crops worldwide. It causes damage to the host plant by feeding on phloem sap as well as transmitting a wide range of devastating plant viruses (especially begomoviruses) that cause severe epidemics on crops. To fend off the menace, modern genomic-based strategies have been adapted to minimize the crop losses due to this destructive pest. Genetic engineering techniques, e.g., transgenics and RNA interference (RNAi) have shown promising results in controlling B. tabaci in plants; however, these techniques often face challenges due to the concerns about GMOs in food crops. With the enhanced knowledge about B. tabaci genomics, new technologies, e.g., manipulation of microbiota or CRISPR-based genome editing have shown promising results in several insect pests and could have an instrumental role in controlling agricultural pests including whitefly. Genome editing is an eco-friendly approach that can be employed to suppress or even destroy the target species. In this review, we have discussed B. tabaci as a pest and advancement in control strategies of B. tabaci. Various potential targets for genome editing have also been discussed that could be used in gene-editing technologies for the efficient management of B. tabaci and the viruses it transmits. Finally, we also outlined the future perspective and effective use of genome editing technology in developing CRISPR-based gene drive for whitefly population modification, suppression, and eradication.
Similar content being viewed by others
References
Aapola U, Shibuya K, Scott HS, Ollila J, Vihinen M, Heino M, Shintani A, Kawasaki K, Minoshima S, Krohn K (2000) Isolation and initial characterization of a novel zinc finger gene, DNMT3L, on 21q22. 3, related to the cytosine-5-methyltransferase 3 gene family. Genomics 65:293–298. https://doi.org/10.1006/geno.2000.6168
Abudayyeh OO, Gootenberg JS, Essletzbichler P, Han S, Joung J, Belanto JJ, Verdine V, Cox DB, Kellner MJ, Regev A (2017) RNA targeting with CRISPR–Cas13. Nature 550:280–284. https://doi.org/10.1038/nature24049
Ahmad M, Akhtar KP (2018) Susceptibility of cotton whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) to diverse pesticides in Pakistan. J Econ Entomol 111:1834–1841. https://doi.org/10.1093/jee/toy112
Ahmad M, Khan RA (2017) Field-evolved resistance of Bemisia tabaci (Hemiptera: Aleyrodidae) to carbodiimide and neonicotinoids in Pakistan. J Econ Entomol 110:1235–1242. https://doi.org/10.1093/jee/tox058
Akbari OS, Bellen HJ, Bier E, Bullock SL, Burt A, Church GM, Cook KR, Duchek P, Edwards OR, Esvelt KM (2015) Safeguarding gene drive experiments in the laboratory. Science 349:927–929. https://doi.org/10.1126/science.aac7932
Ali MF, Morgan ED (1990) Chemical communication in insect communities: a guide to insect pheromones with special emphasis on social insects. Biol Rev 65:227–247. https://doi.org/10.1111/j.1469-185X.1990.tb01425.x
Aman R, Ali Z, Butt H, Mahas A, Aljedaani F, Khan MZ, Ding S, Mahfouz M (2018) RNA virus interference via CRISPR/Cas13a system in plants. Genome Biol 19:1–9. https://doi.org/10.1186/s13059-017-1381-1
Amukamara AU, Washington JT, Sanchez Z, McKinney EC, Moore AJ, Schmitz RJ, Moore PJ (2020) More than DNA methylation: does pleiotropy drive the complex pattern of evolution of Dnmt1? Front Ecol Evol 8:4. https://doi.org/10.3389/fevo.2020.00004
Andreason SA, Shelby EA, Moss JB, Moore PJ, Moore AJ, Simmons AM (2020) Whitefly endosymbionts: biology, evolution, and plant virus interactions. Insects 11:775. https://doi.org/10.3390/insects11110775
Anreiter I, Sokolowski MB (2019) The foraging gene and its behavioral effects: pleiotropy and plasticity. Annu Rev Genet 53:373–392. https://doi.org/10.1146/annurev-genet-112618-043536
Arosio P, Ingrassia R, Cavadini P (2009) Ferritins: a family of molecules for iron storage, antioxidation and more. Biochim Biophys Acta 1790:589–599. https://doi.org/10.1016/j.bbagen.2008.09.004
Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189. https://doi.org/10.1146/annurev.micro.59.030804.121041
Bewick AJ, Sanchez Z, Mckinney EC, Moore AJ, Moore PJ, Schmitz RJ (2019) Dnmt1 is essential for egg production and embryo viability in the large milkweed bug, Oncopeltus fasciatus. Epigenetics Chromatin 12:1–14. https://doi.org/10.1186/s13072-018-0246-5
Borgio JF (2010) RNAi mediated gene knockdown in sucking and chewing insect pests. J Biopestic 3:386. http://www.jbiopest.com/users/lw8/efiles/francis_borgio.pdf
Brown JK (2009) Phylogenetic biology of the Bemisia tabaci sibling species group. In: Bemisia: bionomics and management of a global pest, pp. 31–67. Springer. doi: https://doi.org/10.1007/978-90-481-2460-2_2
Burt A, Crisanti A (2018) Gene drive: evolved and synthetic. ACS Chem Biol 13:343–346. https://doi.org/10.1021/acschembio.7b01031
Byrne DN, Bellows T (1991) Whitefly biology. Ann Rev Entomol 36:431–457. https://doi.org/10.1146/annurev.en.36.010191.002243
Campanacci V, Lartigue A, Hällberg BM, Jones TA, Giudici-Orticoni M-T, Tegoni M, Cambillau C (2003) Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding. Proc Natl Acad Sci U S A 100:5069–5074. https://doi.org/10.1073/pnas.0836654100
Caragata EP, Walker T (2012) Using bacteria to treat diseases. Expert Opin Biol Ther 12:701–712. https://doi.org/10.1517/14712598.2012.677429
Carter V, Underhill A, Baber I, Sylla L, Baby M, Larget-Thiery I, Zettor A, Bourgouin C, Langel Ü, Faye I (2013) Killer bee molecules: antimicrobial peptides as effector molecules to target sporogonic stages of Plasmodium. PLoS Pathog 9:e1003790. https://doi.org/10.1371/journal.ppat.1003790
Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17:1140–1153. https://doi.org/10.1111/mpp.12375
Chen W, Hasegawa DK, Kaur N, Kliot A, Pinheiro PV, Luan J, Stensmyr MC, Zheng Y, Liu W, Sun H (2016) The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. BMC Biol 14:1–15. https://doi.org/10.1186/s12915-016-0321-y
Chen W, Wosula EN, Hasegawa DK, Casinga C, Shirima RR, Fiaboe KK, Hanna R, Fosto A, Goergen G, Tamò M (2019) Genome of the African cassava whitefly Bemisia tabaci and distribution and genetic diversity of cassava-colonizing whiteflies in Africa. Insect Biochem Mol Biol 110:112–120. https://doi.org/10.1016/j.ibmb.2019.05.003
Chi Y, Pan L-L, Liu S-S, Mansoor S, Wang X-W (2021) Implication of the whitefly protein Vps Twenty Associated 1 (Vta1) in the transmission of cotton leaf curl Multan virus. Microorganisms 9:304. https://doi.org/10.3390/microorganisms9020304
Christiaens O, Smagghe G (2014) The challenge of RNAi-mediated control of hemipterans. Curr Opin Insect Sci 6:15–21. https://doi.org/10.1016/j.cois.2014.09.012
Clynen E, Bellés X, Piulachs M-D (2011) Conservation of fruitless’ role as master regulator of male courtship behaviour from cockroaches to flies. Dev Genes Evol 221:43–48. https://doi.org/10.1007/s00427-011-0352-x
Coon KL, Vogel KJ, Brown MR, Strand MR (2014) Mosquitoes rely on their gut microbiota for development. Mol Ecol 23:2727–2739. https://doi.org/10.1111/mec.12771
Costa JT (2018) The other insect societies: overview and new directions. Curr Opin Insect Sci 28:40–49. https://doi.org/10.1016/j.cois.2018.04.008
Courtier-Orgogozo V, Morizot B, Boëte C (2017) Agricultural pest control with CRISPR-based gene drive: time for public debate: Should we use gene drive for pest control? EMBO Rep 18:878–880. https://doi.org/10.15252/embr.201744205
Dearden PK, Gemmell NJ, Mercier OR, Lester PJ, Scott MJ, Newcomb RD, Buckley TR, Jacobs JM, Goldson SG, Penman DR (2018) The potential for the use of gene drives for pest control in New Zealand: a perspective. J R Soc N Z 48:225–244. https://doi.org/10.1080/03036758.2017.1385030
Dinsdale A, Cook L, Riginos C, Buckley Y, De Barro P (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc 103:196–208. https://doi.org/10.1603/AN09061
do Nascimento Silva J, GM Mascarin, R de Paula Vieira de Castro, LR Castilho and DM Freire (2019) Novel combination of a biosurfactant with entomopathogenic fungi enhances efficacy against Bemisia whitefly. Pest Manag Sci 75:2882–2891. https://doi.org/10.1002/ps.5458
Eakteiman G, Moses-Koch R, Moshitzky P, Mestre-Rincon N, Vassão DG, Luck K, Sertchook R, Malka O, Morin S (2018) Targeting detoxification genes by phloem-mediated RNAi: a new approach for controlling phloem-feeding insect pests. Insect Biochem Mol Biol 100:10–21. https://doi.org/10.1016/j.ibmb.2018.05.008
Fiallo-Olivé E, Pan L-L, Liu S-S, Navas-Castillo J (2020) Transmission of begomoviruses and other whitefly-borne viruses: dependence on the vector species. Phytopathology 110:10–17. https://doi.org/10.1094/PHYTO-07-19-0273-FI
Finley KD, Taylor BJ, Milstein M, McKeown M (1997) dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster. Proc Natl Acad Sci U S A 94:913–918. https://doi.org/10.1073/pnas.94.3.913
Firdaus S, van Heusden AW, Hidayati N, Supena EDJ, Mumm R, de Vos RC, Visser RG, Vosman B (2013) Identification and QTL mapping of whitefly resistance components in Solanum galapagense. Theor Appl Genet 126:1487–1501. https://doi.org/10.1007/s00122-013-2067-z
Fortes IM, Fernández-Muñoz R, Moriones E (2020) Host plant resistance to Bemisia tabaci to control damage caused in tomato plants by the emerging crinivirus tomato chlorosis virus. Front Plant Sci 11:1574. https://doi.org/10.3389/fpls.2020.585510
Geng L, Qian L-X, Shao R-X, Liu Y-Q, Liu S-S, Wang X-W (2018) Transcriptome profiling of whitefly guts in response to Tomato yellow leaf curl virus infection. Virol J 15:1–12. https://doi.org/10.1186/s12985-018-0926-6
Ghosh S, Ghanim M (2021) Factors determining transmission of persistent viruses by Bemisia tabaci and emergence of new virus-vector relationships. Viruses 13:1808. https://doi.org/10.3390/v13091808
Gilbertson RL, Batuman O, Webster CG, Adkins S (2015) Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Ann Rev Virol 2:67–93. https://doi.org/10.1146/annurev-virology-031413-085410
Götz M, Popovski S, Kollenberg M, Gorovits R, Brown JK, Cicero JM, Czosnek H, Winter S, Ghanim M (2012) Implication of Bemisia tabaci heat shock protein 70 in begomovirus-whitefly interactions. J Virol 86:13241–13252. https://doi.org/10.1128/JVI.00880-12
Guilinger JP, Thompson DB, Liu DR (2014) Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 32:577. https://doi.org/10.1038/nbt.2909
Gustafson EA, Wessel GM (2010) Vasa genes: emerging roles in the germ line and in multipotent cells. BioEssays 32:626–637. https://doi.org/10.1002/bies.201000001
Hasegawa DK, Chen W, Zheng Y, Kaur N, Wintermantel WM, Simmons AM, Fei Z, Ling K-S (2018) Comparative transcriptome analysis reveals networks of genes activated in the whitefly, Bemisia tabaci when fed on tomato plants infected with Tomato yellow leaf curl virus. Virology 513:52–64. https://doi.org/10.1016/j.virol.2017.10.008
Havron A, Rosen D, Rössler Y, Hillel J (1987) Selection on the male hemizygous genotype in arrhenotokous insects and mites. Entomophaga 32:261–268. https://doi.org/10.1007/BF02373249
He C, Liu S, Liang J, Zeng Y, Wang S, Wu Q, Xie W, Zhang Y (2020) Genome-wide identification and analysis of nuclear receptors genes for lethal screening against Bemisia tabaci Q. Pest Manag Sci 76:2040–2048. https://doi.org/10.1002/ps.5738
Heu CC, McCullough FM, Luan J, Rasgon JL (2020) CRISPR-Cas9-based genome editing in the silverleaf whitefly (Bemisia tabaci). CRISPR J 3:89–96. https://doi.org/10.1089/crispr.2019.0067
Horowitz AR, Ghanim M, Roditakis E, Nauen R, Ishaaya I (2020) Insecticide resistance and its management in Bemisia tabaci species. J Pest Sci 93:893–910. https://doi.org/10.1007/s10340-020-01210-0
Huang HJ, Ye ZX, Lu G, Zhang CX, Chen JP, Li JM (2020) Identification of salivary proteins in the whitefly Bemisia tabaci by transcriptomic and LC–MS/MS analyses. Insect Sci 00:1–13. https://doi.org/10.1111/1744-7917.12856
Jain RG, Robinson KE, Asgari S, Mitter N (2021) Current scenario of RNAi-based hemipteran control. Pest Manag Sci 77:2188–2196. https://doi.org/10.1002/ps.6153
Kanakala S, Ghanim M (2016) Implication of the whitefly Bemisia tabaci cyclophilin B protein in the transmission of Tomato yellow leaf curl virus. Front Plant Sci 7:1702. https://doi.org/10.3389/fpls.2016.01702
Kaur N, Chen W, Zheng Y, Hasegawa DK, Ling K-S, Fei Z, Wintermantel WM (2017) Transcriptome analysis of the whitefly, Bemisia tabaci MEAM1 during feeding on tomato infected with the crinivirus, Tomato chlorosis virus, identifies a temporal shift in gene expression and differential regulation of novel orphan genes. BMC Genom 18:1–20. https://doi.org/10.1186/s12864-017-3751-1
Landmann F (2019) The Wolbachia endosymbionts. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.BAI-0018-2019
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220. https://doi.org/10.1038/nrg2719
Li F, Dewer Y, Li D, Qu C, Luo C (2021) Functional and evolutionary characterization of chemosensory protein CSP2 in the whitefly, Bemisia tabaci. Pest Manag Sci 77:378–388. https://doi.org/10.1002/ps.6027
Liu T-X, Stansly PA, Gerling D (2015) Whitefly parasitoids: distribution, life history, bionomics, and utilization. Ann Rev Entomol 60:273–292. https://doi.org/10.1146/annurev-ento-010814-021101
Luo Y, Chen Q, Luan J, Chung SH, Van Eck J, Turgeon R, Douglas AE (2017) Towards an understanding of the molecular basis of effective RNAi against a global insect pest, the whitefly Bemisia tabaci. Insect Biochem Mol Biol 88:21–29. https://doi.org/10.1016/j.ibmb.2017.07.005
Lyko F (2018) The DNA methyltransferase family: a versatile toolkit for epigenetic regulation. Nat Rev Genet 19:81–92. https://doi.org/10.1038/nrg.2017.80
Mahmood MA, Ahmed N, Hussain S, Muntaha ST, Amin I, Mansoor S (2022) Dominance of Asia II 1 species of Bemisia tabaci in Pakistan and beyond. Sci Rep 12:1–13. https://doi.org/10.1038/s41598-022-05612-1
Makarova KS, Wolf YI, Koonin EV (2018) Classification and nomenclature of CRISPR-Cas systems: where from here? CRISPR J 1:325–336. https://doi.org/10.1089/crispr.2018.0033
Maleszka J, Foret S, Saint R, Maleszka R (2007) RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honeybee (Apis mellifera). Dev Genes Evol 217:189–196. https://doi.org/10.1007/s00427-006-0127-y
Martin JH (2004) Whiteflies of Belize (Hemiptera: Aleyrodidae). Part 1-introduction and account of the subfamily Aleurodicinae Quaintance & Baker. Moscas blancas de Belice (Hemiptera: Aleyrodidae). Zootaxa 681:1–119. https://doi.org/10.11646/zootaxa.1098.1.1
McFarlane GR, Whitelaw CBA, Lillico SG (2018) CRISPR-based gene drives for pest control. Trends Biotechnol 36:130–133. https://doi.org/10.1016/j.tibtech.2017.10.001
McKenzie SK, Oxley PR, Kronauer DJ (2014) Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins. BMC Genom 15:1–14. https://doi.org/10.1186/1471-2164-15-718
Medina RF (2018) Gene drives and the management of agricultural pests. J Responsible Innov 5:S255–S262. https://doi.org/10.1080/23299460.2017.1407913
Mitter N, Worrall EA, Robinson KE, Li P, Jain RG, Taochy C, Fletcher SJ, Carroll BJ, Lu GM, Xu ZP (2017) Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat Plants 3:1–10. https://doi.org/10.1038/nplants.2016.207
Naqvi RZ, SS-e-A Zaidi, KP Akhtar, S Strickler, M Woldemariam, B Mishra, MS Mukhtar, BE Scheffler, JA Scheffler and G Jander (2017) Transcriptomics reveals multiple resistance mechanisms against cotton leaf curl disease in a naturally immune cotton species, Gossypium arboreum. Sci Rep 7:1–15. https://doi.org/10.1038/s41598-017-15963-9
Naqvi RZ, SS-e-A Zaidi, MS Mukhtar, I Amin, B Mishra, S Strickler, LA Mueller, M Asif and S Mansoor (2019) Transcriptomic analysis of cultivated cotton Gossypium hirsutum provides insights into host responses upon whitefly-mediated transmission of cotton leaf curl disease. PLoS One 14:e0210011. https://doi.org/10.1371/journal.pone.0210011
Nässel DR, Winther ÅM (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42–104. https://doi.org/10.1016/j.pneurobio.2010.04.010
Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S (2011) Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 49:219–248. https://doi.org/10.1146/annurev-phyto-072910-095235
Naveen N, Chaubey R, Kumar D, Rebijith K, Rajagopal R, Subrahmanyam B, Subramanian S (2017) Insecticide resistance status in the whitefly, Bemisia tabaci genetic groups Asia-I, Asia-II-1 and Asia-II-7 on the Indian subcontinent. Sci Rep 7:1–15. https://doi.org/10.1038/srep40634
Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257. https://doi.org/10.1016/S0092-8674(00)81656-6
Olivera S, Rodriguez-Ithurralde D, Henley JM (2003) Acetylcholinesterase promotes neurite elongation, synapse formation, and surface expression of AMPA receptors in hippocampal neurones. Mol Cell Neurosci 23:96–106. https://doi.org/10.1016/S1044-7431(03)00021-6
Pelosi P, Iovinella I, Zhu J, Wang G, Dani FR (2018) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biol Rev 93:184–200. https://doi.org/10.1111/brv.12339
Perring TM, PA Stansly, T Liu, HA Smith and SA Andreason (2018) Whiteflies: Biology, ecology, and management. In: Sustainable management of arthropod pests of tomato, pp. 73–110. Elsevier. https://doi.org/10.1016/B978-0-12-802441-6.00004-8
Pyott DE, Sheehan E, Molnar A (2016) Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol Plant Pathol 17:1276–1288. https://doi.org/10.1111/mpp.12417
Qadri M, Short S, Gast K, Hernandez J, Wong AC-N (2020) Microbiome innovation in agriculture: development of microbial based tools for insect pest management. Front Sustain Food Syst 4:547751. https://doi.org/10.3389/fsufs.2020.547751
Reaume CJ, Sokolowski MB (2011) Conservation of gene function in behaviour. Philos Trans R Soc Lond B Biol Sci 366:2100–2110. https://doi.org/10.1098/rstb.2011.0028
Rehman M, Chakraborty P, Tanti B, Mandal B, Ghosh A (2021) Occurrence of a new cryptic species of Bemisia tabaci (Hemiptera: Aleyrodidae): an updated record of cryptic diversity in India. Phytoparasitica. https://doi.org/10.1007/s12600-021-00909-9
Ridley EV, Wong AC, Douglas AE (2013) Microbe-dependent and nonspecific effects of procedures to eliminate the resident microbiota from Drosophila melanogaster. Appl Environ Microbiol 79:3209–3214. https://doi.org/10.1128/AEM.00206-13
Ryuda M, Tsuzuki S, Matsumoto H, Oda Y, Tanimura T, Hayakawa Y (2011) Identification of a novel gene, anorexia, regulating feeding activity via insulin signaling in Drosophila melanogaster. J Biol Chem 286:38417–38426. https://doi.org/10.1074/jbc.M111.267344
Sani I, Ismail SI, Abdullah S, Jalinas J, Jamian S, Saad N (2020) A review of the biology and control of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), with special reference to biological control using entomopathogenic fungi. Insects 11:619. https://doi.org/10.3390/insects11090619
Schlaeger S, Pickett JA, Birkett MA (2018) Prospects for management of whitefly using plant semiochemicals, compared with related pests. Pest Manag Sci 74:2405–2411. https://doi.org/10.1002/ps.5058
Schmitz RJ, Lewis ZA, Goll MG (2019) DNA methylation: shared and divergent features across eukaryotes. Trends Genet 35:818–827. https://doi.org/10.1016/j.tig.2019.07.007
Scott JG, Michel K, Bartholomay LC, Siegfried BD, Hunter WB, Smagghe G, Zhu KY, Douglas AE (2013) Towards the elements of successful insect RNAi. J Insect Physiol 59:1212–1221. https://doi.org/10.1016/j.jinsphys.2013.08.014
Sekiné K, Furusawa T, Hatakeyama M (2015) The boule gene is essential for spermatogenesis of haploid insect male. Dev Biol 399:154–163. https://doi.org/10.1016/j.ydbio.2014.12.027
Shapira M, Thompson CK, Soreq H, Robinson GE (2001) Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies. J Mol Neurosci 17:1–12. https://doi.org/10.1385/JMN:17:1:1
Shukla J, Nagaraju J (2010) Doublesex: a conserved downstream gene controlled by diverse upstream regulators. J Genet 89:341–356. https://doi.org/10.1007/s12041-010-0046-6
Smargon AA, Cox DB, Pyzocha NK, Zheng K, Slaymaker IM, Gootenberg JS, Abudayyeh OA, Essletzbichler P, Shmakov S, Makarova KS (2017) Cas13b is a type VI-B CRISPR-associated RNA-guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Mol Cell 65(618–630):e617. https://doi.org/10.1016/j.molcel.2016.12.023
Snyder JC, Simmons AM, Thacker RR (1998) Attractancy and ovipositional response of adult Bemisia argentifolii (Homoptera: Aleyrodidae) to type IV trichome density on leaves of Lycopersicon hirsutum grown in three day-length regimes. J Entomol Sci 33:270–281. https://doi.org/10.18474/0749-8004-33.3.270
Stangier J, Hilbich C, Burdzik S, Keller R (1992) Orcokinin: a novel myotropic peptide from the nervous system of the crayfish, Orconectes limosus. Peptides 13:859–864. https://doi.org/10.1016/0196-9781(92)90041-Z
Su Q, Peng Z, Tong H, Xie W, Wang S, Wu Q, Zhang J, Li C, Zhang Y (2019) A salivary ferritin in the whitefly suppresses plant defenses and facilitates host exploitation. J Exp Bot 70:3343–3355. https://doi.org/10.1093/jxb/erz152
Su Y-L, Li J-M, Li M, Luan J-B, Ye X-D, Wang X-W, Liu S-S (2012) Transcriptomic analysis of the salivary glands of an invasive whitefly. PLoS ONE 7:e39303. https://doi.org/10.1371/journal.pone.0039303
Suhag A, Yadav H, Chaudhary D, Subramanian S, Jaiwal R, Jaiwal PK (2020) Biotechnological interventions for the sustainable management of a global pest, whitefly (Bemisia tabaci). Insect Sci. https://doi.org/10.1111/1744-7917.12853
Tan X, Hu N, Zhang F, Ramirez-Romero R, Desneux N, Wang S, Ge F (2016) Mixed release of two parasitoids and a polyphagous ladybird as a potential strategy to control the tobacco whitefly Bemisia tabaci. Sci Rep 6:1–9. https://doi.org/10.1038/srep28245
Teem JL, Alphey L, Descamps S, Edgington MP, Edwards O, Gemmell N, Harvey-Samuel T, Melnick RL, Oh KP, Piaggio AJ (2020) Genetic biocontrol for invasive species. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2020.00452
Wang N, Zhao P, Ma Y, Yao X, Sun Y, Huang X, Jin J, Zhang Y, Zhu C, Fang R (2019a) A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance. Philos Trans R Soc B 374:20180313. https://doi.org/10.1098/rstb.2018.0313
Wang P, Heitman J (2005) The cyclophilins. Genome Biol 6:1–6. https://doi.org/10.1186/gb-2005-6-7-226
Wang X-W, Luan J-B, Li J-M, Su Y-L, Xia J, Liu S-S (2011) Transcriptome analysis and comparison reveal divergence between two invasive whitefly cryptic species. BMC Genet 12:1–12. https://doi.org/10.1186/1471-2164-12-458
Wang X, Xu J, Wang X, Qiu B, Cuthbertson AG, Du C, Wu J, Ali S (2019b) Isaria fumosorosea-based zero-valent iron nanoparticles affect the growth and survival of sweet potato whitefly, Bemisia tabaci (Gennadius). Pest Manag Sci 75:2174–2181. https://doi.org/10.1002/ps.5340
Wang Y-J, Wang H-L, Wang X-W, Liu S-S (2020) Transcriptome analysis and comparison reveal divergence between the Mediterranean and the greenhouse whiteflies. PLoS ONE 15:e0237744. https://doi.org/10.1371/journal.pone.0237744
Wang ZZ, Bing Xl, Liu SS, Chen XX (2017) RNA interference of an antimicrobial peptide, Btdef, reduces Tomato yellow leaf curl China virus accumulation in the whitefly Bemisia tabaci. Pest Manag Sci 73:1421–1427. https://doi.org/10.1002/ps.4472
Werren JH (1997) Biology of wolbachia. Annu Rev Entomol 42:587–609. https://doi.org/10.1146/annurev.ento.42.1.587
Winston WM, Molodowitch C, Hunter CP (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295:2456–2459. https://doi.org/10.1126/science.1068836
Wu S, MD Toews, C Oliveira-Hofman, RW Behle, AM Simmons and DI Shapiro-Ilan (2020) Environmental tolerance of entomopathogenic fungi: a new strain of Cordyceps javanica isolated from a whitefly epizootic versus commercial fungal strains. Insects 11:711. https://sciprofiles.com/profile/909473
Xie W, Chen C, Yang Z, Guo L, Yang X, Wang D, Chen M, Huang J, Wen Y, Zeng Y (2017) Genome sequencing of the sweetpotato whitefly Bemisia tabaci MED/Q. GigaScience. https://doi.org/10.1093/gigascience/gix018
Xu H-X, Qian L-X, Wang X-W, Shao R-X, Hong Y, Liu S-S, Wang X-W (2019) A salivary effector enables whitefly to feed on host plants by eliciting salicylic acid-signaling pathway. Proc Natl Acad Sci U S A 116:490–495. https://doi.org/10.1073/pnas.1714990116
Yan S, Ren B, Zeng B, Shen J (2020) Improving RNAi efficiency for pest control in crop species. Biotechniques 68:283–290. https://doi.org/10.2144/btn-2019-0171
Ye X-D, Su Y-L, Zhao Q-Y, Xia W-Q, Liu S-S, Wang X-W (2014) Transcriptomic analyses reveal the adaptive features and biological differences of guts from two invasive whitefly species. BMC Genom 15:1–12. https://doi.org/10.1186/1471-2164-15-370
Yokokura T, Ueda R, Yamamoto D (1995) Phenotypic and molecular characterization of croaker, a new mating behavior mutant of Drosophila melanogaster. Japan J Genet 70:103–117. https://doi.org/10.1266/jjg.70.103
You Y, Xie M, Ren N, Cheng X, Li J, Ma X, Zou M, Vasseur L, Gurr GM, You M (2015) Characterization and expression profiling of glutathione S-transferases in the diamondback moth, Plutella xylostella (L.). BMC Genom 16:1–13. https://doi.org/10.1186/s12864-015-1343-5
Zaidi SS-e-A, RW Briddon and S Mansoor, (2017a) Engineering dual begomovirus-Bemisia tabaci resistance in plants. Trends Plant Sci 22:6–8. https://doi.org/10.1016/j.tplants.2016.11.005
Zaidi SS-e-A, MM Mahfouz and S Mansoor (2017b) CRISPR-Cpf1: a new tool for plant genome editing. Trends Plant Sci 22:550–553. https://doi.org/10.1016/j.tplants.2017b.05.001
Zaidi SSeA, RZ Naqvi, M Asif, S Strickler, S Shakir, M Shafiq, AM Khan, I Amin, B Mishra and MS Mukhtar (2020) Molecular insight into cotton leaf curl geminivirus disease resistance in cultivated cotton (Gossypium hirsutum). Plant Biotechnol J. 18:691–706. https://doi.org/10.1111/pbi.13236
Zhang H, Demirer GS, Zhang H, Ye T, Goh NS, Aditham AJ, Cunningham FJ, Fan C, Landry MP (2019) DNA nanostructures coordinate gene silencing in mature plants. Proc Natl Acad Sci U S A 116:7543–7548. https://doi.org/10.1073/pnas.1818290116
Zhang Y-N, Ye Z-F, Yang K, Dong S-L (2014) Antenna-predominant and male-biased CSP19 of Sesamia inferens is able to bind the female sex pheromones and host plant volatiles. Gene 536:279–286. https://doi.org/10.1016/j.gene.2013.12.011
Zhao J, Lei T, Zhang X-J, Yin T-Y, Wang X-W, Liu S-S (2020) A vector whitefly endocytic receptor facilitates the entry of begomoviruses into its midgut cells via binding to virion capsid proteins. PLoS Pathog 16:e1009053. https://doi.org/10.1371/journal.ppat.1009053
Acknowledgments
Authors are highly grateful to Dr. Jodi Scheffler (USDA-ARS, Stoneville, MS, USA) for critical reading and improving the English language of this manuscript.
Funding
The authors have not disclosed any funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interest
The authors declare no competing interests.
Additional information
Communicated by Antonio Biondi.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mahmood, M.A., Naqvi, R.Z., Siddiqui, H.A. et al. Current knowledge and implementations of Bemisia tabaci genomic technologies for sustainable control. J Pest Sci 96, 427–440 (2023). https://doi.org/10.1007/s10340-022-01520-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-022-01520-5