Virus/vector interaction for aphids (Hemiptera: Aphididae) and whitefly (Hemiptera: Aleyrodidae)
DOI:
https://doi.org/10.35699/2447-6218.2019.15153Keywords:
Insect control, Molecular interaction virus/vector, Integrated pest management, RNAiAbstract
Impact caused by aphids and whiteflies has grown considerably in the last decades, due to the increase in population outbreaks of of these virus-transmitting pests in a variety of economically important crops. The acquisition and transmission of most phytopathogenic viruses by a vector insect is the central point of the cycle of an infection. Plant viruses can interact with their insect hosts in a variety of ways, in some cases even virus replication can occur in insect cells. Virus interaction with your host/vector insects requires specific molecular interactions between virus and host, commonly via proteins, however, which vector components are involved and how they work to facilitate transmission is not well understood. The focus of the present work was to perform a systematic review on the basic virus/vector relationships in aphids and whiteflies; to show the practices currently used in integrated pest management for aphids and whiteflies and to report how insect vector interactions are opening new doors for the control of insect plant virus vectors using new genetic and computational technologies. The systematic review methodology was used, the work was conducted in stages that involved the development of the review protocol with the research questions, the search strategy, the identification of the inclusion and exclusion criteria, the search in the databases, previously defined, critical evaluation, extraction of relevant data and synthesis. Identification of articles was realized in the PUBMED database www.ncbi.nlm.nih.gov/pubmed/. We concluded it is required to combine the use of new technologies such as RNAi with the tools already used in integrated pest management for greater effectiveness of aphid and whitefly control, however, the continued study and application of new molecular technologies in investigating virus-vector interactions will provide further assistance in the control of plant diseases spread by aphid and whitefly in the future.
References
Abdellatef, E.; Wil, T.; Koch, A.; Imani, J.; Vilcinskas, A.; Kogel, K-H.2015. Silencing the expression of the salivary sheath protein causes transgenerational feeding suppression in the aphid Sitobion avenae. Plant Biotechnology Journal, 13(6): 849–857.doi: 10.1111/pbi.12322
Abd-Rabou, S.; Simmons, A. M. 2012.Survey of Reproductive Host Plants of Bemisia tabaci (Hemiptera: Aleyrodidae) in Egypt, Including New Host Records . Entomological News, 121(5): 456–465. doi: 10.315/021.121.0507
Anderson, P. K. Cunningham, A. A.; Patel, N. G.; Morales, F. J.; Epstein, P. R.; Daszak, P. 2004. Emerging infectious diseases of plants: Pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology and Evolution, 19(10): 535–544. doi:10.1016/j.tree.2004.07.021
Blua, M. J.; Perring, T. M.; 1994. Madore, M. A. Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients. Journal of Chemical Ecology, 20(3): 691–707. doi: 10.1007/BF02059607
Boquel, S.; Giordanengo, P.; Ameline, A. 2011. Divergent effects of PVY-infected potato plant on aphids. European Journal of Plant Pathology, 129(4): 507–510. doi: 10.1007/s10658-010-9732-8
Bourtzis, K.; Dobson, S. L.; Xi, Z., Rasgon, J. L.; Calvitti, M.; Moreira, L. A.; Bossin, H. C.; Moretti, R.; Baton, L. A.; Hughes, G. L. 2014. Harnessing mosquito–Wolbachia symbiosis for vector and disease control. Acta tropica, 132: S150-S163.doi: 10.1016/j.actatropica.2013.11.004
Bragard, C.; Caciagli, P.; Lemaire, O.; Lopez-Moya, J.; MacFarlane, S.; Peters, D.; Susi, P.; Torrance, L.2013. Status and Prospects of Plant Virus Control Through Interference with Vector Transmission. Annual Review of Phytopathology, 51(1): 177–201. doi: 10.1146/annurev-phyto-082712-102346
Buckner, J. S. freeman, T. P.; Ruud, R. L.; Chu, C-c.; Henneberry, T. J.2002. Characterization and functions of the whitefly egg pedicel. Archives of Insect Biochemistry and Physiology, 49(1): 22–33. doi: 10.1002/arch.10006
Cabanillas, H. E.; Jones, W. A. 2009. Pathogenicity of Isaria sp. (Hypocreales: Clavicipitaceae) against the sweet potato whitefly B biotype, Bemisia tabaci (Hemiptera: Aleyrodidae). Crop Protection, 28(4): 333–337. doi: 10.1016/j.cropro.2008.11.015
Casteel, C. L. Yang, C.; Nanduri, A. C.; De Jong, H. N.; Whitham, S. A.; Jander, G. 2014. The NIa-Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). Plant Journal, 77(4): 653–663. doi: 10.1111/tpj.12417
Casteel, C. L. De Alwis, M,; Bak, A.; Dong, H.; Whitham, S. A.; Jander, G. 2015. Disruption of Ethylene Responses by Turnip mosaic virus Mediates Suppression of Plant Defense against the Green Peach Aphid Vector. Plant Physiology, 169: 209-215. doi: 10.1104/pp.15.00332
Castle, S. J.; Berger, P. H. 1993. Rates of growth and increase of Myzus persicae on virus‐infected potatoes according to type of virus‐vector relationship. Entomologia Experimentalis et Applicata, 69(1): 51–60.
Chen, A. Y. S. Walker, G. P.; Carter, D.; Ng, J. C. K. 2011. A virus capsid component mediates virion retention and transmission by its insect vector. Proceedings of the National Academy of Sciences,108(40): 16777–16782. doi: 10.1073/pnas.1109384108
Chen, Q. Wang, H.; Ren, T.; Xie, L.; Wei, T. 2015. Interaction between non-structural protein Pns10 of rice dwarf virus and cytoplasmic actin of leafhoppers is correlated with insect vector specificity. Journal of General Virology, 96(4): 933–938. doi:10.1099/jgv.0.000022
Cicero, J. M.; Brown, J. K. 2011. Functional Anatomy of Whitefly Organs Associated With Squash Leaf Curl Virus (Geminiviridae: Begomovirus) Transmission by the B Biotype of Bemisia tabaci (Hemiptera: Aleyrodidae). Annals of the Entomological Society of America, 104(2): 261–279. doi: 10.1603/AN10075
Dângelo, R. A. C. Michereff-Filho, M.; Campos, M. R.; da Silva, P. S.; Guedes, R. N. C. 2018. Insecticide resistance and control failure likelihood of the whitefly Bemisia tabaci (MEAM1; B biotype): a Neotropical scenario. Annals of Applied Biology, 172(1): 88–99. doi: 10.1111/aab.12404
Daniell, H. Lin, C-S.; Yu, M.; Chang, W-J. 2016. Chloroplast genomes: Diversity, evolution, and applications in genetic engineering. Genome Biology, 17:1–29. doi: 10.1186/s13059-016-1004-2
De Barro, P. J.; liu, S-S.; Boykin, L. M.; Dinsdale, A. B.2011. Bemisia tabaci : A Statement of Species Status . Annual Review of Entomology, 56(1):1–19. doi: 10.1146/annurev-ento-112408-085504
De Paula, N. T.; De Faria, J. C.; Aragão, F. J. L. 2015. Reduction of viral load in whitefly (Bemisia tabaci Gen.) feeding on RNAi-mediated bean golden mosaic virus resistant transgenic bean plants. Virus Research, 210: 245–247. doi: 10.1016/j.virusres.2015.08.012
Dietzgen, R. G.; Mann, K. S.; Johnson, K. N. 2016. Plant virus-insect vector interactions: Current and potential future research directions. Viruses, 8(11): 1–21. doi: 10.3390/v8110303
Döring, T. F.; Chittka, L. 2007. Visual ecology of aphids—a critical review on the role of colours in host finding. Arthropod-Plant Interactions, 1(1): 3–16. doi: 10.1007/s11829-006-9000-1
Eigenbrode, S. D.; Ding, H.; Shiel, P.; Berger, P. H. 2002. Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proceedings of the Royal Society B: Biological Sciences, 269(1490):455–460. doi: 10.1098/rspb.2001.1909
Eigenbrode, S. D.; Bosque-Pérez, N. A.; Davis, T. S. 2017.Insect-Borne Plant Pathogens and Their Vectors: Ecology, Evolution, and Complex Interactions. Annual Review of Entomology, 63(1): 169–191. doi: 10.1146/annurev-ento-020117- 043119
Ellsworth, P. C.; Martinez-Carrillo, J. L. 2001. IPM for Bemisia tabaci: A case study from North America. Crop Protection, 20(9): 853–869. doi: 10.1016/S0261-2194(01)00116-8
Erdogan, C. Moores, D. G.; Gurkan, M. O.; Gorman, K. J.; Denholm, I. 2008. Insecticide resistance and biotype status of populations of the tobacco whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) from Turkey. Crop Protection, 27; 600–605. doi: 10.1016/j.cropro.2007.09.002
Faria, J. C.; Bezera, I. C.; Zerbini, F. M.; Ribeiro, S. G.; Lima, M. F. 2000. Situação Atual Das Geminiviroses no Brasil. Fitopatologia Brasileira, 25:125-137.
Faria, M.; Wraight, S. P. 2001. Biological control of Bemisia tabaci with fungi. Crop Protection, 20(9): 767–778. doi: 10.1016/S0261-2194(01)00110-7
Martin, B.; Collar, J. L.; Tjallingii, W. F.; Fereres, A. 1997. Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. Journal of General Virology, 78(10): 2701–2705. doi: 10.1099/0022-1317-78-10-2701
Gadhave, K. R. Dutta, B.; Coolong, T.; Srinivasan, R. 2019. A non-persistent aphid-transmitted Potyvirus differentially alters the vector and non-vector biology through host plant quality manipulation. Scientific Reports, 9(1): 1–12.doi: 10.1038/s41598-019-39256-5
Gerling, D.; Horowitz, A. R. 1986. Baumgaertner, J. Autecology of Bemisia tabaci. Agriculture, Ecosystems and Environment, 17: 5–19.
Pakkianathan, B. C.; Kontsedalov, S.; Lebedev, G.; Mahadav, A.; Zeidan, M.; Czosnek, H.; Ghanim, M. 2015. Replication of Tomato Yellow Leaf Curl Virus in Its Whitefly Vector, Bemisia tabaci. Journal of Virology, 89(19): 9871-9803. doi: 10.1128/JVI.00779-15
Ghanim, M.; Morin, S.; Czosnek, H. 2001. Rate of Tomato yellow leaf curl virus translocation in the Circulative Transmission Pathway of its Vector, the Whitefly Bemisia tabaci . Phytopathology, 91(2): 188–196. doi:10.1094/PHYTO.2001.91.2.188
Gibbs, A. J. Ohshima, K.; Phillips, M. J.; Gibbs, M; J. 2008. The Prehistory of Potyviruses : Their Initial Radiation Was during the Dawn of Agriculture. Plos One, 3(6): e2523. doi: 10.1371/journal.pone.0002523
Gilbertson, R. L. Batuman, O.; Webster, C. G.; adkins, S.2015. Role of the Insect Supervectors Bemisia tabaci and Frankliniella occidentalis in the Emergence and Global Spread of Plant Viruses . Annual Review of Virology, 2: 67–93. doi: 10.1146/annurev-virology-031413-085410
Glasa, M. Kúdela, O.; Marie-Jeanne, V.; Quiot, J. B. 2007. Evidence of a Naturally Occurring Recombinant Isolate of Plum pox virus from Slovakia . Plant Disease, 85(8): 920–920. doi: 10.1094/PDIS.2001.85.8.920C
Gray, S.; Cilia, M.; Ghanim, M. 2014. Circulative, “Nonpropagative” virus transmission: An orchestra of virus-, insect-, and plant-derived instruments. Advances in Virus Research, 89:141-189. doi: 10.1016/B978-0-12-800172-1.00004-5
Gray, S.; Gildow, F. E. L. 2003. Luteovirus-Aphid Interactions. Annual Review of Phytopathology, 41: 539–566. doi: 10.1146/annurev.phyto.41.012203.105815
Grover, S. Jindal, V.; Banta, G.; Taning, C. N. T.; Smagghe, G.; Christiaens, O.2019. Potential of RNA interference in the study and management of the whitefly, Bemisia tabaci. Archives of Insect Biochemistry and Physiology, 100(2): 1–17. doi: 10.1002/arch.21522
Gupta, V. 2012. Aphids on the world’s crops. An identification and information guide. Oriental Insects, 35:104–104. doi: 10.1080/00305316.2001.10417292
Gusmão, M. R.; Picanço, M. C.; Zanuncio, J. c.; Silva, D. J. H.; Barrigossi, J. A. F. 2005. Standardised sampling plan for Bemisia tabaci (Homoptera: Aleyrodidae) in outdoor tomatoes. Scientia Horticulturae, 103(4): 403–412. doi: 10.1016/j.scienta.2004.04.005
Hill, J. H.; Whitham, S. A. 2014. Control of Virus Diseases in Soybeans. Advances in Virus Research, 90: 355-390. doi: 10.1016/B978-0-12-801246-8.00007-X
Hogenhout, S. A.; Ammar, E-D.; Whitfield, A. E.; Redinbaugh, M. G. 2008. Insect Vector Interactions with Persistently Transmitted Viruses. Annual Review of Phytopathology, 46: 327–359. doi: 10.1146/annurev.phyto.022508.092135
Hoh, F.; Uzest, M.; Drucker, M.; Plisson-Chastang, C.; Bron, P.; Blanc, S.; Dumas, C.2010. Structural Insights into the Molecular Mechanisms of Cauliflower Mosaic Virus Transmission by Its Insect Vector. Journal of Virology, 84(9): 4706–4713. doi: 10.1128/JVI.02662-09
Inoue-Nagata, A. K.; Navas-Castillo, J.; Melo, P. C. T.; Avila, A. C. de. 2006. Busca por Tomato yellow leaf curl virus e Tomato yellow leaf curl Sardinia virus em tomateiros. Horticultura Brasileira, 22(4): 799–800. doi: 10.1590/S0102-05362004000400027.
Ivanov, K. I.; Eskelin, K.; Löhmus, A.; Mäkinen, K. 2014. Molecular and cellular mechanisms underlying potyvirus infection. Journal of General Virology, 95: 1415–1429. doi: 10.1099/vir.0.064220-0
Jacobson, A. L.; Duffy, S.; Sseruwagi, P. 2018. Whitefly-transmitted viruses threatening cassava production in Africa. Current Opinion in Virology, 33: 167–176. doi: 10.1016/j.coviro.2018.08.016
Kalleshwaraswamy, C. M.; Kumar, N. K. K. 2008. Transmission Efficiency of Papaya ringspot virus by Three Aphid Species . Phytopathology, 98(5): 541–546. doi: 10.1094/PHYTO-98-5-0541
Kasprowicz, L.; Gaynor, M.; Jon, P.; Brian, F. 2008. Spatial and temporal dynamics of Myzus persicae clones in fields and suction traps. Agricultural and Forest Entomology, 10(2): 91–100. doi: 10.1111/j.1461-9563.2008.00365.x
Khajuria, C.; Ivashuta, S.; Wiggins, E.; Flagel, L.; Moar, W.; Pleau, M.; Miller, K.; Zhang, Y.; et al. 2018. Development and characterization of the first dsRNA-resistant insect population from western corn rootworm, Diabrotica virgifera virgifera LeConte. PLoS ONE, 13(5): 1–19. doi: 10.1371/journal.pone.0197059
Krause-Sakate, R.; Fakhfakh, H.; Peypelut, M.; pavan, M. A.; Zerbini, F. M.; Marrakchi, M.; Candresse, T.; Le Gall, O. 2004. A naturally occurring recombinant isolate of Lettuce mosaic virus. Archives of Virology, 149: 191–197. doi: 10.1007/s00705-003-0201-y
Costa, E. M. R.; Marchese, A.; maluf, W.R.; Silva, A. A. 2014. Resistência de genótipos de couve-manteiga ao pulgão-verde e sua relação com a cerosidade foliar. Revista Ciência Agronômica, 45: 146–154.
Mauck, K. E.; Chesnais, Q.; Shapiro, L. R. 2018. Evolutionary Determinants of Host and Vector Manipulation by Plant Viruses. Advances in Virus Research. 101: 189-250. doi: 10.1016/bs.aivir.2018.02.007
Mauck, K. E.; De Moraes, C. M.; Mescher, M. C. 2014. Biochemical and physiological mechanisms underlying effects of Cucumber mosaic virus on host-plant traits that mediate transmission by aphid vectors. Plant, Cell and Environment, 37(6):1427–1439. doi: 10.1111/pce.12249
Mauck, K.; Bosque-Pérez, N. A.; Eigenbrode, S. D.; De Moraes, C. M.; Mescher, M. C. 2012. Transmission mechanisms shape pathogen effects on host-vector interactions: Evidence from plant viruses. Functional Ecology, 26(5): 1162–1175. doi: 10.1111/j.1365-2435.2012.02026.x
Mauck, K. E.; De Moraes, C. M.; Mescher, M. C. 2010. Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proceedings of the National Academy of Sciences, 107(8): 3600–3605. doi: 10. 10.1073/pnas.0907191107
Meekes, E. T. M.; Fransen, J. J.; Van Lenteren, J. C. 2002. Pathogenicity of Aschersonia spp. against whiteflies Bemisia argentifolii and Trialeurodes vaporariorum. Journal of Invertebrate Pathology, 81: 1–11, doi: 10.1016/S0022-2011(02)00150-7
Miller, G. L.; Foottit, R. G. 2017. The Taxonomy of Crop Pests : The Aphids. Insect Biodiversity: Science and Society, 1: 627–639. doi: 10.1002/9781118945568.ch20
Moran, N. A. 1992. The Evolution Of Aphid Life Cycles. Annual Review of Entomology, 37: 321–348. doi: 10.1146/annurev.en.37.010192.001541
Moreno, A.; Tjallingii, W. F.; Fernandez-Mata, G.; Fereres, A. 2019. Communication Differences in the mechanism of inoculation between a semi-persistent and a non-persistent aphid-transmitted plant virus. Journal of General Virology, 2012: 662–667. doi: 10.1099/vir.0.037887-0
Moriones, E.; Navas-Castillo, J. 2000. Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Research, 71: 123–134. doi: 10.1016/S0168-1702(00)00193-3
Naranjo, S. E.; Chu, C.-C.; Henneberry, T. J. 2003. Economic injury levels for Bemisia tabaci (Homoptera: Aleyrodidae) in cotton: impact of crop price, control costs, and efficacy of control. Crop Protection, 15(8): 779–788. doi: 10.1016/S0261-2194(96)00061-0
Nauen, R.; Denholm, I. 2005. Resistance of insect pests to neonicotinoid insecticides: Current status and future prospects. Archives of Insect Biochemistry and Physiology, 58(4): 200–215, 2005. doi: 10.1002/arch.20043
Navas-Castillo, J.; Fiallo-Olivé, E.; Sánchez-Campos, S. 2011. Emerging Virus Diseases Transmitted by Whiteflies.Annual Reveiew of Phytopathology, 49: 219-248. doi: 10.1146/annurev-phyto-072910-095235
Ng, J. C. K.; Falk, B. W. 2006. Virus-Vector Interactions Mediating Nonpersistent and Semipersistent Transmission of Plant Viruses. Annual Review of Phytopathology, 44: 183–212. doi: 10.225./annurev.phyto.44.070505.143325
Ng, J. C. K.; Perry, K. L. 2004. Transmission of plant viruses by aphid vectors. Molecular Plant Pathology, 5(6): 505–511. doi: 10.1111/j.1364-3703.2004.00240.x
Oliveira, M. R. V. de; Amancio, E.; Laumann, R. A.; Gomes, L de O.2003. Natural enemies of Bemisia tabaci (Gennadius) B biotype and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) in Brasília, Brazil. Neotropical Entomology, 32(1): 151–154. doi: 10.1590/S1519-566X2003000100023.
Palumbo, J. C.; Horowitz, A. R.; Prabhaker, N. 2001. Insecticidal control and resistance management for Bemisia tabaci. Crop Protection, 20(9): 739–765. doi: 10.1016/S0261-2194(01)00117-X
Pirone, T., P.; Perry, K., L. 2002. Aphids : Non-persistent Transmission. Advances in Botanical Research, 36: 1-19.doi: 10.1016/S0065-2296(02)36056-7
Quintela, E. D.; Abreu, A. G.; lima, J. F. dos S.; Mascarin, G. M.; Santos, J. B. dos. 2016. Reproduction of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) B biotype in maize fields (Zea mays L.) in Brazil. Pest management science, 72(1): 2181–2187. doi: 10.1002/ps.4259
Revers, F.; García, J. A. 2015. Molecular biology of potyviruses. Academic Press, 92: 101-199. doi: 10.1016/bs.aivir.2014.11.006
Rojas, M. R.; Macedo, M. A.; Maliano, M. R.; Soto-Aguilar, M.; Souza, J. O.; Briddon, R. W.; Kenyon, L.; Bustamante, R. F. R. et al. 2018. World Management of Geminiviruses. Annual Review of Phytopathology, 56: 637–677. doi: 10.1146/annurev-phyto-080615-100327
Sheveleva, A.; Ivanoc, P.; Gasanova, T.; Osipov, G.; Chirkov, S. 2018. Sequence Analysis of Plum pox virus Strain C Isolates from Russia Revealed Prevalence of the D96E Mutation in the Universal Epitope and Interstrain Recombination Events. Viruses, 10(9): 450. doi: 10.3390/v10090450
Sicard, A.; Zeddam, J-L.; Yvon, M.; Michalakis, Y.; Gutiérrez, S.; Blanc, S. 2015. Circulative Nonpropagative Aphid Transmission of Nanoviruses: an Oversimplified View. Journal of Virology, 89(19): 9719–9726. doi: 10.1128/JVI.00780-15
Silva, A. K. F.; Santos, C. D. G.; Nascimento, A. K. Q. 2010. Transmissão de begomovírus de plantas daninhas para tomateiros pela mosca-branca. Planta Daninha, 28(3): 507–514. doi: 10.1590/S0100-83582010000300007
Singh, G.; Singh, R. 2016. Review Article Distribution of Aphis Spiraecola Patch 1914. International Journal of Recent Advances in Multidisciplinary Research, 3(12): 2100-2111.
Siomi, H.; Siomi, M. C. 2009. On the road to reading the RNA-interference code. Nature, 457: 396–404. doi: 10.1038/nature07754
Srinivasan, R.; Alvarez, J. M.; Eigenbrode, S. D.; Bosque-pérez, N. A. 2009. Influence of Hairy Nightshade Solanum sarrachoides (Sendtner) and Potato leafroll virus (Luteoviridae: Polerovirus ) on the Host Preference of Myzus persicae (Sulzer) (Homoptera: Aphididae) . Environmental Entomology, 35(2): 546–553. doi: 10.1603/0046-225X-35.2.546
Stansly, P. A.; Naranjo, S. E. 2010. Bemisia: Bionomics and Management of a Global Pest. New York, Springer. doi: 10.1007/978-90-481-2460-2
Stewart, L. R.; Medina, V.; Tian, T.; Turina, M.; Falk, B. W.; Ng, J. C. 2010.A Mutation in the Lettuce Infectious Yellows Virus Minor Coat Protein Disrupts Whitefly Transmission but Not In Planta Systemic Movement. Journal of Virology, 84(23): 12165-12173. doi: 10.1128/JVI.01192-10
Syller, J. 2006. The roles and mechanisms of helper component proteins encoded by potyviruses and caulimoviruses. Physiological and Molecular Plant Pathology, 67(3): 119–130, 2006. doi: 10.1016/j.pmpp.2005.12.005
Wang, L. L.; Wei, X. M.; Ye, X. D.; Xu, H. X.; Zhou, X. P.; Liu, S. S.; Wang, X. W. 2014.Expression and functional characterisation of a soluble form of Tomato yellow leaf curl virus coat protein. Pest Management Science, 70(10): 1624-1631. doi: 10.1002/ps.3750
Whitfield, A. E.; Falk, B. W.; Rotenberg, D. 2015. Insect vector-mediated transmission of plant viruses. Virology, 479–480: 278–289. doi: 10.1016/j.virol.2015.03.026
Yu, X. D.; Liu, Z. C.; Huang, S. L.; Chen, Z. Q.; Sun, Y. W.; Duan, P. F.; Ma, Y. Z.; Xia, L. Q. 2016. RNAi-mediated plant protection against aphids. Pest Management Science, 72(6): 1090-1098. doi: 10.1002/ps.4258
Zabala, M. de T.; Littlejohn, G.; Jayaraman, S.; Studholme, D.; Bailey, T.; Lawson, T.; Tillich, M.; Licht, D.; Bölter, B.; Delfino, L. 2015. Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nature Plants, 1(6): 15074. doi: 10.1038/NPLANTS.2015.74
Zhang, T.; Luan, J. B.; Qi, J. F.; Huang, C. J.; Li, M.; Zhou, X. P.; Liu, S. S. 2012.Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Molecular Ecology, 21(5): 1294-1304. doi: 10.1111/j.1365-294X.2012.05457.x
Zhao, J.; Zhang, X.; Hong, Y.; Liu, Y. 2016.Chloroplast in plant-virus interaction. Frontiers in Microbiology, 7: 1565. doi: 10.3389/fmicb.2016.01565
Zuñiga, E.; Guttierez, P. A.2002 Inverno com pulgões. Revista Cultivar, 2002.
Downloads
Published
Issue
Section
License
Authors who publish in this journal agree to the following terms:
The Copyright for articles published in this journal follow authorship. The articles are open access, with their own attributions, in educational and non-commercial applications.
The journal reserves the right to make regulatory, orthographic and grammatical changes in the originals, with the aim of maintaining the standard language and the credibility of the vehicle. It will respect, however, the writing style of the authors.
Changes, corrections or suggestions of conceptual order will be forwarded to the authors, when necessary. In such cases, the articles, once appropriate, should be submitted for further consideration.
The opinions issued by the authors of the articles are their sole responsibility.