Cassava is the fourth largest source of calories in the world but is subject to economically important yield losses due to viral diseases, including cassava brown streak disease and cassava mosaic disease. Cassava mosaic disease occurs in sub-Saharan Africa and the Asian subcontinent and is associated with nine begomovirus species, whereas cassava brown streak disease has to date been reported only in sub-Saharan Africa and is caused by two distinct ipomovirus species. We present an overview of key milestones and their significance in the understanding and characterization of these two major diseases as well as their associated viruses and whitefly vector. New biotechnologies offer a wide range of opportunities to reduce virus-associated yield losses in cassava for farmers and can additionally enable the exploitation of this valuable crop for industrial purposes. This review explores established and new technologies for genetic manipulation to achieve desired traits such as virus resistance.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Olsen KM, Schaal BA. 1.  1999. Evidence on the origin of cassava: phylogeography of Manihot esculenta. PNAS 96:5586–91 [Google Scholar]
  2. Hillocks RJ. 2.  2002. Cassava in Africa. Cassava: Biology, Production and Utilization RJ Hillocks, JM Thresh, AC Bellotti 41–54 New York: CABI Publ. [Google Scholar]
  3. 3. Food Agric. Org. (FAO). 2013. Save and Grow: Cassava. A Guide to Sustainable Production Intensification Rome: FAO [Google Scholar]
  4. 4. Food Agric. Org. (FAO). 2015. FAOSTAT Rome: FAO http://www.fao.org/faostat/ [Google Scholar]
  5. Baguma Y, Nuwamanya E, Rey C. 5.  2016. The African perspective: developing an African bio-resource based industry: the case for cassava. Creating Sustainable Bioeconomies: The Bioscience Revolution in Europe and Africa I Virgin, EJ Morris 115–27 London: Routledge [Google Scholar]
  6. Legg JP, Jeremiah SC, Obiero HM, Maruthi MN, Ndyetabula I. 6.  et al. 2011. Comparing the regional epidemiology of the cassava mosaic and cassava brown streak virus pandemics in Africa. Virus Res 159:161–70 [Google Scholar]
  7. Legg JP, Kumar PL, Makeshkumar T, Tripathi L, Ferguson M. 7.  et al. 2015. Cassava virus diseases: biology, epidemiology, and management. Adv. Virus Res. 91:85–142 [Google Scholar]
  8. Patil BL, Fauquet CM. 8.  2009. Cassava mosaic geminiviruses: actual knowledge and perspectives. Mol. Plant Pathol. 10:685–701 [Google Scholar]
  9. Mohammed IU, Abarshi MM, Muli B, Hillocks RJ, Maruthi MN. 9.  2012. The symptom and genetic diversity of cassava brown streak viruses infecting cassava in East Africa. Adv. Virol 2012:795697 [Google Scholar]
  10. Ogwok E, Patil BL, Alicai T, Fauquet CM. 10.  2010. Transmission studies with Cassava brown streak Uganda virus (Potyviridae: Ipomovirus) and its interaction with abiotic and biotic factors in Nicotiana benthamiana. J. Virol. Methods 169:296–304 [Google Scholar]
  11. Winter S, Koerbler M, Stein B, Pietruszka A, Paape M, Butgereitt A. 11.  2010. Analysis of cassava brown streak viruses reveals the presence of distinct virus species causing cassava brown streak disease in East Africa. J. Gen. Virol. 91:1365–72 [Google Scholar]
  12. Fargette D, Thresh JM, Otim-Nape GW. 12.  1994. The epidemiology of African cassava mosaic geminivirus: reversion and the concept of equilibrium. Trop. Sci. 34:123–33 [Google Scholar]
  13. Dubern J. 13.  1994. Transmission of African cassava mosaic geminivirus by the whitefly (Bemisia tabaci). Trop. Sci. 34:82–91 [Google Scholar]
  14. Maruthi MN, Hillocks RJ, Mtunda K, Raya MD, Muhanna M. 14.  et al. 2005. Transmission of Cassava brown streak virus by Bemisia tabaci (Gennadius). J. Phytopathol 153:307–12 [Google Scholar]
  15. Storey HH, Nichols RFW. 15.  1938. Studies of the mosaic diseases of cassava. Ann. Appl. Biol. 25:790–806 [Google Scholar]
  16. Wagaba H, Beyene G, Trembley C, Alicai T, Fauquet CM, Taylor NJ. 16.  2013. Efficient transmission of cassava brown streak disease viral pathogens by chip bud grafting. BMC Res. Notes 6:516 [Google Scholar]
  17. Moreno I, Gruissem W, Vanderschuren H. 17.  2011. Reference genes for reliable potyvirus quantitation in cassava and analysis of Cassava brown streak virus load in host varieties. J. Virol. Methods 177:49–54 [Google Scholar]
  18. Legg J. 18.  2010. Epidemiology of a whitefly-transmitted cassava mosaic geminivirus pandemic in Africa. Bemisia: Bionomics and Management of a Global Pest PA Stansly, SE Naranjo 233–57 Dordrecht, Neth.: Springer [Google Scholar]
  19. Scholthof KBG, Adkins S, Czosnek H, Palukaitis P, Jacquot E. 19.  et al. 2011. Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 12:938–54 [Google Scholar]
  20. Warburg O. 20.  1894. Die Kulturpflanzen Usambaras Berlin: E.S. Mittler & Sohn [Google Scholar]
  21. Fauquet C, Fargette D. 21.  1990. African cassava mosaic-virus—etiology, epidemiology, and control. Plant Disease 74:404–11 [Google Scholar]
  22. Fargette D, Konaté G, Fauquet C, Muller E, Peterschmitt M, Thresh JM. 22.  2006. Molecular ecology and emergence of tropical plant viruses. Annu. Rev. Phytopathol. 44:235–60 [Google Scholar]
  23. Abraham A. 23.  1956. Tapioca cultivation in India Farm Bull. 17 Indian Counc. Agric. Res. New Delhi, India: [Google Scholar]
  24. Malathi VG, Nair NG, Shantha P. 24.  1985. Cassava Mosaic Disease Trivandrum, India: Cent. Tuber Crops Res. Inst. [Google Scholar]
  25. Bock KR, Guthrie EJ, Figueiredo G. 25.  1981. A strain of cassava latent virus occurring in coastal districts of Kenya. Ann. Appl. Biol. 99:151–59 [Google Scholar]
  26. Bock KR, Woods RD. 26.  1983. Etiology of African cassava mosaic disease. Plant Disease 67:994–95 [Google Scholar]
  27. Stanley J, Gay MR. 27.  1983. Nucleotide sequence of cassava latent virus DNA. Nature 301:260–62 [Google Scholar]
  28. Jeske H. 28.  2009. Geminiviruses. TT Viruses—The Still Elusive Human Pathogens EM de Villiers, H zur Hausen 185–226 Berlin: Springer [Google Scholar]
  29. Fondong VN. 29.  2013. Geminivirus protein structure and function. Mol. Plant Pathol. 14:635–49 [Google Scholar]
  30. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. 30.  2013. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat. Rev. Microbiol. 11:777–88 [Google Scholar]
  31. Li F, Xu X, Huang C, Gu Z, Cao L. 31.  et al. 2015. The AC5 protein encoded by Mungbean yellow mosaic India virus is a pathogenicity determinant that suppresses RNA silencing-based antiviral defenses. New Phytol 208:555–69 [Google Scholar]
  32. Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D. 32.  1999. Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit. Rev. Plant Sci. 18:71–106 [Google Scholar]
  33. Brown JK, Zerbini FM, Navas-Castillo J, Moriones E, Ramos-Sobrinho R. 33.  et al. 2015. Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Arch. Virol. 160:1593–619 [Google Scholar]
  34. Rey ME, Ndunguru J, Berrie LC, Paximadis M, Berry S. 34.  et al. 2012. Diversity of dicotyledenous-infecting geminiviruses and their associated DNA molecules in southern Africa, including the south-west Indian Ocean islands. Viruses 4:1753–91 [Google Scholar]
  35. Bull SE, Briddon RW, Sserubombwe WS, Ngugi K, Markham PG, Stanley J. 35.  2006. Genetic diversity and phylogeography of cassava mosaic viruses in Kenya. J. Gen. Virol. 87:3053–65 [Google Scholar]
  36. Zhou XP, Liu YL, Robinson DJ, Harrison BD. 36.  1998. Four DNA-A variants among Pakistani isolates of cotton leaf curl virus and their affinities to DNA-A of geminivirus isolates from okra. J. Gen. Virol. 79:915–23 [Google Scholar]
  37. Harimalala M, Lefeuvre P, De Bruyn A, Tiendrebeogo F, Hoareau M. 37.  et al. 2012. A novel cassava-infecting begomovirus from Madagascar: cassava mosaic Madagascar virus. Arch. Virol. 157:2027–30 [Google Scholar]
  38. Berrie LC, Rybicki EP, Rey ME. 38.  2001. Complete nucleotide sequence and host range of South African cassava mosaic virus: further evidence for recombination amongst begomoviruses. J. Gen. Virol. 82:53–58 [Google Scholar]
  39. Zhou XP, Liu YL, Calvert L, Munoz C, Otim-Nape GW. 39.  et al. 1997. Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J. Gen. Virol. 78:2101–11 [Google Scholar]
  40. Fondong VN, Pita JS, Rey ME, de Kochko A, Beachy RN, Fauquet CM. 40.  2000. Evidence of synergism between African cassava mosaic virus and a new double-recombinant geminivirus infecting cassava in Cameroon. J. Gen. Virol. 81:287–97 [Google Scholar]
  41. Tiendrebeogo F, Lefeuvre P, Hoareau M, Harimalala MA, De Bruyn A. 41.  et al. 2012. Evolution of African cassava mosaic virus by recombination between bipartite and monopartite begomoviruses. Virol. J. 9:67 [Google Scholar]
  42. Monde G, Walangululu J, Winter S, Bragard C. 42.  2010. Dual infection by cassava begomoviruses in two leguminous species (Fabaceae) in Yangambi, Northeastern Democratic Republic of Congo. Arch. Virol. 155:1865–69 [Google Scholar]
  43. Austin MND. 43.  1986. Scientists identify cassava viruses. Asian Agribus 3:10 [Google Scholar]
  44. Saunders K, Salim N, Mali VR, Malathi VG, Briddon R. 44.  et al. 2002. Characterisation of Sri Lankan cassava mosaic virus and Indian cassava mosaic virus: evidence for acquisition of a DNA B component by a monopartite begomovirus. Virology 293:63–74 [Google Scholar]
  45. Jose A, Makeshkumar T, Edison S. 45.  2011. Survey of cassava mosaic disease in Kerala. J. Root Crops 37:41–47 [Google Scholar]
  46. Wang HL, Cui XY, Wang XW, Liu SS, Zhang ZH, Zhou XP. 46.  2016. First report of Sri Lankan cassava mosaic virus infecting cassava in Cambodia. Plant Dis 100:1029 [Google Scholar]
  47. Kashina BD, Alegbejo MD, Banwo OO, Nielsen SL, Nicolaisen M. 47.  2013. Molecular identification of a new begomovirus associated with mosaic disease of Jatropha curcas L. in Nigeria. Arch. Virol. 158:511–14 [Google Scholar]
  48. Snehi SK, Srivastava A, Raj SK. 48.  2012. Biological characterization and complete genome sequence of a possible strain of Indian cassava mosaic virus from Jatropha curcas in India. J. Phytopathol 160:547–53 [Google Scholar]
  49. Wang G, Sun YW, Xu RR, Qu J, Tee C. 49.  et al. 2014. DNA-A of a highly pathogenic Indian cassava mosaic virus isolated from Jatropha curcas causes symptoms in Nicotiana benthamiana. Virus Genes 48:402–5 [Google Scholar]
  50. Ndunguru J, Legg J, Aveling T, Thompson G, Fauquet C. 50.  2005. Molecular biodiversity of cassava begomoviruses in Tanzania: evolution of cassava geminiviruses in Africa and evidence for East Africa being a center of diversity of cassava geminiviruses. Virol. J. 2:21 [Google Scholar]
  51. Sseruwagi P, Maruthi MN, Colvin J, Rey MEC, Brown JK, Legg JP. 51.  2006. Colonization of non-cassava plant species by cassava whiteflies (Bemisia tabaci) in Uganda. Entomol. Exp. Appl. 119:145–53 [Google Scholar]
  52. Lefeuvre P, Martin DP, Hoareau M, Naze F, Delatte H. 52.  et al. 2007. Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. J. Gen. Virol. 88:3458–68 [Google Scholar]
  53. Legg JP. 53.  1996. Host-associated strains within Ugandan populations of the whitefly Bemisia tabaci (Genn.), (Hom., Aleyrodidae). J. Appl. Entomol. 120:523–27 [Google Scholar]
  54. Berry SD, Fondong VN, Rey C, Rogan D, Fauquet CM, Brown JK. 54.  2004. Molecular evidence for five distinct Bemisia tabaci (Homoptera: Aleyrodidae) geographic haplotypes associated with cassava plants in sub-Saharan Africa. Ann. Entomol. Soc. Am. 97:852–59 [Google Scholar]
  55. Esterhuizen LL, Mabasa KG, van Heerden SW, Czosnek H, Brown JK. 55.  et al. 2012. Genetic identification of members of the Bemisia tabaci cryptic species complex from South Africa reveals native and introduced haplotypes. J. Appl. Entomol. 137:122–35 [Google Scholar]
  56. Stanley J, Townsend R. 56.  1985. Characterisation of DNA forms associated with cassava latent virus infection. Nucleic Acids Res 13:2189–206 [Google Scholar]
  57. Ndunguru J, Legg JP, Fofana IBF, Aveling TAS, Thompson G, Fauquet CM. 57.  2006. Identification of a defective molecule derived from DNA-A of the bipartite begomovirus of East African cassava mosaic virus. Plant Pathol. 55:2–10 [Google Scholar]
  58. Frischmuth T, Stanley J. 58.  1991. African cassava mosaic virus DI DNA interferes with the replication of both genomic components. Virology 183:539–44 [Google Scholar]
  59. Ndunguru J, De Leon L, Doyle CD, Sseruwagi P, Plata G. 59.  et al. 2016. Two novel DNAs that enhance symptoms and overcome CMD2 resistance to cassava mosaic disease. J. Virol. 90:4160–73 [Google Scholar]
  60. Maredza AT, Allie F, Plata G, Rey ME. 60.  2016. Sequences enhancing cassava mosaic disease symptoms occur in the cassava genome and are associated with South African cassava mosaic virus infection. Mol. Genet. Genom. 291:1467–85 [Google Scholar]
  61. Liu SS, Colvin J, De Barro PJ. 61.  2012. Species concepts as applied to the whitefly Bemisia tabaci systematics: How many species are there?. J. Integr. Agric. 11:176–86 [Google Scholar]
  62. Dinsdale A, Cook L, Riginos C, Buckley YM, De Barro P. 62.  2010. Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann. Entomol. Soc. Am. 103:196–208 [Google Scholar]
  63. Maruthi MN, Colvin J, Seal S, Gibson G, Cooper J. 63.  2002. Co-adaptation between cassava mosaic geminiviruses and their local vector populations. Virus Res 86:71–85 [Google Scholar]
  64. Abdullahi I, Winter S, Atiri GI, Thottappilly G. 64.  2003. Molecular characterization of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae) populations infesting cassava. Bull. Entomol. Res. 93:97–106 [Google Scholar]
  65. Gnankiné O, Mouton L, Henri H, Terraz G, Houndété T. 65.  et al. 2012. Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv. Divers. 6:411–21 [Google Scholar]
  66. Legg JP, French R, Rogan D, Okao-Okuja G, Brown JK. 66.  2002. A distinct Bemisia tabaci (Gennadius) (Hemiptera: Sternorrhyncha: Aleyrodidae) genotype cluster is associated with the epidemic of severe cassava mosaic virus disease in Uganda. Mol. Ecol. 11:1219–29 [Google Scholar]
  67. Legg JP, Shirima R, Tajebe LS, Guastella D, Boniface S. 67.  et al. 2014. Biology and management of Bemisia whitefly vectors of cassava virus pandemics in Africa. Pest Manag. Sci. 70:1446–53 [Google Scholar]
  68. Storey HH. 68.  1936. Virus diseases of East African plants. VI. A progress report on studies of the disease of cassava. East Afr. Agric. J. 2:34–39 [Google Scholar]
  69. Nichols RFW. 69.  1950. The brown streak disease of cassava: distribution climatic effects and diagnostic symptoms. East Afr. Agric. J. 15:154–60 [Google Scholar]
  70. Alicai T, Omongo CA, Maruthi MN, Hillocks RJ, Baguma Y. 70.  et al. 2007. Re-emergence of cassava brown streak disease in Uganda. Plant Dis 91:24–29 [Google Scholar]
  71. Storey HH. 71.  1939. Report of the plant pathologist. East Afr. Agric. Res. Station Rep 1939:9 [Google Scholar]
  72. Lister RM. 72.  1959. Mechanical transmission of cassava brown streak virus. Nature 183:1588–89 [Google Scholar]
  73. Monger WA, Seal S, Isaac AM, Foster GD. 73.  2001. Molecular characterization of the Cassava brown streak virus coat protein. Plant Pathol 50:527–34 [Google Scholar]
  74. Mbanzibwa DR, Tian Y, Mukasa SB, Valkonen JP. 74.  2009. Cassava brown streak virus (Potyviridae) encodes a putative Maf/HAM1 pyrophosphatase implicated in reduction of mutations and a P1 proteinase that suppresses RNA silencing but contains no HC-Pro. J. Virol 83:6934–40 [Google Scholar]
  75. Mbanzibwa DR, Tian YP, Tugume AK, Mukasa SB, Tairo F. 75.  et al. 2009. Genetically distinct strains of Cassava brown streak virus in the Lake Victoria basin and the Indian Ocean coastal area of East Africa. Arch. Virol. 154:353–59 [Google Scholar]
  76. Dombrovsky A, Reingold V, Antignus Y. 76.  2014. Ipomovirus—an atypical genus in the family Potyviridae transmitted by whiteflies. Pest Manag. Sci. 70:1553–67 [Google Scholar]
  77. Chung BY, Miller WA, Atkins JF, Firth AE. 77.  2008. An overlapping essential gene in the Potyviridae. PNAS 105:5897–902 [Google Scholar]
  78. Legg JP, Raya MD. 78.  1998. Survey of cassava virus diseases in Tanzania. Int. J. Pest Manag. 44:17–23 [Google Scholar]
  79. Hillocks RJ, Kibani THM. 79.  2002. Factors affecting the distribution, incidence and spread of fusarium wilt of cotton in Tanzania. Exp. Agric. 38:13–27 [Google Scholar]
  80. Jeremiah SC, Ndyetabula IL, Mkamilo GS, Haji S, Muhanna MM. 80.  et al. 2015. The dynamics and environmental influence on interactions between cassava brown streak disease and the whitefly, Bemisia tabaci. Phytopathology 105:646–55 [Google Scholar]
  81. Mauck KE, De Moraes CM, Mescher MC. 81.  2010. Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. PNAS 107:3600–5 [Google Scholar]
  82. Wu D, Qi T, Li WX, Tian H, Gao H. 82.  et al. 2017. Viral effector protein manipulates host hormone signaling to attract insect vectors. Cell Res 27:402–15 [Google Scholar]
  83. Szittya G, Silhavy D, Molnar A, Havelda Z, Lovas A. 83.  et al. 2003. Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22:633–40 [Google Scholar]
  84. Ghoshal B, Sanfacon H. 84.  2014. Temperature-dependent symptom recovery in Nicotiana benthamiana plants infected with tomato ringspot virus is associated with reduced translation of viral RNA2 and requires ARGONAUTE 1. Virology 456:188–97 [Google Scholar]
  85. Hillocks RJ, Jennings DL. 85.  2003. Cassava brown streak disease: a review of present knowledge and research needs. Int. J. Pest Manag. 49:225–34 [Google Scholar]
  86. Mbanzibwa DR, Tian YP, Tugume AK, Patil BL, Yadav JS. 86.  et al. 2011. Evolution of cassava brown streak disease-associated viruses. J. Gen. Virol. 92:974–87 [Google Scholar]
  87. Ndunguru J, Sseruwagi P, Tairo F, Stomeo F, Maina S. 87.  et al. 2015. Analyses of twelve new whole genome sequences of cassava brown streak viruses and Ugandan cassava brown streak viruses from East Africa: diversity, supercomputing and evidence for further speciation. PLOS ONE 10:e0139321 [Google Scholar]
  88. Alicai T, Ndunguru J, Sseruwagi P, Tairo F, Okao-Okuja G. 88.  et al. 2016. Cassava brown streak virus has a rapidly evolving genome: implications for virus speciation, variability, diagnosis and host resistance. Sci. Rep. 6:36164 [Google Scholar]
  89. Massart S, Candresse T, Gil J, Lacomme C, Predajna L. 89.  et al. 2017. A framework for the evaluation of biosecurity, commercial, regulatory, and scientific impacts of plant viruses and viroids identified by NGS technologies. Front. Microbiol. 8:45 [Google Scholar]
  90. Fregene M, Morante N, Sánchez T, Marin J, Ospina C. 90.  et al. 2006. Molecular markers for introgression of useful traits from wild Manihot relatives of cassava, marker-assisted selection (MAS) of disease and root quality traits. J. Root Crops 32:1–31 [Google Scholar]
  91. Akano O, Dixon O, Mba C, Barrera E, Fregene M. 91.  2002. Genetic mapping of a dominant gene conferring resistance to cassava mosaic disease. Theor. Appl. Genet. 105:521–25 [Google Scholar]
  92. Okogbenin E, Porto MCM, Egesi C, Mba C, Espinosa E. 92.  et al. 2007. Marker-assisted introgression of resistance to cassava mosaic disease into Latin American germplasm for the genetic improvement of cassava in Africa. Crop. Sci. 47:1895–904 [Google Scholar]
  93. Rabbi IY, Hamblin MT, Kumar PL, Gedil MA, Ikpan AS. 93.  et al. 2014. High-resolution mapping of resistance to cassava mosaic geminiviruses in cassava using genotyping-by-sequencing and its implications for breeding. Virus Res 186:87–96 [Google Scholar]
  94. Fregene M, Angel F, Gomez R, Rodriguez F, Chavarriaga P. 94.  et al. 1997. A molecular genetic map of cassava (Manihot esculenta Crantz). Theor. Appl. Genet. 95:431–41 [Google Scholar]
  95. Okogbenin E, Egesi CN, Olasanmi B, Ogundapo O, Kahya S. 95.  et al. 2012. Molecular marker analysis and validation of resistance to cassava mosaic disease in elite cassava genotypes in Nigeria. Crop. Sci. 52:2576–86 [Google Scholar]
  96. Wolfe MD, Rabbi IY, Egesi C, Hamblin M, Kawuki R. 96.  et al. 2016. Genome-wide association and prediction reveals genetic architecture of cassava mosaic disease resistance and prospects for rapid genetic improvement. Plant Genome 9:1–13 [Google Scholar]
  97. Prochnik S, Marri PR, Desany B, Rabinowicz PD, Kodira C. 97.  et al. 2012. The cassava genome: current progress, future directions. Trop. Plant Biol. 5:88–94 [Google Scholar]
  98. Bredeson JV, Lyons JB, Prochnik SE, Wu GA, Ha CM. 98.  et al. 2016. Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat. Biotechnol. 34:562–70 [Google Scholar]
  99. Louis B, Rey C. 99.  2015. Resistance gene analogs involved in tolerant cassava-geminivirus interaction that shows a recovery phenotype. Virus Genes 51:393–407 [Google Scholar]
  100. Soto JC, Ortiz JF, Perlaza-Jimenez L, Vasquez AX, Lopez-Lavalle LAB. 100.  et al. 2015. A genetic map of cassava (Manihot esculenta Crantz) with integrated physical mapping of immunity-related genes. BMC Genom 16:190 [Google Scholar]
  101. Allie F, Pierce EJ, Okoniewski MJ, Rey C. 101.  2014. Transcriptional analysis of South African cassava mosaic virus-infected susceptible and tolerant landraces of cassava highlights differences in resistance, basal defense and cell wall associated genes during infection. BMC Genom 15:1006 [Google Scholar]
  102. Lozano R, Hamblin MT, Prochnik S, Jannink JL. 102.  2015. Identification and distribution of the NBS-LRR gene family in the cassava genome. BMC Genom 16:360 [Google Scholar]
  103. Maruthi MN, Bouvaine S, Tufan HA, Mohammed IU, Hillocks RJ. 103.  2014. Transcriptional response of virus-infected cassava and identification of putative sources of resistance for cassava brown streak disease. PLOS ONE 9:e96642 [Google Scholar]
  104. Chisholm ST, Parra MA, Anderberg RJ, Carrington JC. 104.  2001. Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of tobacco etch virus. Plant Physiol 127:1667–75 [Google Scholar]
  105. Leal LG, Perez A, Quintero A, Bayona A, Ortiz JF. 105.  et al. 2013. Identification of immunity-related genes in Arabidopsis and cassava using genomic data. Genom. Proteom. Bioinform. 11:345–53 [Google Scholar]
  106. Kourelis J, van der Hoorn RAL, Sueldo DJ. 106.  2016. Decoy engineering: the next step in resistance breeding. Trends Plant Sci 21:371–73 [Google Scholar]
  107. Maule AJ, Caranta C, Boulton MI. 107.  2007. Sources of natural resistance to plant viruses: status and prospects. Mol. Plant Pathol. 8:223–31 [Google Scholar]
  108. Bastet A, Robaglia C, Gallois JL. 108.  2017. eIF4E resistance: Natural variation should guide gene editing. Trends Plant Sci 22:411–19 [Google Scholar]
  109. Hou H, Atlihan N, Lu ZX. 109.  2014. New biotechnology enhances the application of cisgenesis in plant breeding. Front. Plant Sci. 5:389 [Google Scholar]
  110. Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V. 110.  2013. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9:39 [Google Scholar]
  111. Bogdanove AJ, Schornack S, Lahaye T. 111.  2010. TAL effectors: finding plant genes for disease and defense. Curr. Opin. Plant Biol. 13:394–401 [Google Scholar]
  112. Schornack S, Moscou MJ, Ward ER, Horvath DM. 112.  2013. Engineering plant disease resistance based on TAL effectors. Annu. Rev. Phytopathol. 51:383–406 [Google Scholar]
  113. Rogans SJ, Allie F, Tirant JE, Rey ME. 113.  2016. Small RNA and methylation responses in susceptible and tolerant landraces of cassava infected with South African cassava mosaic virus. Virus Res 225:10–22 [Google Scholar]
  114. Ogwok E, Ilyas M, Alicai T, Rey ME, Taylor NJ. 114.  2016. Comparative analysis of virus-derived small RNAs within cassava (Manihot esculenta Crantz) infected with cassava brown streak viruses. Virus Res 215:1–11 [Google Scholar]
  115. Vanderschuren H, Lentz E, Zainuddin I, Gruissem W. 115.  2013. Proteomics of model and crop plant species: status, current limitations and strategic advances for crop improvement. J. Proteom. 93:5–19 [Google Scholar]
  116. Windram O, Penfold CA, Denby KJ. 116.  2014. Network modeling to understand plant immunity. Annu. Rev. Phytopathol. 52:93–111 [Google Scholar]
  117. Duan CG, Wang CH, Guo HS. 117.  2012. Application of RNA silencing to plant disease resistance. Silence 3:5 [Google Scholar]
  118. Zhang P, Vanderschuren H, Futterer J, Gruissem W. 118.  2005. Resistance to cassava mosaic disease in transgenic cassava expressing antisense RNAs targeting virus replication genes. Plant Biotechnol. J. 3:385–97 [Google Scholar]
  119. Vanderschuren H, Akbergenov R, Pooggin MM, Hohn T, Gruissem W, Zhang P. 119.  2007. Transgenic cassava resistance to African cassava mosaic virus is enhanced by viral DNA-A bidirectional promoter-derived siRNAs. Plant Mol. Biol. 64:549–57 [Google Scholar]
  120. Vanderschuren H, Alder A, Zhang P, Gruissem W. 120.  2009. Dose-dependent RNAi-mediated geminivirus resistance in the tropical root crop cassava. Plant Mol. Biol. 70:265–72 [Google Scholar]
  121. Raja P, Sanville BC, Buchmann RC, Bisaro DM. 121.  2008. Viral genome methylation as an epigenetic defense against geminiviruses. J. Virol. 82:8997–9007 [Google Scholar]
  122. Yadav JS, Ogwok E, Wagaba H, Patil BL, Bagewadi B. 122.  et al. 2011. RNAi-mediated resistance to Cassava brown streak Uganda virus in transgenic cassava. Mol. Plant Pathol. 12:677–87 [Google Scholar]
  123. Vanderschuren H, Moreno I, Anjanappa RB, Zainuddin IM, Gruissem W. 123.  2012. Exploiting the combination of natural and genetically engineered resistance to cassava mosaic and cassava brown streak viruses impacting cassava production in Africa. PLOS ONE 7:9 [Google Scholar]
  124. Wagaba H, Beyene G, Aleu J, Odipio J, Okao-Okuja G. 124.  et al. 2016. Field level RNAi-mediated resistance to cassava brown streak disease across multiple cropping cycles and diverse East African agro-ecological locations. Front. Plant Sci. 7:2060 [Google Scholar]
  125. Duffy S, Shackelton LA, Holmes EC. 125.  2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9:267–76 [Google Scholar]
  126. Schopke C, Taylor N, Carcamo R, Konan NK, Marmey P. 126.  et al. 1996. Regeneration of transgenic cassava plants (Manihot esculenta Crantz) from microbombarded embryogenic suspension cultures. Nat. Biotechnol. 14:731–35 [Google Scholar]
  127. Li HQ, Sautter C, Potrykus I, Puonti-Kaerlas J. 127.  1996. Genetic transformation of cassava (Manihot esculenta Crantz). Nat. Biotechnol. 14:736–40 [Google Scholar]
  128. Bull SE, Owiti JA, Niklaus M, Beeching JR, Gruissem W, Vanderschuren H. 128.  2009. Agrobacterium-mediated transformation of friable embryogenic calli and regeneration of transgenic cassava. Nat. Protoc. 4:1845–54 [Google Scholar]
  129. Chavarriaga-Aguirre P, Brand A, Medina A, Prias M, Escobar R. 129.  et al. 2016. The potential of using biotechnology to improve cassava: a review. In Vitro Cell. Dev. Biol. Plant 52:461–78 [Google Scholar]
  130. Liu J, Zheng Q, Ma Q, Gadidasu KK, Zhang P. 130.  2011. Cassava genetic transformation and its application in breeding. J. Integr. Plant Biol. 53:552–69 [Google Scholar]
  131. Zainuddin I, Schlegel K, Gruissem W, Vanderschuren H. 131.  2012. Robust transformation procedure for the production of transgenic farmer-preferred cassava landraces. Plant Methods 8:24 [Google Scholar]
  132. Chauhan RD, Beyene G, Kalyaeva M, Fauquet CM, Taylor N. 132.  2015. Improvements in Agrobacterium-mediated transformation of cassava (Manihot esculenta Crantz) for large-scale production of transgenic plants. Plant Cell Tissue Organ Cult 121:591–603 [Google Scholar]
  133. Nyaboga E, Njiru J, Nguu E, Gruissem W, Vanderschuren H, Tripathi L. 133.  2013. Unlocking the potential of tropical root crop biotechnology in east Africa by establishing a genetic transformation platform for local farmer-preferred cassava cultivars. Front. Plant Sci. 4:526 [Google Scholar]
  134. Chetty CC, Rossin CB, Gruissem W, Vanderschuren H, Rey ME. 134.  2013. Empowering biotechnology in southern Africa: establishment of a robust transformation platform for the production of transgenic industry-preferred cassava. New Biotechnol 30:136–43 [Google Scholar]
  135. Vanderschuren H. 135.  2012. Strengthening African R&D through effective transfer of tropical crop biotech to African institutions. Nat. Biotechnol. 30:1170–72 [Google Scholar]
  136. Ma QX, Zhou WZ, Zhang P. 136.  2015. Transition from somatic embryo to friable embryogenic callus in cassava: dynamic changes in cellular structure, physiological status, and gene expression profiles. Front. Plant Sci. 6:824 [Google Scholar]
  137. Kitimu SR, Taylor J, March TJ, Tairo F, Wilkinson MJ, Rodriguez Lopez CM. 137.  2015. Meristem micropropagation of cassava (Manihot esculenta) evokes genome-wide changes in DNA methylation. Front. Plant Sci. 6:590 [Google Scholar]
  138. Horowitz AR, Antignus Y, Gerling D. 138.  2011. Management of Bemisiatabaci whiteflies. Interaction with Geminivirus-Infected Host Plants: Bemisia tabaci, Host Plants and Geminiviruses WMO Thompson 293–322 Dordrecht, Neth.: Springer [Google Scholar]
  139. Shukla AK, Upadhyay SK, Mishra M, Saurabh S, Singh R. 139.  et al. 2016. Expression of an insecticidal fern protein in cotton protects against whitefly. Nat. Biotechnol. 34:1046–51 [Google Scholar]
  140. Mascarin GM, Kobori NN, Quintela ED, Delalibera I. 140.  2013. The virulence of entomopathogenic fungi against Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) and their conidial production using solid substrate fermentation. Biol. Control 66:209–18 [Google Scholar]
  141. Price DRG, Gatehouse JA. 141.  2008. RNAi-mediated crop protection against insects. Trends Biotechnol 26:393–400 [Google Scholar]
  142. Raza A, Malik HJ, Shafiq M, Amin I, Scheffler JA. 142.  et al. 2016. RNA interference based approach to down regulate osmoregulators of whitefly (Bemisia tabaci): potential technology for the control of whitefly. PLOS ONE 11:e0153883 [Google Scholar]
  143. Joga MR, Zotti MJ, Smagghe G, Christiaens O. 143.  2016. RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Front. Physiol. 7:553 [Google Scholar]
  144. Malik HJ, Raza A, Amin I, Scheffler JA, Scheffler BE. 144.  et al. 2016. RNAi-mediated mortality of the whitefly through transgenic expression of double-stranded RNA homologous to acetylcholinesterase and ecdysone receptor in tobacco plants. Sci. Rep. 6:38469 [Google Scholar]
  145. Omongo CA, Kawuki R, Bellotti AC, Alicai T, Baguma Y. 145.  et al. 2012. African cassava whitefly, Bemisia tabaci, resistance in African and South American cassava genotypes. J. Integr. Agric. 11:327–36 [Google Scholar]
  146. Anjanappa RB, Mehta D, Maruthi MN, Kanju E, Gruissem W. Vanderschuren H.145.  2016. Characterization of brown streak virus-resistant cassava. Mol. Plant-Microbe Interact. 29:527–34 [Google Scholar]
  147. Anjanappa RB, Mehta D, Okoniewski MJ, Szabelska A, Gruissem W, Vanderschuren H. 147.  2017. Molecular insights into cassava brown streak virus susceptibility and resistance by profiling of the early host response. Mol. Plant Pathol. In press [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error