Exploiting the combination of natural and genetically engineered resistance to cassava mosaic and cassava brown streak viruses impacting cassava production in Africa.
Vanderschuren, Hervé; Moreno, Isabel; Anjanappa, Ravi B.et al.
Africa South of the Sahara; Agrobacterium/genetics; Begomovirus/pathogenicity/physiology; Genetic Engineering; Inverted Repeat Sequences/genetics; Manihot/genetics/immunology/virology; Plant Diseases/genetics/immunology/virology; Plant Immunity/genetics; Plants, Genetically Modified; Potyviridae/pathogenicity/physiology; RNA, Small Interfering/genetics/metabolism; RNA, Viral/genetics; Sequence Analysis, DNA; Transformation, Genetic; Viral Proteins/chemistry/genetics
Abstract :
[en] Cassava brown streak disease (CBSD) and cassava mosaic disease (CMD) are currently two major viral diseases that severely reduce cassava production in large areas of Sub-Saharan Africa. Natural resistance has so far only been reported for CMD in cassava. CBSD is caused by two virus species, Cassava brown streak virus (CBSV) and Ugandan cassava brown streak virus (UCBSV). A sequence of the CBSV coat protein (CP) highly conserved between the two virus species was used to demonstrate that a CBSV-CP hairpin construct sufficed to generate immunity against both viral species in the cassava model cultivar (cv. 60444). Most of the transgenic lines showed high levels of resistance under increasing viral loads using a stringent top-grafting method of inoculation. No viral replication was observed in the resistant transgenic lines and they remained free of typical CBSD root symptoms 7 month post-infection. To generate transgenic cassava lines combining resistance to both CBSD and CMD the hairpin construct was transferred to a CMD-resistant farmer-preferred Nigerian landrace TME 7 (Oko-Iyawo). An adapted protocol allowed the efficient Agrobacterium-based transformation of TME 7 and the regeneration of transgenic lines with high levels of CBSV-CP hairpin-derived small RNAs. All transgenic TME 7 lines were immune to both CBSV and UCBSV infections. Further evaluation of the transgenic TME 7 lines revealed that CBSD resistance was maintained when plants were co-inoculated with East African cassava mosaic virus (EACMV), a geminivirus causing CMD. The innovative combination of natural and engineered virus resistance in farmer-preferred landraces will be particularly important to reducing the increasing impact of cassava viral diseases in Africa.
Exploiting the combination of natural and genetically engineered resistance to cassava mosaic and cassava brown streak viruses impacting cassava production in Africa.
Publication date :
2012
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, United States - California
Mbanzibwa DR, Tian Y, Mukasa SB, Valkonen JP, (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: 6934-6940.
Winter S, Koerbler M, Stein B, Pietruszka A, Paape M, et al. (2010) Analysis of cassava brown streak viruses reveals the presence of distinct virus species causing cassava brown streak disease in East Africa. Journal of General Virology 91: 1365-1372.
Patil BL, Fauquet CM, (2009) Cassava mosaic geminiviruses: actual knowledge and perspectives. Mol Plant Pathol 10: 685-701.
Legg JP, Jeremiah SC, Obiero HM, Maruthi MN, Ndyetabula I, et al. (2011) Comparing the regional epidemiology of the cassava mosaic and cassava brown streak virus pandemics in Africa. Virus Research 159: 161-170.
Alicai T, Omongo CA, Maruthi MN, Hillocks RJ, Baguma Y, et al. (2007) Re-emergence of cassava brown streak disease in Uganda. Plant Disease 91: 24-29.
Ogwok E, Patil BL, Alicai T, Fauquet CM, (2010) Transmission studies with Cassava brown streak Uganda virus (Potyviridae: Ipomovirus) and its interaction with abiotic and biotic factors in Nicotiana benthamiana. Journal of Virological Methods 169: 296-304.
Legg JP, Owor B, Sseruwagi P, Ndunguru J, (2006) Cassava mosaic virus disease in East and central Africa: epidemiology and management of a regional pandemic. Adv Virus Res 67: 355-418.
Fregene M, Bernal A, Duque M, Dixon A, Tohme J, (2000) AFLP analysis of African cassava (Manihot esculenta Crantz) germplasm resistant to the cassava mosaic disease (CMD). Theoretical and Applied Genetics 100: 678-685.
Legg JP, Thresh JM, (2000) Cassava mosaic virus disease in East Africa: a dynamic disease in a changing environment. Virus Res 71: 135-149.
Akano O, Dixon O, Mba C, Barrera E, Fregene M, (2002) Genetic mapping of a dominant gene conferring resistance to cassava mosaic disease. Theor Appl Genet 105: 521-525.
Okogbenin E, Porto MCM, Egesi C, Mba C, Espinosa E, 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 Science 47: 1895-1904.
Ding SW, Voinnet O, (2007) Antiviral immunity directed by small RNAs. Cell 130: 413-426.
Vanderschuren H, Akbergenov R, Pooggin MM, Hohn T, Gruissem W, et al. (2007) Transgenic cassava resistance to African cassava mosaic virus is enhanced by viral DNA-A bidirectional promoter-derived siRNAs. Plant Mol Biol 64: 549-557.
Vanderschuren H, Alder A, Zhang P, Gruissem W, (2009) Dose-dependent RNAi-mediated geminivirus resistance in the tropical root crop cassava. Plant Mol Biol 70: 265-272.
Yadav JS, Ogwok E, Wagaba H, Patil BL, Bagewadi B, et al. (2011) RNAi-mediated resistance to Cassava brown streak Uganda virus in transgenic cassava. Molecular Plant Pathology 12: 677-687.
Collinge DB, Jorgensen HJ, Lund OS, Lyngkjaer MF, (2010) Engineering pathogen resistance in crop plants: current trends and future prospects. Annu Rev Phytopathol 48: 269-291.
Bucher E, Lohuis D, van Poppel PM, Geerts-Dimitriadou C, Goldbach R, et al. (2006) Multiple virus resistance at a high frequency using a single transgene construct. J Gen Virol 87: 3697-3701.
Mbanzibwa DR, Tian YP, Tugume AK, Patil BL, Yadav JS, et al. (2011) Evolution of cassava brown streak disease-associated viruses. The Journal of general virology 92: 974-987.
Raji A, Ladeinde O, Dixon A, (2008) Screening landraces for additional sources of field resistance to cassava mosaic disease and green mite for integration into the cassava improvement program. Journal of integrative plant biology 50: 311-318.
Bull SE, Owiti JA, Niklaus M, Beeching JR, Gruissem W, et al. (2009) Agrobacterium-mediated transformation of friable embryogenic calli and regeneration of transgenic cassava. Nature Protocols 4: 1845-1854.
Zainuddin I, Schlegel K, Gruissem W, Vanderschuren H, (2012) Robust transformation procedure for the production of transgenic farmer-preferred cassava landraces. Plant methods 8: 24.
Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, et al. (1994) Fast Folding and Comparison of Rna Secondary Structures. Monatshefte Fur Chemie 125: 167-188.
Akbergenov R, Si-Ammour A, Blevins T, Amin I, Kutter C, et al. (2006) Molecular characterization of geminivirus-derived small RNAs in different plant species. Nucleic Acids Res 34: 462-471.
Moreno I, Gruissem W, Vanderschuren H, (2011) Reference genes for reliable potyvirus quantitation in cassava and analysis of Cassava brown streak virus load in host varieties. Journal of Virological Methods 177: 49-54.
Mbanzibwa DR, Tian YP, Tugume AK, Mukasa SB, Tairo F, 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: 353-359.
Patil BL, Ogwok E, Wagaba H, Mohammed IU, Yadav JS, et al. (2011) RNAi-mediated resistance to diverse isolates belonging to two virus species involved in Cassava brown streak disease. Molecular Plant Pathology 12: 31-41.
Liu J, Zheng Q, Ma Q, Gadidasu KK, Zhang P, (2011) Cassava genetic transformation and its application in breeding. Journal of integrative plant biology 53: 552-569.
Mbanzibwa DR, Tian YP, Tugume AK, Mukasa SB, Tairo F, et al. (2011) Simultaneous virus-specific detection of the two cassava brown streak-associated viruses by RT-PCR reveals wide distribution in East Africa, mixed infections, and infections in Manihot glaziovii. J Virol Methods 171: 394-400.
Sayre R, Beeching JR, Cahoon EB, Egesi C, Fauquet C, et al. (2011) The BioCassava plus program: biofortification of cassava for sub-Saharan Africa. Annual Review of Plant Biology 62: 251-272.
Niklaus M, Gruissem W, Vanderschuren H, (2011) Efficient transformation and regeneration of transgenic cassava using the neomycin phosphotransferase gene as aminoglycoside resistance marker gene. GM crops 2: 193-200.
Zainuddin I, Schlegel K, Gruissem W, Vanderschuren H (2012) Robust transformation procedure for the production of transgenic farmer-preferred cassava landraces. Plant Methods (in press).
Syller J, (2012) Facilitative and antagonistic interactions between plant viruses in mixed infections. Molecular Plant Pathology 13: 204-216.
Voinnet O, Pinto YM, Baulcombe DC, (1999) Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A 96: 14147-14152.
Vanitharani R, Chellappan P, Pita JS, Fauquet CM, (2004) Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J Virol 78: 9487-9498.
Trinks D, Rajeswaran R, Shivaprasad PV, Akbergenov R, Oakeley EJ, et al. (2005) Suppression of RNA Silencing by a Geminivirus Nuclear Protein, AC2, Correlates with Transactivation of Host Genes. J Virol 79: 2517-2527.
Lokko Y, Danquah EY, Offei SK, Dixon AGO, Gedil MA, (2005) Molecular markers associated with a new source of resistance to the cassava mosaic disease. African Journal of Biotechnology 4: 873-881.
Zhou X, Liu Y, Calvert L, Munoz C, Otim-Nape GW, 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 (Pt 8): 2101-2111.
Fargette D, Konate G, Fauquet C, Muller E, Peterschmitt M, et al. (2006) Molecular ecology and emergence of tropical plant viruses. Annual Review of Phytopathology 44: 235-260.
Mansoor S, Zafar Y, Briddon RW, (2006) Geminivirus disease complexes: the threat is spreading. Trends Plant Sci 11: 209-212.
Strange RN, Scott PR, (2005) Plant disease: A threat to global food security. Annual Review of Phytopathology 43: 83-116.
Gonsalves D, (1998) Control of papaya ringspot virus in papaya: a case study. Annu Rev Phytopathol 36: 415-437.
Azevedo J, Garcia D, Pontier D, Ohnesorge S, Yu A, et al. (2010) Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev 24: 904-915.
Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW, et al. (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. The EMBO journal 17: 6739-6746.
Simon-Mateo C, Garcia JA, (2011) Antiviral strategies in plants based on RNA silencing. Biochimica et Biophysica Acta 1809: 722-731.
Di Nicola-Negri E, Tavazza M, Salandri L, Ilardi V, (2010) Silencing of Plum pox virus 5'UTR/P1 sequence confers resistance to a wide range of PPV strains. Plant Cell Reports 29: 1435-1444.
Leibman D, Wolf D, Saharan V, Zelcer A, Arazi T, et al. (2011) A high level of transgenic viral small RNA is associated with broad potyvirus resistance in cucurbits. Molecular plant-microbe interactions: MPMI 24: 1220-1238.
Senthil-Kumar M, Hema R, Anand A, Kang L, Udayakumar M, et al. (2007) A systematic study to determine the extent of gene silencing in Nicotiana benthamiana and other Solanaceae species when heterologous gene sequences are used for virus-induced gene silencing. The New phytologist 176: 782-791.
Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, et al. (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. The Plant cell 24: 859-874.
Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, et al. (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8: 517-527.
Bonnet E, He Y, Billiau K, Van de Peer Y, (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26: 1566-1568.
