Virus Resistance in Potato Cultivars: A Review on The Use of Pathogen-Derived Resistance Strategies as a Tool

Abstract

Potato has always been a subject of extensive research owing to its importance as a food crop; being used as staple in many localities. Among various pathogens, viruses provide a continuous threat to potato. Pathogen-derived resistance (PDR) has mainly been employed to engineer potato to confer resistance against viruses. Many different strategies of pathogen-derived resistance have been utilized including protein-mediated resistance, and nucleic acid-mediated resistance (DNA/RNA) involving transcriptional and post-transcriptional gene silencing. This review provides an insight into the past, discusses situation at present, and gives important suggestions for future implications of these strategies for the improvement of this crop.

Keywords

• Pathogen-derived resistance,potato,protein-mediated resistance,nucleic acid-mediated resistance

Patates Kültürlerinde Virüs Dirençliliği: Patojen Köken Viral Dirençlilik Üzerine Strateji Belirlemesi

Öz

Patates önemli bir gıda ürünü olmasından ötürü daima pek çok bölgede geniş araştırma konularına sahiptir. Çeşitli patojenler arasında virüsler patateste devamlı bir tehdit unsurudur. Virüslere karşı dirençliliği arttırmamıza yönelik Patojen türevli direnç (PTD) uygulaması yapılmaktadır. Pek çok PTD üretim stratejisi kullanılmaktadır. Bunlar arasında transkripsiyonal ve post transkripsiyonal gen susturuculu protein ilişkili direnç, nukleotid ilişkili direnç (DNA/RNA) gelmektedir. Bu derleme patates bitkisinde, konunun tartışılmasında geçmiş ve geleceğe ilişkin yaklaşımlara ışık tutmaktadır.

Anahtar Kelimeler

• Patojen türevli direnç,patates,protein ilişkili direnç,nükleotid ilişkili direnç

References

1. Ali A., Hassan S and Asad A., 2002. Incidence of six potato viruses in spring, summer and autumn potato crops of the North West Frontier Province of Pakistan. Australasian Plant Pathology, 31: 143-146.
2. Allison RF., Schneider WL and Greene AE., 1996. Recombination in plants expressing viral transgenes. Seminars in Virology, 7: 417-422.
3. Arif M., Thomas PE., Crosslin JM and Brown CR., 2009a. Agrobacterium-mediated transformation of potato using PLRV-REP and PVY-CP genes and assessment of replicase-mediated resistance against natural infection of PLRV. Pakistan Journal of Botany, 41(3): 1477-1488.
4. Arif M., Thomas PE., Crosslin JM and Brown CR., 2009b. Development of molecular resistance in potato against potato leafroll virus and potato virus Y through Agrobacterium-mediated double transgenesis. Pakistan Journal of Botany, 41(2): 945-954.
5. Arif M., Azhar U., Arshad M., Zafar Y., Mansoor S and Asad S., 2012. Engineering broad-spectrum resistance against RNA viruses in potato. Transgenic Research, 21: 303-311.
6. Bai Y., Guo Z., Wang X., Bai D and Zhang W., 2009. Generation of double-virus-resistant marker-free transgenic potato plants. Progress in Natural Science, 19: 543-548.
7. Barker H., Reavy B., Kumar A., Webster KD and Mayo MA., 1992. Restricted virus multiplication in potatoes transformed with the coat protein gene of potato leafroll luteovirus: similarities with a type of host gene-mediated resistance. Annals of Applied Biology, 120: 55-64.
8. Bartel DP., 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116: 281-297.

9. Baulcombe DC., 1996. Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell, 8: 1833-1844.
10. Beachy RN., 1997. Mechanisms and applications of pathogen-derived resistance in transgenic plants. Current Opinions in Biotechnology, 8: 215-220.
11. Beachy RN., 1999. Coat protein-mediated resistance to tobacco mosaic virus: discovery mechanisms and exploitation. Philosophical Transactions of Royal Society London, 354: 659-664.
12. Bostan H and Haliloglu K., 2004. Distribution of PLRV, PVS, PVX and PVY (PVYN, PVYO and PVYC) in the seed potato tubers in Turkey. Pakistan Journal of Biological Sciences 7: 1140-1143.
13. Bucher E., Lohuis D., Van Poppel PMJA., Geerts-Dimitriadou C., Goldbach R and Prins M., 2006. Multiple virus resistance at a high frequency using a single transgene construct. Journal of General Virology, 87: 3697-3701.
14. Carr JP., Marsh JE., Lomonossoff GP., Sekiya ME and Zaitlin M., 1992. Resistance to TMV induced by the 54 kDa gene sequences requires expression of the 54 kDa protein. Molecular Plant-Microbe Interactions, 5: 397-404.
15. Cheong EJ., Mock R and Li RH., 2012. Elimination of five viruses from sugarcane using in vitro culture of axillary buds and apical meristems. Plant Cell Tissue Organ Culture, 109: 439-445.
16. Chung BN., Yoon J and Palukaitis P., 2013. Engineered resistance in potato against potato leafroll virus, potato virus A and potato virus Y. Virus Genes, 47: 86-92.
17. de Haan P., Gielen JJL., Prins M., Wijkamp IG., van Schepen A., Peters D., Van Grinsven MQJM and Goldbach R., 1992. Characterization of RNA-mediated resistance to tomato spotted wilt virus in transgenic tobacco plants. Biotechnology, 10: 1133-1137.
18. Denli AM and Hannon GJ., 2003. RNAi: an ever-growing puzzle. Trends in Biochemical Sciences, 28: 196-201.
19. Doreste V., Ramos EL., Enrfquez GA., Rodrfguez R., Peral R and Pujol M., 2002. Transgenic potato plants expressing the potato virus X (PVX) coat protein gene developed resistance to the viral infection. Phytoparasitica, 30(2): 177-185.
20. Ehrenfeld N., Romano E., Serrano C and Arce-Johnson P., 2004. Replicase-mediated resistance against potato leafroll virus in potato Desiree plants. Biological Research, 37: 71-82.
21. Faccioli G., 2001. Control of potato viruses using meristem culture and stem-cutting cultures, thermotherapy and chemotherapy. p. 365-390. Virus and Virus-Like Diseases of Potatoes and Production of Seed-Potatoes (Eds. G. Loebenstein, PH. Berger, A Brunt and RH Lawson), Kluwer. Dordrecht.
22. FAO 2011. FAOSTAT: Production-Crops, 2010 data. Food and Agriculture Organization of the United Nations.
23. Fuchs M and Gonsalves D., 1995. Resistance of transgenic hybrid squash ZW-20 expressing the coat protein genes of zucchini yellow mosaic virus and watermelon mosaic virus 2 to mixed infections by both potyviruses. Nature Biotechnology, 13: 1466-1473.
24. Fuchs M., McFerson JR., Tricoli DM., McMaster JR., Deng RZ., Boeshore ML., Reynolds JF., Russell PF., Quemada HD and Gonsalves D., 1997. Cantaloupe line CZW-30 containing coat protein gene of cucumber mosaic virus, zucchini yellow virus and water melon mosaic virus 2 is resistant to these three viruses in the field. Molecular Breeding, 3: 279-290.
25. Golemboski DB., Lomonossoff GP and Zaitlin M., 1990. Plants transformed with a tobacco mosaic virus non-structural gene sequence are resistant to the virus. Proceedings of the National Academy of Sciences of the United States of America, 87: 6311-6315.
26. Gong XQ and Liu JH., 2012. Genetic transformation and genes for resistance to abiotic and biotic stresses in citrus and its related genera. Plant Cell Tissue Organ Culture, 113(2): 137-147.
27. Hassairi A., Masmoudi K., Albouy J., Robaglia C., Jullien M and Ellouz R., 1998. Transformation of two potato cultivars 'Spunta' and 'Clauster' (Solanum tuberosum) with lettuce mosaic coat protein gene and heterologous immunity to potato virus Y. Plant Science, 136: 31-42.
28. Hefferon KL., Khalilian H and AbouHaidar MG., 1997. Expression of the PVYO coat protein (CP) under the control of the PVX CP gene leader sequence: protection under greenhouse and field conditions against PVYO and PVYN infection in three potato cultivars. Theoretical and Applied Genetics, 94: 287-292.
29. Hoekema A., Huisman MJ., Molendijk L., van den Elzen PJM and Cornelissen BJC., 1989. The genetic engineering of two commercial potato cultivars for resistance to potato virus X. Nature Biotechnology, 7: 273-278.
30. Hossain M., Ali MS and Rashid MM., 1994. Effect of inoculum levels of potato virus Y (PVY) on yield and subsequent spread of the disease under insecticide spray and unsprayed condition. Bangladesh Journal of Botany, 23: 87.
31. Huimin Xu., Houri K., Mohamed E., Sam S and Mounir G., 1995. Genetically engineered resistance to potato virus X in four commercial potato cultivars. Plant Cell Reports, 15: 91-96.
32. Hutvagner G and Zamore PD., 2002. RNAi: nature abhors a double-strand. Potato Biology and Biotechnology: Advances and Perspectives (Ed. D. Vreugdenhil), Elsevier, pp. 225-232.
33. Jayasinghe U and Salazar LF., 1998. Present status of controlling potato leafroll virus. Plant Virus Disease Control. (Eds. A Hadidi, RK Khetarpal and H Koganezawa), Minnesota Press, pp. 584-592.
34. Jeffries C., Barker H and Khurana SMP., 2005. Potato viruses (and viroids) and their management. Potato Production, Improvement and Post-Harvest Management. The Haworth’s Food Products Press, New York.
35. Kamachi S., Mochizaki A., Nishiguch M and Tabei Y., 2007. Transgenic Nicotiana benthamiana plants resistant to cucumber green mottle mosaic virus based on RNA silencing. Plant Cell Reports, 26: 1283-1288.
36. Kaniewski W., Lawson C., Sammons B., Haley L., Hart J and Delannay X., 1990. Field resistance of transgenic Russet Burbank potato to effects of infection by potato virus X and potato virus Y. Biotechnology, 8: 750-754.
37. Kawchuk LM., Lyncha DR., Martinb RR., Kozuba GC and Farriesa B., 1997. Field resistance to potato leafroll luteovirus in transgenic and somaclone potato plants reduces tuber disease symptoms. Canadian Journal of Plant Pathology, 19(3): 260-266.
38. Kawchuk LM., Martin RR and McPherson J., 1990. Resistance in transgenic potato expressing the potato leafroll virus coat protein gene. Molecular Plant-Microbe Interactions, 3(5): 301-307.
39. Kawchuk LM., Martin RR and McPherson., 1991. Sense and antisense RNA-mediated resistance to potato leafroll virus in Russet Burbank potato plants. Molecular Plant-Microbe Interactions, 4(3): 247-253.
40. Kojima M and Lapierre H., 1988. Potato leafroll virus (PLRV). European Handbook of Plant Diseases (Eds. IM Smith, DH Phillips, RA Lelliot and SA Archer), Blackwell Scientific Publications, pp. 23-24.
41. Lawson C., Kaniewski W., Haley L., Rozman R., Newell C and Sanders P., 1990. Engineering resistance to mixed virus infection in a commercial potato cultivar: resistance to potato virus X and potato virus Y in transgenic Russet Burbank. Biotechnology, 8: 127-134.
42. Lawson EC., Weiss JD., Thomas PE and Kaniewski WK., 2001. NewLeaf Plus® Russet Burbank potatoes: replicase-mediated resistance to potato leafroll virus. Molecular Breeding, 7(1): 1-12.
43. Loebenstein G., Berger PH., Brunt A and Lawson R., 2001. Virus and virus-like diseases of potatoes and production of seed-potatoes. Kluwer, Dordrecht.
44. MacFarlane SA and Davies JW., 1992. Plants transformed with a region of the 201KDa replicase gene from pea early browning virus RNA1 are resistant to virus infection. Procedings of National Academy of Scientists of the United States of America, 89: 5829-5833.
45. MacKenzie DJ., Tremaine JH and Mcpherson J., 1991. Genetically engineered resistance to potato virus S in potato cultivar Russet Burbank. Molecular Plant-Microbe Interactions, 4(1): 95-102.
46. MacKenzie DJ., Tremaine JH and Stace-Smith R., 1989. Organization and interviral homologies of the 3'-terminal portion of potato virus S RNA. Journal of General Virology, 70: 1053-1063.
47. Maki-Valkama T., Valkonen JPT., Lehtinen A and Pehu E., 2001. Protection against potato virus Y (PVY) in the field in potatoes transformed with the PVY P1 gene. American Journal of Potato Research, 78: 209-214.
48. Maki-Valkama T., Valkonen JPT., Kreuze JF and Pehu E., 2000. Transgenic resistance to PVY associated with post-transcriptional silencing of P1 transgene is overcome by PVY N strains that carry highly homologous P1 sequences and recover transgene expression at infection. Molecular Plant-Microbe Interactions, 13(4): 366-373.
49. Malnoe P., Farinelli L., Collet GF and Reust W., 1994. Small-scale field tests with transgenic potato, cv. Bintje, to test resistance to primary and secondary infections with potato virus Y. Plant Molecular Biology, 25(6): 963-975.
50. Missiou A., Kalantidis K., Boutla A., Tzortzakaki S., Tabler M and Tsagris M., 2004. Generation of transgenic potato plants highly resistant to potato virus Y (PVY) through RNA silencing. Molecular Breeding, 14: 185-197.
51. Monci F., Sanchez-Campos S., Navas-Castillo J and Moriones E., 2002. A natural recombinant between the Gemini-viruses tomato yellow leaf curl Sardinia virus and tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virololgy Journal, 303: 317-326.
52. Murray SL., Thompson G., Visser A and Berger DK., 2002. Transgenic potatoes (cv. Late Harvest) show increased tolerance to potato leafroll virus in greenhouse and field trials. South African Journal of Science, 98.
53. Nelson R., Mc Cormick SM., Delannay X., Dube P and Layton J., 1988. Virus tolerance, plant growth and field performance of transgenic tomato plants expressing the coat protein from tobacco mosaic virus. Biotechnology, 6: 403-409.
54. Nicola-Negri E., Brunetti A., Tavazza M and Ilardi V., 2005. Hairpin RNA-mediated silencing of plum pox virus P1 and HC-pro genes for efficient and predictable resistance to the virus. Transgenic Research, 14: 989-994.
55. Niu QW., Lin SS., Reyes JL., Chen KC., Wu HW., Yeh SD and Chua NH., 2006. Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nature Biotechnology, 24: 1420-148.
56. Novy RG., Gillen AM and Whitworth JL., 2007. Characterization of the expression and inheritance of potato leaf roll virus (PLRV) and potato virus Y (PVY) resistance in three generations of germplasm derived from Solanum tuberosum. Theoretical and Applied Genetics, 114: 1161-1172.
57. Okamoto D., Nielsen SVS., Albrechtsen M and Borkhardt B., 1996. General resistance against potato virus Y introduced into a commercial potato cultivar by genetic transformation with PVYN coat protein gene. Potato Research, 39(2): 271-282.
58. Pehu TM., Maki-Valkama TK., Valkonen JPT., Koivu KT and Lehto KM., 1995. Potato plants transformed with a potato virus Y P1 gene sequence are resistant to PVYO. American Journal of Potato Research, 72: 523-532.
59. Powell PA., Stark DM., Sanders PR and Beachy RN., 1989. Protection against tobacco mosaic virus in transgenic plants that express tobacco mosaic virus antisense RNA. Proceedings of National Academy of Sciences, 86: 6949-6952.
60. Powell-Abel P., Nelson RS., Hoffmann NDB., Rogers SG., Fraley RT and Beachy RN., 1986. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science, 232: 738-743.
61. Presting GG., Smith OP and Brown CR., 1995. Resistance to potato leafroll virus in potato plants transformed with a coat protein gene or with vector control constructs. Phytopathology, 85(4).
62. Prins M., Laimer M., Noris E., Schubert J., Wassenegger M and Tepfer M., 2008. Strategies for antiviral resistance in transgenic plants. Molecular Plant Pathology, 9(1): 73-83.
63. Prins M., de Haan P., Luyten R., van Veller M., van Grinsven MQJM and Goldbach R., 1995. Molecular Plant-Microbe Interactions, 8: 85-91.
64. Raben A., Tagliabue A., Christensen NJ., Madsen J., Holst JJ and Astrup A., 1994. Resistant starch: the effect on postprandial glycemia, hormonal response, and satiety. American Journal of Clinical Nutrition, 60: 544-551.
65. Racman DS.,Mcgeachy K., Reavy B., Strukelj B., Zel J and Barker H., 2001. Strong resistance to potato tuber necrotic ringspot disease in potato induced by transformation with coat protein gene sequences from an NTN isolate of Potato virus Y. Annals of Applied Biology, 139(2): 269-275.
66. Rahman MS and Akandaw AM., 2009. Performance of seed potato produced from sprout cutting, stem cutting and conventional tubers against PVY and PLRV. Bangladesh Journal of Agricultural Research, 34: 609-622.
67. Ratcliff F., Harrison BD and Baulcombe DC., 1997. A similarity between viral defense and gene silencing in plants. Science, 276: 1558-1560.
68. Romano E., Ferreira AT., Dusi AN., Proite K., Buso JA., Avila AC., Nishijima ML., Nascimento AS., Bravo-Almonacid F., Mentaberry A., Monte D., Campos MA., Melo PE., Cattony MK and Torres AC., 2001. Extreme resistance to two Brazilian strains of Potato virus Y (PVY) in transgenic potato, cv. Achat, expressing the PVYO coat protein. Horticultura Brasileira, 19(2): 118-122.
69. Roux L., Simon AE and Holland JJ., 1991. Effects of defective interfering viruses on virus replication and pathogenesis. Advances in Virus Research, 40: 181-210.
70. Rovere CV., Asurmendi S and Hopp HE., 2001. Transgenic resistance in potato plants expressing potato leaf roll virus (PLRV) replicase gene sequences is RNA-mediated and suggests the involvement of post-transcriptional gene silencing. Archives of Virology, 146: 1337-1353.
71. Rubio T., Borja M., Scholthof HB and Jackson AO., 1999. Recombination with host transgenes and effects on virus evolution: An overview and opinion. Molecular Plant-Microbe Interactions, 12: 87-92.
72. Salazar L., 2003. Potato viruses after the XX century effects, dissemination and their control.
73. Schubert J., Matousek J and Mattern D., 2004. Pathogen-derived resistance in potato to Potato virus Y-aspects of stability and biosafety under field conditions. Virus Research, 100: 41-50.
74. Sijen T., Wellenk J., Hendriks J., Verner J and van Kammen A., 1995. Replication of cowpea mosaic virus RNA1 or RNA2 is specifically blocked in transgenic Nicotiana benthamiana plants expressing the full-length replicase or movement protein genes. Molecular Plant-Microbe Interactions, 8: 340-347.
75. Simon-Mateo C and Garcia JA., 2011. Antiviral strategies in plants based on RNA silencing. Biochimica et Biophysica Acta, 1809: 722-731.
76. Smith NA., Singh SP., Wang MB., Stoutjesdijk PA., Green AG and Waterhouse PM., 2000. Gene expression: total silencing by intron-spliced hairpin RNAs. Nature, 407: 319-320.
77. Spillane C., Baulcombe DC and Kavanagh TA., 1998. Genetic engineering of the potato cultivar Glenroe for increased resistance to potato virus X (PVX). Irish Journal of Agricultural and Food Research, 37: 173-182.
78. Stashevskia Z and Il’inskayab ON., 2011. Virus resistance of transgenic potato plants (Solanum tuberosum L.) bearing PVYNTN CP gene of potato virus Y coat protein. Russian Journal of Genetics, 1(2): 103-111.
79. Suszkin J., 2008. Aphid pest gets "egged". Agricultural Research, 56(5): 19.
80. Szittya G., Silhavy D., Molnar A., Havelda Z., Lovas A., Lakatos L., Banfalvi Z and Burgyan J., 2003. Low temperature inhibits RNA silencing-mediated defense by the control of siRNA generation. EMBO Journal, 22: 633-640.
81. Tanzer MM., Thompson WF., Law MD., Wernsman EA and Uknes S., 1997. Characterization of post-transcriptionally suppressed transgene expression that confers resistance to TEV infection in tobacco. Plant Cell, 9: 1411-1423.
82. Tepfer M., 1993. Viral genes and transgenic plants. Biotechnology, 11: 1125-1132.
83. Thomas PE., Lawson EC., Zalewski JC., Reed GL and Kaniewski WK., 2000. Extreme resistance to potato leafroll virus in potato cv. Russet Burbank mediated by the viral replicase gene. Virus Research, 71: 49-62.
84. Thomas PE., Kaniewski WK and Lawson EC., 1997. Reduced field spread of potato leafroll virus in transgenic potatoes expressing the potato leafroll virus coat protein gene. Plant Disease, 81(12): 1447-1453.
85. Tijsterman M., Ketting RF and Plasterk RH., 2002. The genetics of RNA silencing. Annual Review of Genetics, 36: 489-519.
86. Tricoli DM., Carney KJ., Russell PF., McMaster JR., Groff DW., Hadden KC., Himmel PT., Hubbard JP., Boeshore ML and Quemada HD., 1995. Field evaluation of transgenic squash containing single or multiple virus coat protein gene constructs for resistance to cucumber mosaic virus, watermelon mosaic virus 2, and zucchini yellow mosaic virus. Nature Biotechnology, 13: 1458-1465.
87. Valkonen JPT., 2007. Viruses: economical losses and biotechnological potential. p. 619-641.
88. vander Wilk F., Willink DP., Huisman MJ., Huttinga H and Goldbach R., 1991. Expression of the potato leafroll luteovirus coat protein gene in transgenic potato plants inhibits viral infection. Plant Molecular Biology, 17(3): 431-439.
89. Vaucheret H and Fagard M., 2001. Transcriptional gene silencing in plants: targets, inducers and regulators. Trends in Genetics, 17: 29-35.
90. Wang B., Ma YL., Zhang ZB., Wu ZM., Wu WF., Wang QC and Li MF., 2011. Potato viruses in China. Crop Protection, 30: 1117-1123.
91. Wang MB., Abbott DC and Waterhouse PM., 2000. A single copy of a virus-derived transgene encoding hairpin RNA gives immunity to barley yellow dwarf virus. Molecular Plant Pathology, 1: 347-356.
92. Wang-Pruski G and Schofield A., 2012. Potato: improving crop productivity and abiotic stress tolerance, improving crop resistance to abiotic stress. Wiley-VCH Verlag GmbH and Co. K Ga A.
93. Waterhouse PM and Helliwell CA., 2003. Exploring plant genomes by RNA-induced gene silencing. Nature Reviews Genetics, 4: 29-38.
94. Xu H., Khalilian H., Eweida M., Squire S and Abou Haidar MG., 1995. Genetically engineered resistance to potato virus X in four commercial cultivars. Plant Cell Reports, 15: 91-96.
95. Zhang HL., Peng XX., Song YR., Li TR., Meng Q., Li C and Cui XJ., 1997. Resistance to mixed PVY and PLRV infection in potato cultivars expressing dual PVY and PLRV coat protein genes. Acta Botanica Sinica, 39(3): 236-240.
96. Zhang ZY., Wang YG., Shen XJ., Li L., Zhou SF., Li WC and Fu FL., 2013. RNA interference-mediated resistance to maize dwarf mosaic virus. Plant Cell Tissue Organ Culture, 113: 571-578.