Modernization in plant breeding approaches for improving biotic stress resistance in crop plants

Biotic stresses are a potential threat to global food security. The origin of new pathogens and insect races due to climatic andgenetic factors is a major challenge for plant breeders in breeding biotic stress resistant crops. Yield losses due to biotic stresses haveresulted in 800 million people underfed in the world. Reduced yield due to biotic stresses and increasing food demand put internationalfood security at risk as 70% more food will be required in 2050. This review describes and compares the conventional and moleculargenetics methods being used for breeding biotic stress resistant crops. In the past, classical breeding approaches like introduction,hybridization, composite crossing, multiline, and backcross breeding were utilized for this purpose. However, these methods wereslow, expensive, and hectic for developing resistance in crops. Furthermore, breakdown of resistance due to fast evolving pathogenscould not be coped with using these time consuming methods. Therefore, molecular genetics approaches like mutation, marker assistedselection (MAS), genomics, recombinant DNA technology, targeted induced local lesions in genome (TILLING), and virus inducedgene silencing (VIGS) were adapted by breeders to develop effective resistance in crop plants in a shorter time. TILLING, being anontransgenic method, is expected to become the most powerful tool for this purpose.

Anahtar Kelimeler:

Gene pyramiding, MAS, QTLs, TILLING, transgenic, VIGS

Modernization in plant breeding approaches for improving biotic stress resistance in crop plants

Keywords:

Gene pyramiding, MAS, QTLs, TILLING, transgenic, VIGS,

PDF

___

Ali SA, Gunupuru LR, Kumar GBS, Khan M, Scofield S, Nicholson P, Doohan FM (2014). Plant disease resistance is augmented in uzu barley lines modified in the brassinosteroid receptor BRI 1. BMC Plant Biol 14: 227.
Alonso JM, Joseph R (2006). Moving forward in reverse genetic technologies to enable genome-wide phenomic screens in Arabidopsis. Nat Rev Genet, doi:10.1038/nrg1893.
Aragao FJ, Faria JC (2009). First transgenic Gemini virus resistant plant in the field. Nat Biotechnol 27: 1086–1088.
Arens P, Mansilla C, Deinum D, Cavellini L, Moretti A, Rolland S, van der Schoot H, Calvache D, Ponz F, Collonnier C et al. (2010). Development and evaluation of robust molecular markers linked to disease resistance in tomato for distinctness, uniformity and stability testing. Theor Appl Genet 120: 655– 664.
Ashizawa T, Zenbayashi K, Koizumi S (2001). Development of a simulation model for forecasting rice blast epidemics in multiline. Japanese J Phytopathol 67: 194–197.
Ayliffe MA, Steinau M, Park RF, Rooke L, Pacheco MG, Hulbert SH (2004). Aberrant mRNA processing of the maize Rp1-D rust resistance gene in wheat and barley. Mol Plant Microbe Interact 17: 853–864.
Bakhetia M, Charlton W, Atkinson HJ, McPherson MJ (2005). RNA interference of dual oxidase in the plant nematode Meloidogyne incognita. Mol. Plant Microbe Interact 18: 1099–1106.
Beclin C, Boutet S, Waterhouse P, Vaucheret H (2002). A branched pathway for transgene-induced RNA silencing in plants. Curr Biol 12: 684–688.
Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, Zhu J (2004). The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc Nat Acad Sci 101: 886–890.
Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363–366.
Brahim KM, Barrett JA (1991). Evolution of mildew resistance in a hybrid bulk population of barley. Heredity 67: 247–256.
Browning JA, Frey KJ (1969). Multiline cultivars as a means of disease control. Annu Rev Phytopathol 7: 355–382.
Brunner S, Stirnweis D, Quijano CD, Buesing G, Herren G, Parlange F, Barret P, Tassy C, Sautter C, Winzeler M et al. (2012). Transgenic Pm3 multilines of wheat show increased powdery mildew resistance in the field. Plant Biotechnol J 10: 398–409.
Butron A, Widstrom NW (2001). Mass selection for agronomic performance and resistance to ear-feeding insects in three corn population. Madica 46: 207–212.
Cakir C, Tor M (2010). Factors influencing barley stripe mosaic virus-mediated gene silencing in wheat. Physiol Mol Plant Pathol 74: 246–253.
Carstens M, McCrindle TK, Adams N, Diener A, Guzha DT (2014). Increased resistance to biotrophic pathogens in the Arabidopsis constitutive induced resistance 1 mutant is EDS1 and PAD4- dependent and modulated by environmental temperature.
PLoS ONE 9: e109853. doi:10.1371/journal.pone. 0109853. Chen SK, Togashi T, Miki D, Aoyama M, Wong HL, Kawasaki T, Shimamoto K (2010). Analysis of the Rac/Rop small GTPase family in rice. Expression, subcellular localization and role in disease resistance. Plant Cell Physiol 51: 585–595.
Chern MS, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC (2005). Over-expression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant-Microbe Interact 18: 511–520.
Christou P, Twyman RM (2004). The potential of genetically enhanced plants to address food insecurity. Nut Res Rev 17: 23–42.
Chu CG, Friesen TL, Xu SS, Faris JD (2008). Identification of novel tan spot resistance loci beyond the known host-selective toxin insensitivity genes in wheat. Theor Appl Genet 117: 873–881.
Chu CG, Friesen TL, Xu SS, Faris JD, Kolmer JA (2009). Identification of novel QTLs for seedling and adult plant leaf rust resistance in a wheat doubled haploid population. Theor Appl Genet 119: 263–269.
Chujo T, Miyamoto K, Ogawa S, Masuda Y, Shimizu T (2014). Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice. PLoS ONE 9(6): e98737. doi:10.1371/journal.pone.0098737.
Chuntao Y, James EJ, Scot HH (2011). Development of a hostinduced RNAi system in the wheat stripe Rust fungus Puccinia striiformis. Mol Plant Microbe Interact 24: 554–561.
Coca M, Bortolotti C, Rufat M, Penas G, Eritja R (2004). Transgenic rice plants expressing the antifungal AFP protein from Aspergillus giganteus show enhanced resistance to the rice blast fungus Magnaporthe grisea. Plant Mol Biol 54: 245–259.
Danquah EY, Barrett JA (2002). Evidence of natural selection for disease resistance in Composite Cross Five (CCV) of barley. Genetica 115: 195–203.
Diener AC, Ausubel FM (2005). Resistance to Fusarium Oxysporum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171: 305–321.
Dietrich RA, Terrence P, Scott D, Uknes J, Ward AR, Ryals JA, Dangl JL (1994). Arabidopsis mutants simulating disease resistance response. Cell 77: 565–577.
Ding SW (2010). RNA-based antiviral immunity. Nat Rev Immunol 10: 632–644.
Duan CG, Fang YY, Zhou BJ, Zhao JH, Hou WN, Zhu H, Ding SW, Guo HS (2012). Suppression of Arabidopsis ARGONAUTE1- mediated slicing, transgene induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b protein. Plant Cell 24: 259–274.
Escobar MA, Civerolo EL, Summerfelt KR, Dandekar AM (2001). RNAi-mediated oncogene silencing confers resistance to Crown Gall Tumorigenesis. Proc Natl Acad Sci 98: 13437– 13442.
Fairbairn DJ, Cavalloro AS, Bernard M, Mahalinga-Iyer J, Graham MW, Botella JR (2007). Host-delivered RNAi: an effective strategy to silence genes in plant parasite nematodes. Planta 226: 1525–1533.
Fanelli E, Di Vito M, Jones JT, De Giorgi C (2005). Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, Using RNAi. Gene 349: 87–95.
Federici BA (1998). Broad scale use of pest killing plants to be true test. California Agric 52: 13–20.
Finckh M, Gacek E, Goyeau H, Lannou C, Merz U (2000). Cereal variety and species mixtures in practice, with emphasis on disease resistance. Agronomie EDP Sci 20: 813–837.
Fleming RA, Person C (1978). Disease control through use of multilines: A theoretical contribution. Dis Cont Pest Manag 68: 1230–1233.
Genger RK, Jurkowski GI, McDowell JM, Lu H, Jung HW, Greenberg JT, Bent AF (2008). Signaling pathways that regulate the enhanced disease resistance of Arabidopsis “defense, no death” mutants. Mol Plant Microbe Interact 21: 1285–1296.
Gill KS, Nanda GS, Singh G, Aujla SS (1980). Studies on multilines in wheat (Triticum aestivum L.): breeding of a multiline variety by convergence of breeding lines. Euphytica 29: 125–128.
Goddard R, Peraldi A, Ridout C, Nicholson P (2014). Enhanced disease resistance caused by BRI1 mutation is conserved between Brachypodium distachyon and barley (Hordeum vulgare). Mol Plant Microbe Interact 27: 1095–1106.
Hammer K, Khoshbakht K (2005). Towards a ’red list’ for crop plant species. Genet Resour Crop Evol 52: 249–265.
Hanur VS (2011). GM crops and centers of origin-a case study of Bt brinjal in India. Curr Sci 100: 1285–1286.
Haq QMI, Arif A, Malathi VG (2010). Engineering resistance against mungbean yellow mosaic India virus using antisense RNA. Indian J Virol 21: 82–85.
Head G, Surber AB, Watson NA, Martin JW, Duan JJ (2002). No detection of Cry1Ac protein in soil after multiple years of transgenic Bt cotton (Bollgard) use. Environ Entomol 31: 30–36.
Hu G, Richter TE, Hulbert SH Pryor T (1996). Disease lesion mimicry caused by mutations in the rust resistance gene rp1. Plant Cell 8: 1367–1376.
Huang L, Brooks SA, Li WL, Fellers JP, Trick HN, Gill BS (2003). Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genet 164: 655– 664.
Huang X, Li J, Bao F, Zhang X, Yang S (2010). A gain-of-function mutation in the Arabidopsis disease resistance gene RPP4 confers sensitivity to low temperature. Plant Physiol 154: 796– 809.
Hussain B, Khan MA, Ali Q, Shaukat S (2012). Double haploid production is the best method for genetic improvement and genetic studies of wheat. Int J Agro Vet Med Sci 6: 216–228.
Ishizaki K, Hoshi T, Abe S, Sasaki Y, Kobayashi K, Kasaneyama H, Matsui T, Azuma S (2005). Breeding of blast resistant lines in rice variety “Koshihikari” and evaluation of their characters. Breed Sci 55: 371–377.
Iwai T, Kaku H, Honkura R, Nakamura S, Ochiai H (2002). Enhanced resistance to seed-transmitted bacterial diseases in transgenic rice plants over producing an oat cell-wall-bound thionin. Mol Plant Microbe Interact 15: 515–521.
Jackson LF, Webster RK, Allard RW, Kahler AL (1982). Genetic analysis of changes in scald resistance in barley composite cross V. Phytopathol 72: 1069–1072.
James C (2003). Global status of commercialized transgenic crops. Manila: Int. Serv. Acquis. Agri-Biotech Appl. Philippines. Johal GS (2007). Disease lesion mimics mutants of maize. Online. APSnet Features. doi: 10.1094/APSnetFeatures-2007-0707.
Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H (2007). A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Develop 21: 3123–3134.
Keneni G, Bekele E, Imtiaz M, Dagne K (2012). Genetic vulnerability of modern crop cultivars: causes, mechanism and remedies. Int J Plant Res 2: 69–79.
Kumar S, Chandra A, Pandey KC (2008). Bacillus thuringiensis (Bt) transgenic crop: an environment friendly insect-pest management strategy. J Environ Biol 29: 641–653.
Landry BS, Kesseli RV, Farrara B, Michelmore RW (1987). A genetic map of lettuce (Lactuca sativa L.) with restriction fragment length polymorphism, isozyme, disease resistance and morphological markers. Genet 116: 331–337.
Lawton KA, Friedrich L, Hunt M, Weymann K, Delaney T, Kessmann H, Staub T, Ryals J (1996). Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10: 71–82.
Lin WC, Lu CF, Wu JW, Cheng ML, Lin YM, Yang NS, Black L, Green SK, Wang JF, Cheng CP (2004). Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Trans Res 13: 567–581.
Lorrain S, Vailleau F, Balague C, Roby D (2003). Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8: 263–271.
Makandar R, Essig JS, Schapaugh MA, Trick HN, Shah J (2006). Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. Mol Plant Microbe Interact 19: 123–129.
Maroof MAS, Webster RK, Allard RW (1983). Evolution of resistance to scald, powdery mildew, and net blotch in barley composite cross II populations. Theor Appl Genet 66: 279–283. Marshall DR, Pryor AJ (1978). Multiline varieties and disease control. TheorAppl Genet 51: 177–184.
McDonald BA (2014). Using dynamic diversity to achieve durable disease resistance in agricultural ecosystems. Trop Plant Pathol 39: 191–196.
Mejlhede N, Kyjovska Z, Backes G, Burhenne K, Rasmussen SK, Jahoor A (2006). Eco-TILLING for the identification of allelic variation in the powdery mildew resistance genes Mlo and Mla of barley. Plant Breed 125: 461–467.
Mentag R, Luckevich M, Morency MJ, Séguin A (2003). Bacterial disease resistance of transgenic hybrid poplar expressing the synthetic antimicrobial peptide D4E1. Tree Physiol 23: 405– 411.
Montesinos E (2007). Antimicrobial peptides and plant disease control. FEMS MicrobiolLett 270: 1–11.
Mundt CC (2002). Use of multiline cultivars and cultivar mixtures for disease management. Annu Rev Phytopathol 40: 381–410. Mundt CC (2014). Durable resistance: a key to sustainable management of pathogens and pests. Infect Genet Evol 27: 446–455.
Murphy K, Lammer D, Lyon S, Carter B, Jones SS (2004). Breeding for organic and low-input farming systems: an evolutionaryparticipatory breeding method for inbred cereal grains. Renew Agri Food Sys 20: 48–55.
Mutlu N, Miklas P, Reiser J, Coyne D (2005). Backcross breeding for improved resistance to common bacterial blight in pinto bean (Phaseolus vulgaris L.). Plant Breed 124: 282–287.
Nakayashiki H (2005). RNA silencing in fungi: mechanisms and applications. Fed Eur Biochem Soc Lett 579: 5950–5970. Neuffer MG, Calvert OH (1975). Dominant disease lesion mimics in maize. J Heredity 66: 265–270.
Niblett CL, Bailey AM (2012). Potential applications of gene silencing or RNA interference (RNAi) to control disease and insect pests of date palm. Emir J Food Agric 24: 462–469.
Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010). HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22: 3130–3141.
Ogwok E, Odipio J, Halsey M, Gaitán-Solís E, Bua A, Taylor NJ, Fauquet CM, Alicai T (2012). Transgenic RNA interference (RNAi)-derived field resistance to cassava brown streak disease. Mol Plant Pathol 13: 1019–1031.
Oh BJ, Frederiksen RA Magill CW (1994). Identification of molecular markers linked to head smut resistance gene (Shs) in sorghum by RFLP and RAPD analyses. Phytopathol 84: 830–833. Padmanabhan SY (1973). The great Bengal famine. Annu Rev Phytopathol 11: 11–26.
Parkhi V, Kumar V, Campbell LA, Bell AA, Shah J, Rathore KS (2010). Resistance against various fungal pathogens and reniform nematode in transgenic cotton plants expressing Arabidopsis NPR1. Trans Res 19: 959–975.
Person C, Groth JV, Mylyk M (1976). Genetic change in host-parasite populations. Annu Rev Phytopathol 14: 117–188.
Phillips SL, Wolfe MS (2005). Evolutionary plant breeding for low input systems. J Agric Sci 143: 245–254.
Pooggin M, Shivaprasad PV, Veluthambi K, Hohn T (2003). RNAi targeting of DNA virus in plants. Nat Biotechnol 21: 131–132.
Portis E, Acquadro A, Comino C, Lanteri S (2004). Effect of farmers’ seed selection on genetic variation of a landrace population of pepper (Capsicum annuum L.), grown in North-West Italy. Genet Resour Crop Evol 51: 581–590.
Prins R, Pretorius ZA, Bender CM, and Lehmensiek A (2011). QTL mapping of stripe, leaf and stem rust resistance genes in a Kariega × Avocet S doubled haploid wheat population. Mol Breed 27: 259–270.
Priya B, Somasekhar N, Prasad JS, Kirti PB (2011). Transgenic tobacco plants constitutively expressing Arabidopsis NPR1 show enhanced resistance to root knot nematode, Meloidogyne incognita. BMC Res Notes 4: 231.
Quilis J, Penas G, Messeguer J, Brugidou C, Segundo BS (2008). The Arabidopsis AtNPR1 inversely modulates defense responses against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol Plant Microbe Interact 21: 1215–1231.
Rajasekaran K, Cary JW, Jaynes JM, Cleveland TE (2007). Disease resistance conferred by the expression of a gene encoding a synthetic peptide in transgenic cotton (Gossypiumhirsutum L.) plants. Plant Biotechnol J 3: 545–554.
Rashid M, He G, Guanxiao Y, Khurram Z (2011). Relevance of tilling in plant genomics. Australian J Crop Sci 5: 411–420.
Reif JC, Zhang P, Dreisigacker S, Warburton ML, van Ginkel M, Hoisington D, Bohn M, Melchinger AE (2005). Wheat genetic diversity trends during domestication and breeding. Theor Appl Genet 110: 859–864.
Rogers DL (2004). Genetic erosion: no longer just an agricultural issue. Native Plants 2004: 113–122.
Sabir HM, Tahir SH, Khan MB (2011). BT cotton and its impact on cropping pattern in Punjab. Pak J Soc Sci 31: 127–134.
Sattari A, Fakheri B, Hassan FSC, Noroozi M (2014). Blast resistance in rice: a review of breeding and biotechnology. Int J Agri Crop Sci 7: 329–333.
Schlaich T, Urbabiak B, Plissonnier M-L, Malgras N, Sautter C (2007). Exploration and Swiss field testing of a viral gene for specific quantitative resistance against smuts and bunts in wheat. Adv Biochem Engin Biotechnol 107: 97–112.
Schwind N, Zwiebel M, Itaya A, Ding B, Wang MB, Krczal G, Wassenegger M (2009). RNAi-mediated resistance to potato spindle tuber viroid in transgenic tomato expressing a viroid hairpin RNA construct. Mol Plant Pathol 10: 459–469.
Segers GC, Hamada W, Oliver RP, Spanu PD (1999). Isolation and characteristaion of five different hydrophobin-encoding cDNA from the fungal tomato pathogen Cladosporium fulvum. Mol Gen Genet 261: 644–652.
Seralini G-E (2009). Effects on Health and Environment of Transgenic (or GM) Bt Brinjal. CRIIGEN, University of Caen, France
Shabbir MZ, Arshad M, Hussain B, Nadeem I, Ali S, Abbasi A, Ali Q (2014). Genotypic response of chickpea (Cicer arietinum L.) for resistance against gram pod borer (Helicoverpa armigera). Adv Life Sci 2: 23–30.
Shah MA, Hussain CA, Hussain KI (1982). Selection of high yielding, disease resistance and frost tolerant varieties from exotic germplasm. Pak J Agric Res 3: 479–482.
Sharma D, Sanghera GS, Sahu P, Sahu P, Parikh M, Sharma B, Bhandarkar S, Chaudhari PR, Jena BK (2013). Tailoring rice plants for sustainable yield through ideotype breeding and physiological interventions. African J Agri Res 8: 5004–5019.
Sharma HC, Sharma KK, Crouch JH (2004). Genetic transformation of crops for insect resistance: potential and limitations. Crit Rev Plant Sci 23: 47–72.
Shelly PS, Ramesh V, Anil KM, Vikas K, Peter P (2010). Silencing potential of viral derived RNAi constructs in tomato leaf curl virus-AC4 gene suppression in tomato. Transg Res 19: 45–55.
Simmonds NW (1993). Introgression and incorporation. Strategies for the use of crop genetic resources. Biol Rev 68: 539–562.
Simon-Mateo C, Garcia JA (2011). Antiviral strategies in plants based on RNA silencing. Biochim Biophys Acta 1809: 722–731.
Sindhu S, Maier TR, Mitchum MG, Hussey RS, Davis EL, Baum TJ (2009). Effective and specific in plant RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J Exp Bot 60: 315–324.
Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK Singh S, Govindan V (2011). The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49: 465–481.
Spanu P (1997). HCf-1, a hydrophobin from the tomato pathogen Cladosporium fulvum. Gene 93: 89–96.
Steffan P, Borgen A, Lazzaro M, Backes G, Torp AM, Rasmussen SK (2011). Marker assisted breeding and mass selection of wheat composite cross populations. In: Organic Plant Breeding: What makes the difference? 10 Year’s Anniversary Conference, 3–4 Nov, 2011 Frankfurt, Germany.
Steves RM, Todd TC, Essig JS, Trick HN (2006). Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heteroderaglycines reproduction. Funct Plant Biol 33: 991–999.
Strange RN (2005). Plant disease: a threat to global food security. Annu Rev Phytopathol 43: 83–116.
Szankowski I, Briviba K, Fleschhut J, Schonherr J, Jacobsen HJ, Kiesecker H (2003). Transformation of apple (Malus domestica Borkh.) with the stilbene synthase gene from grapevine (Vitis vinifera L.) and a PGIP gene from kiwi (Actinidia deliciosa). Plant Cell Rep 22: 141–149.
Takumi S, Motoyasu Y, Taiyun W, Hirohiko H, Toshihiro O (2008). Silencing by RNAi of the gene for Pns12, a viroplasm matrix protein of rice dwarf virus, results in strong resistance of transgenic rice plants to the virus. Plant Biotechnol J 7: 24–32.
Ullstrup AJ (1972). The impact of the southern corn leaf blight epidemics of 1970–71. Annu Rev Phytopathol 10: 37–50.
van de Wouw M, Kik C, van Hintum T, van Treuren R, Visser B (2009). Genetic erosion in crops: concept, research results and challenges. Plant Genet Resour 8: 1–15.
Van der Plank JE (1975). Principles of Plant Infection. New York, San Francisco, and London: Academic Press. pp 216.
van der Vossen E, Sikkema A, Hekkert BTL, Gros J, Stevens P, Muskens M (2003). An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J 36: 867–882.
Walbot V, Hoisington DA, Neuffer MG (1983). Disease lesion mimic mutations. In: Genetic Engineering of Plants. New York, NY, USA: Plenum Publ. Corp., pp. 431–442.
Wally O, Jayaraj J, Punja Z (2009). Broad‐spectrum disease resistance to necrotrophic and biotrophic pathogens in transgenic carrots (Daucus carota L.) expressing an Arabidopsis NPR1 gene. Planta 231: 131–141.
Wang D, Guo C, Huang J, Yang S, Tian D, Zhang X (2014). Allelemining of rice blast resistance genes at AC134922 locus. Biochem Biophys Res Commun 446: 1085–1090.
Wang H, Pandey MK, Qiao L, Qin H, Culbreath AK, He G, Varshney RK, GuoB (2013). Genetic mapping and QTL analysis for disease resistance using F2 and F5 generationbased genetic maps derived from Tifrunner × GT-C20 in 2 peanut (Arachishypogaea L.). plant genome, doi: 10.3835/ plantgenome2013.05.0018.
Warren RF, Henk A, Mowery P, Holub E, Innes RW (1998). A Mutation within the Leucine-Rich Repeat domain of the arabidopsis disease resistance gene rps5 partially suppresses multiple bacterial and downy mildew resistance Genes. Plant Cell 10: 1439–1452.
Wawrzynska A, Christiansen KM, Lan Y, Rodibaugh NL, Innes RW (2008). Powdery mildew resistance conferred by loss of the ENHANCED DISEASE RESISTANCE1 protein kinase is suppressed by a missense mutation in KEEP ON GOING, a regulator of abscisic acid signaling. Plant Physiol 148: 1510– 1522.
Wilson IW, Schiff CL, Hughes DE, Somerville SC (2001). Quantitative trait loci analysis of powdery mildew disease resistance in the Arabidopsis thaliana accession Kashmir-1. Genetics 158: 1301– 1309.
Wilson JP, Gates RN, Panwar MS (2001). Dynamic multiline population approach to resistance gene management. Phytopathol 91: 255–260.
Wolfe MS (1993). Can the strategic use of disease resistant hosts protect their inherent durability? In: Jacobs T, Parleviet JE (Ed). Durability of Disease Resistance. Wageningen, Neth.: Kluwer.
Yang ZP, Gilbert J, Fedak G, Somers DJ (2005). Genetic characterization of QTL associated with resistance to Fusarium head blight in a doubled-haploid spring wheat population. Genome 48: 187–196
Yin Z, Chen J, Zeng L, Goh M, Leung H (2000). Characterizing rice lesion mimic mutants and identifying a mutant with broadspectrum resistance to rice blast and bacterial blight. Mol Plant Microbe Interact 13: 869–876.
Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M (2004). Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16: 2795–2808.
Zhang BH, Guo T-L, Wang Q-L (2000). Inheritance and segregation of exogenous genes in transgenic cotton. J Genet 79: 71–75. Zhang LH, Xu JL, Birch RG (1999). Engineered detoxification confers resistance against a pathogenic bacterium. Nat Biotechnol 17: 1021–1024.
Zhang XD, Francis MI, Dawson WO, Graham JH, Orbovic V, Triplett EW, Mou ZL (2010). Over‐expression of the Arabidopsis NPR1 gene in citrus increases resistance to citrus canker. European J Plant Pathol 128: 91–100.
Zhang Y, Goritschnig S, Dong X, Li X (2003). A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15: 2636–2646.
Zhao BY, Lin XH, Poland J, Trick H, Leach J, Hulbert S (2005). From the cover: a maize resistance gene functions against bacterial streak disease in rice. Proc Nat Acad Sci 102: 15383–15388.
Zhu B, Lawrence JR, Warwick SI, Mason P, Braun L, Halfhill MD, Stewart CN (2004). Stable Bacillus thuringiensis (Bt) toxin content in interspecific F1 and backcross populations of wild Brassica rapa after Bt gene transfer. Mol Ecol 13: 237–241.
Zhu Y, Du B, Qian J, Zou B, Hua J (2013). Disease resistance geneinduced growth inhibition is enhanced by rcd1 independent of defense activation in Arabidopsis. Plant Physiol 161: 2005– 2013.
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764–767.