Genomics of Papaya Disease Resistance

  • Brad W. Porter
  • David A. Christopher
  • Yun J. ZhuEmail author
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 10)


From seedling emergence through postharvest fruit distribution, Carica papaya is challenged by a wide range of pests and pathogens that diminish fruit yield and marketability. Because chemical control may be costly, unavailable, or ineffective, comprehensive pathogen management strategies, including increased genetic resistance, are needed. Today, heterologous transformation and interspecific and intergeneric hybridization are used to improve disease resistance. Transgene approaches have been used to control several strains of papaya ringspot virus and, along with the introgression of resistance from wild relatives, may be used for controlling other pathogens as well. Expansions of these sources of resistance are needed to ensure that modern cultivars evolve with microbial populations. The papaya genome sequence is available and can be used to provide markers to identify and isolate R-genes from C. papaya and related species. These genes can be introduced into susceptible lines using transformation. The emergence of new diseases and movement of pathogens suggests that extending resistance durability will require a comprehensive strategy of integrating genetic resistance, cultural practices, and factors including innate protection provided by beneficial plant–microbe interactions. Transgene efficacy will need to be monitored during disease epidemics and, likewise, evaluated for changes that may occur over generations in the absence of pathogen selection pressure. Developing and coordinating the use of papaya’s disease resistance resources will ensure that this species continues to provide a valuable source of nutrition for the world’s tropical and subtropical regions and the markets that rely upon these regions for imported fruit.


Arbuscular Mycorrhizal Fungus Botrytis Cinerea Parthenocarpic Fruit Postzygotic Barrier Papaya Ringspot Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abel PP, Nelson RS, De B, Hoffmann N, Rogers G, Fraley RT, Beachy RN (1986) Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science 232:738–743PubMedCrossRefGoogle Scholar
  2. Adrian M, Jeandet P, Veneau J, Weston LA, Bessis R (1997) Biological activity of resveratrol, a stilbenic compound from grapevines, against Botrytis cinerea, the causal agent for gray mold. J Chem Ecol 23:1689–1702CrossRefGoogle Scholar
  3. Aluja M, Jimene A, Camino M, Aldana L, Castrejon V, Valdes YME (1994) Determinacion de la susceptibilidad de tres variedades de papaya (Carica papaya) al ataque de Toxotrypana curvicauda (Diptera: Tephritidae). Folia Entomol Mex 90:33–42Google Scholar
  4. Alvarez AM, Nishijima WT (1987) Postharvest diseases of papaya. Plant Disease 71:681–686CrossRefGoogle Scholar
  5. Aradhya MK, Manshardt RM, Zee F, Morden CW (1999) A phylogenetic analysis of the genus Carica L. (Caricaceae) based on restriction fragment length variation in a cpDNA intergenic spacer region. Genet Resour Crop Evol 46:579–586CrossRefGoogle Scholar
  6. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274CrossRefGoogle Scholar
  7. Arocha Y, Horta D, Peralta E, Jones P (2003) First report on molecular detection of phytoplasmas in papaya in Cuba. Disease notes. Plant Disease 87:1148CrossRefGoogle Scholar
  8. Arocha Y, Piñol B, Picornell B, Almeida R, Jones P (2006) First report of a 16SrII (“Candidatus Phytoplasma aurantifolia”) group phytoplasma associated with a bunchy-top disease of papaya in Cuba. New disease report. Plant Pathol 55:821CrossRefGoogle Scholar
  9. Arocha Y, Bekele B, Tadesse D, Jones P (2007) First report of a 16SrII group phytoplasma associated with die-back diseases of papaya and citrus in Ethiopia. New disease report. Plant Pathol 56:1039CrossRefGoogle Scholar
  10. Arocha Y, Vigheri N, Nkoy-Florent B, Bakwanamaha K, Bolomphety B, Kasongo M, Betts P, Monger WA, Harju V, Mumford RA, Jones P (2008) First report of the identification of Moroccan watermelon mosaic virus in papaya in Democratic Republic of Congo. New disease report. Plant Pathol 57:387CrossRefGoogle Scholar
  11. Asurmendi S, Berg RH, Koo JC, Beachy RN (2004) Coat protein regulates formation of replication complexes during tobacco mosaic virus infection. Proc Natl Acad Sci USA 101:1415–1420PubMedCrossRefGoogle Scholar
  12. Austin MB, Noel JP (2003) The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep 20:79–110PubMedCrossRefGoogle Scholar
  13. Badillo VM (2000) Carica L. vs. Vasconcellea St. Hil. (Caricaceae) con la rehabilitacion de este ultimo. Ernstia 10:74–79Google Scholar
  14. Bau HJ, Kung YJ, Raja JA, Chan SJ, Chen KC, Chen YK, Wu HW, Yeh SD (2008) Potential threat of a new pathotype of Papaya leaf distortion mosaic virus infecting transgenic papaya resistant to Papaya ringspot virus. Phytopathology 98:848–856PubMedCrossRefGoogle Scholar
  15. Baulcombe DC (1996) Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 8:1833–1844PubMedGoogle Scholar
  16. Bazzini AA, Hopp HE, Beachy RN, Asurmendi S (2006) Posttranscriptional gene silencing does not play a significant role in Potato virus X coat protein-mediated resistance. Phytopathology 96:1175–1178PubMedCrossRefGoogle Scholar
  17. Bendahmane M, Szecsi J, Chen I, Berg RH, Beachy RN (2002) Characterization of mutant tobacco mosaic virus coat protein that interferes with virus cell-to-cell movement. Proc Natl Acad Sci USA 99:3645–3650PubMedCrossRefGoogle Scholar
  18. Birch PR, Rehmany AP, Pritchard L, Kamoun S, Beynon JL (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol 14:8–11PubMedCrossRefGoogle Scholar
  19. Boot RG, Blommaart EF, Swart E, Ghauharali-van der Vlugt K, Bijl N, Moe C, Place A, Aerts JM (2001) Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J Biol Chem 276:6770–6778PubMedCrossRefGoogle Scholar
  20. Bos JI, Armstrong MR, Gilroy EM, Boevink PC, Hein I, Taylor RM, Zhendong T, Engelhardt S, Vetukuri RR, Harrower B, Dixelius C, Bryan G, Sadanandom A, Whisson SC, Kamoun S, Birch PR (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc Natl Acad Sci USA 107:9909–9914PubMedCrossRefGoogle Scholar
  21. CERA (2010) GM crop database. Center for Environmental Risk Assessment (CERA), ILSI Research Foundation, Washington, DC.
  22. Champouret N, Bouwmeester K, Rietman H, van der Lee T, Maliepaard C, Heupink A, van de Vondervoort PJ, Jacobsen E, Visser RG, van der Vossen EA, Govers F, Vleeshouwers VG (2009) Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato. Mol Plant Microbe Interact 22:1535–1545PubMedCrossRefGoogle Scholar
  23. Chang LS, Lee YS, Su HJ, Hung TH (2003) First report of Papaya leaf curl virus infecting papaya plants in Taiwan. Disease notes. Plant Disease 87:204CrossRefGoogle Scholar
  24. Chaudhari SS, Arakane Y, Specht CA, Moussian B, Boyle DL, Park Y, Kramer KJ, Beeman RW, Muthukrishnan S (2011) Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton. Proc Natl Acad Sci USA 108:17028–17033PubMedCrossRefGoogle Scholar
  25. Chen KC, Chiang CH, Raja JA, Liu FL, Tai CH, Yeh SD (2008) A single amino acid of NIaPro of Papaya ringspot virus determines host specificity for infection of papaya. Mol Plant Microbe Interact 21:1046–1057PubMedCrossRefGoogle Scholar
  26. Chen RS, Wang WL, Li JC, Wang YY, Tsay JG (2009) First report of papaya scab caused by Cladosporium cladosporioides in Taiwan. Disease notes. Plant Disease 93:426CrossRefGoogle Scholar
  27. Chin M, Ahmad MH, Tennant P (2007) Momordica charantia is a weed host reservoir for Papaya ringspot virus Type P in Jamaica. Disease notes. Plant Disease 91:1518CrossRefGoogle Scholar
  28. Chou S, Krasileva KV, Holton JM, Steinbrenner AD, Alber T, Staskawicz BJ (2011) Hyaloperonospora arabidopsidis ATR1 effector is a repeat protein with distributed recognition surfaces. Proc Natl Acad Sci USA 108:13323–13328PubMedCrossRefGoogle Scholar
  29. Conove RA (1964) Distortion ringspot, a severe virus disease of papaya in Florida. Fla Agric Exp Stations J Ser 2001:440–444Google Scholar
  30. Conover RA, Litz RE (1978) Progress in breeding papayas with tolerance to papaya ringspot virus. Proc Fla State Hortic Soc 91:182–184Google Scholar
  31. Conover RA, Litz RE, Malo SE (1986) “Cariflora” a papaya ringspot virus tolerant papaya for South Florida and the Caribbean. Hortscience 21:1072Google Scholar
  32. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  33. Delaunois B, Cordelier S, Conreux A, Clément C, Jeandet P (2009) Molecular engineering of resveratrol in plants. Plant Biotechnol J 7:2–12PubMedCrossRefGoogle Scholar
  34. DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7:1243–1249PubMedCrossRefGoogle Scholar
  35. Diallo HA, Monger W, Kouassi N, Yoro DT, Jones P (2007) First report of Papaya ringspot virus infecting papaya in Côte d’Ivoire. New disease report. Plant Pathol 56:718CrossRefGoogle Scholar
  36. Dianese AC, Blum LEB, Dutra JB, Lopes LF, Sena MC, Freitas LF, Yamanishi OK (2007) Reaction of papaya genotypes to black-spot and foot-rot. Fitopatol Bras 32:419–423Google Scholar
  37. Dianese AC, Blum LEB, Dutra JB, Freitas LF, Lopes LF, Sena MC, Lima L, Yamanishi OK, Martins DMS (2010) Reaction of papaya (Carica papaya) genotypes to foot rot caused by Phytophthora palmivora. Acta Hortic 864:249–255Google Scholar
  38. Dillon SK, Drew RA, Ramage C (2005a) Development of a co-dominant SCAR marker linked to a putative PRSV-P resistance locus in “wild papaya”. Acta Hortic 694:101–104Google Scholar
  39. Dillon S, Ramage C, Drew R, Ashmore S (2005b) Genetic mapping of a PRSV-P resistance gene in “highland papaya” based on inheritance of RAF markers. Euphytica 145:11–23CrossRefGoogle Scholar
  40. Dillon S, O’Brien CM, Drew RA, Ramage C (2006a) Application of SCAR markers linked to a putative PRSV-P resistance locus for assisted breeding of resistant C. papaya cultivars. Acta Hortic 725:627–633Google Scholar
  41. Dillon S, Ramage C, Ashmore S, Drew RA (2006b) Development of a codominant CAPS marker linked to PRSV-P resistance in highland papaya. Theor Appl Genet 113:1159–1169PubMedCrossRefGoogle Scholar
  42. Ding X, Gopalakrishnan B, Johnson LB, White FF, Wang X, Morgan TD, Kramer KJ, Muthukrishnan S (1998) Insect resistance of transgenic tobacco expressing an insect chitinase gene. Transgenic Res 7:77–84PubMedCrossRefGoogle Scholar
  43. Dowd C, Wilson IW, McFadden H (2004) Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Mol Plant Microbe Interact 17:654–667PubMedCrossRefGoogle Scholar
  44. Drew RA, Magdalita PM, O’Brien CM (1998) Development of Carica interspecific hybrids. Acta Hortic 461:285–291Google Scholar
  45. Drew R, Persley D, O’Brien C, Bateson M (2005a) Papaya ringspot virus in Australia and the development of virus resistant plants. Acta Hortic 692:101–106Google Scholar
  46. Drew RA, Siar SV, Villegas VN, O’Brien CM, Sajise AGC (2005b) Development of PRSV-P resistant Carica papaya genotypes by introgression of genes from wild Vasconcella species. Acta Hortic 694:73–77Google Scholar
  47. Drew R, Siar SV, Dillon S, Ramage C, O’Brien C, Sajise AGC (2007) Intergeneric hybridisation between Carica papaya and wild Vasconcellea species and identification of a PRSV-P resistance gene. Acta Hortic 738:165–169Google Scholar
  48. Ellis JG, Dodds PN (2011) Showdown at the RXLR motif: Serious differences of opinion in how effector proteins from filamentous eukaryotic pathogens enter plant cells. Proc Natl Acad Sci USA 108:14381–14382PubMedCrossRefGoogle Scholar
  49. Environmental Protection Agency (2009) Pesticide Fact Sheet. Available:
  50. Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. APS, St. PaulGoogle Scholar
  51. Fermin G, Inglessis V, Garboza C, Rangel S, Dagert M, Gonsalves D (2004) Engineered resistance against papaya ringspot virus in Venezuelan transgenic papayas. Plant Disease 88:516–522CrossRefGoogle Scholar
  52. Ferrer JL, Austin MB, Stewart C Jr, Noel JP (2008) Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant Physiol Biochem 46:356–370PubMedCrossRefGoogle Scholar
  53. Fischer R, Budde I, Hain R (1997) Stilbene synthase gene expression causes changes in flower colour and male sterility in tobacco. Plant J 11:489–498CrossRefGoogle Scholar
  54. Fitch MMM (1993) High frequency somatic embryogenesis and plant regeneration from papaya hypocotyl callus. Plant Cell Tiss Org Cult 32:205–212CrossRefGoogle Scholar
  55. Fitch MMM, Manshardt RM (1990) Somatic embryogenesis and plant regeneration from immature zygotic embryos of papaya (Carica papaya L.). Plant Cell Rep 9:320–324Google Scholar
  56. Fitch MMM, Manshardt RM, Gonsalves D, Slightom JL, Sanford JC (1990) Stable transformation of papaya via microprojectile bombardment. Plant Cell Rep 9:189–194Google Scholar
  57. Fitch MMM, Manshardt RM, Gonsalves D, Slightom JL, Sanford JC (1992) Virus resistant papaya plants derived from tissues bombarded with the coat protein gene of papaya ringspot virus. Nat Biotechnol 10:1466–1472CrossRefGoogle Scholar
  58. Fitter AH, Moyerson B (1996) Evolutionary trends in root-microbe symbioses. Phil Trans R Soc Land B 351:1367–1375CrossRefGoogle Scholar
  59. Food and Agriculture Organization of the United Nations (2009) Statistics Division, FAOSTAT, Crops Production DataGoogle Scholar
  60. Fornara V, Onelli E, Sparvoli F, Rossoni M, Aina R, Marino G, Citterio S (2008) Localization of stilbene synthase in Vitis vinifera L. during berry development. Protoplasma 233:83–93PubMedCrossRefGoogle Scholar
  61. Freeman S, Rodriguez RJ (1992) A rapid, reliable bioassay for pathogenicity of Colletotrichum magna on cucurbits and its use in screening for nonpathogenic mutants. Plant Disease 76:901–905CrossRefGoogle Scholar
  62. Freeman S, Rodriguez RJ (1993) Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260:75–78PubMedCrossRefGoogle Scholar
  63. Fry W (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9:385–402PubMedCrossRefGoogle Scholar
  64. Fullerton RA, Taufa L, Vanneste JL, Yu J, Cornish DA, Park D (2011) First record of bacterial crown rot of papaya (Carica papaya) caused by an Erwinia papayae-like bacterium in the Kingdom of Tonga. Disease notes. Plant Disease 95:70CrossRefGoogle Scholar
  65. Ganz T (2003) Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3:710–720PubMedCrossRefGoogle Scholar
  66. Gao AG, Hakimi SM, Mittanck CA, Wu Y, Woerner BM, Stark DM, Shah DM, Liang J, Rommens CM (2000) Fungal pathogen protection in potato by expression of a plant defensin peptide. Nat Biotechnol 18:1307–1310PubMedCrossRefGoogle Scholar
  67. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS One 6(7):e22629PubMedCrossRefGoogle Scholar
  68. Gera A, Mawassi M, Zeidan M, Spiegel S, Bar-Joseph M (2005) An isolate of “Candidatus Phytoplasma australiense” group associated with Nivun-Haamir-Die Back disease of papaya in Israel. New disease report. Plant Pathol 54:560CrossRefGoogle Scholar
  69. Gibb KS, Schneider B, Padovan AC (1998) Differential detection and genetic relatedness of phytoplasmas in papaya. Plant Pathol 47:325–332CrossRefGoogle Scholar
  70. Gilroy EM, Taylor RM, Hein I, Boevink P, Sadanandom A, Birch PR (2011) CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytol 190:653–666PubMedCrossRefGoogle Scholar
  71. Goff L (1986) Spider mites (Acari: Tetranychidae) in the Hawaiian Islands. Int J Acarol 12:43–49CrossRefGoogle Scholar
  72. Gonsalves D (1998) Control of papaya ringspot virus in papaya: a case study. Annu Rev Phytopathol 36:415–437PubMedCrossRefGoogle Scholar
  73. Grünwald NJ, Flier WG (2005) The biology of Phytophthora infestans at its center of origin. Annu Rev Phytopathol 43:171–190PubMedCrossRefGoogle Scholar
  74. Guttman JA, Samji FN, Li Y, Deng W, Lin A, Finlay BB (2007) Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens. Cell Microbiol 9:131–141PubMedCrossRefGoogle Scholar
  75. Hain R, Reif HJ, Krause E, Langebartels R, Kindl H, Vornam B, Wiese W, Schmelzer E, Schreier PH, Stöcker RH, Stenzel K (1993) Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361:153–156PubMedCrossRefGoogle Scholar
  76. Hammerbacher A, Ralph SG, Bohlmann J, Fenning TM, Gershenzon J, Schmidt A (2011) Biosynthesis of the major tetrahydroxystilbenes in spruce, astringin and isorhapontin, proceeds via resveratrol and is enhanced by fungal infection. Plant Physiol 157:876–890, Epub 2011 Aug 24PubMedCrossRefGoogle Scholar
  77. Hawtin RE, Zarkowska T, Arnold K, Thomas CJ, Gooday GW, King LA, Kuzio JA, Possee RD (1997) Liquefaction of Autographa californica nucleopolyhedrovirus-infected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes. Virology 238:243–253PubMedCrossRefGoogle Scholar
  78. Hijmans RJ, Spooner DM (2001) Geographic distribution of wild potato species. Am J Bot 88:2101–2112PubMedCrossRefGoogle Scholar
  79. Hipskind JD, Paiva NL (2000) Constitutive accumulation of a resveratrol-glucoside in transgenic alfalfa increases resistance to Phoma medicaginis. Mol Plant Microbe Interact 13:551–562PubMedCrossRefGoogle Scholar
  80. Horovitz S, Jiménez H (1967) Cruzamientos interespecíficos e intergenéricos en caricaceae y sus implicaciones fitotécnicas. Agron Trop 3:323–343Google Scholar
  81. Ingrosso I, Bonsegna S, Dedomenico S, Laddomada B, Blando F, Santino A, Giovinazzo G (2011) Over-expression of a grape stilbene synthase gene in tomato induces parthenocarpy and causes abnormal pollen development. Plant Physiol Biochem 49:1092–1099PubMedCrossRefGoogle Scholar
  82. Initiative AG (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  83. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  84. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467PubMedCrossRefGoogle Scholar
  85. Jain RK, Nasiruddin KM, Sharma J, Pant RP, Varma A (2004) First report of occurrence of papaya ring spot virus infecting papaya in Bangladesh. Disease notes. Plant Disease 88:221CrossRefGoogle Scholar
  86. Jaizme-Vega MC, Rodríguez-Romero AS, Núñez LAB (2006) Effect of the combined inoculation of arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria on papaya (Carica papaya L.) infected with the root-knot nematode Meloidogyne incognita. Fruits 61:151–162CrossRefGoogle Scholar
  87. Jha S, Tank HG, Prasad BD, Chattoo BB (2009) Expression of Dm-AMP1 in rice confers resistance to Magnaporthe oryzae and Rhizoctonia solani. Transgenic Res 18:59–69PubMedCrossRefGoogle Scholar
  88. Jobin-Décor MP, Graham GC, Henry RJ, Drew RA (1997) RAPD and isozyme analysis of genetic relationships between Carica papaya and wild relatives. Genet Resour Crop Evol 44:471–477CrossRefGoogle Scholar
  89. Júnior MTS, Nickel O, Gonsalves D (2005) Development of virus resistant transgenic papayas expressing the coat protein gene from a Brazilian isolate of Papaya ringspot virus. Fitopatol Bras 30:357–365Google Scholar
  90. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T, Lawrence CB, Shan W, Tyler BM (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284–295PubMedCrossRefGoogle Scholar
  91. Kalleshwaraswamy CM, Kumar NK (2008) Transmission efficiency of papaya ringspot virus by three aphid species. Phytopathology 98:541–546PubMedCrossRefGoogle Scholar
  92. Keith RC, Nishijima KA, Keith LM, Fitch MM, Nishijima WT, Wall MM (2008) Atypical internal yellowing of papaya fruit in Hawaii caused by Enterobacter sakazakii. Disease notes. Plant Disease 92:487CrossRefGoogle Scholar
  93. Kempler C, Kabaluk T (1996) Babaco (Carica pentagona Heilb.): a possible crop for the greenhouse. Hortscience 31:785–788Google Scholar
  94. Kilman S (2001) Monsanto Co. shelves seed that turned out to be a dud of a spud. Wall Street J B21 (March 21)Google Scholar
  95. Kim MS, Moore PH, Zee F, Fitch MMM, Steiger DL, Manshardt RM, Paull RE, Drew RA, Sekioka T, Ming R (2002) Genetic diversity of Carica papaya as revealed by AFLP markers. Genome 45:503–512PubMedCrossRefGoogle Scholar
  96. Kung YJ, Bau HJ, Wu YL, Huang CH, Chen TM, Yeh SD (2009) Generation of transgenic papaya with double resistance to Papaya ringspot virus and Papaya leaf-distortion mosaic virus. Phytopathology 99:1312–1320PubMedCrossRefGoogle Scholar
  97. Kung YJ, Yu TA, Huang CH, Wang HC, Wang SL, Yeh SD (2010) Generation of hermaphrodite transgenic papaya lines with virus resistance via transformation of somatic embryos derived from adventitious roots of in vitro shoots. Transgenic Res 19:621–635PubMedCrossRefGoogle Scholar
  98. Kyndt T, Gheysen G (2007) Evolutionary relationships between and within the highland papayas (Genus Vasconcellea) and the common papaya (Carica papaya). Acta Hortic 740:61–72Google Scholar
  99. Latijnhouwers M, de Wit PJ, Govers F (2003) Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol 11:462–469PubMedCrossRefGoogle Scholar
  100. Leckband G, Lörz H (1998) Transformation and expression of a stilbene synthase gene of Vitis vinifera L. in barley and wheat for increased fungal resistance. Theor Appl Genet 96:1004–1012CrossRefGoogle Scholar
  101. Lentz DL (1999) Plant resources of the ancient Maya, The paleoethnobotanical evidence. In: White CD (ed) Reconstructing ancient Maya diet. The University of Utah Press, Salt Lake City, pp 3–18 (Chapter 1)Google Scholar
  102. Ling K, Namba S, Gonsalves C, Slightom JL, Gonsalves G (1991) Protection against detrimental effects of potyvirus infection in transgenic tobacco plants expressing the papaya ringspot virus coat protein gene. Biotechnology 9:752–758PubMedCrossRefGoogle Scholar
  103. Liu Z, Zhuang C, Sheng S, Shao L, Zhao W, Zhao S (2011) Overexpression of a resveratrol synthase gene (PcRS) from Polygonum cuspidatum in transgenic Arabidopsis causes the accumulation of trans-piceid with antifungal activity. Plant Cell Rep 30:2027–2036PubMedCrossRefGoogle Scholar
  104. Magdalita PM, Adkins SW, Godwin ID, Drew RA (1996) An improved embryo-rescue protocol for a Carica interspecific hybrid. Aust J Bot 44:343–353CrossRefGoogle Scholar
  105. Magdalita PM, Persley DM, Godwin ID, Drew RA (1997) Screening Carica papaya × C. cauliflora hybrids for resistance to papaya ringspot virus-type P. Plant Pathol 46:837–841CrossRefGoogle Scholar
  106. Magdalita PM, Drew RA, Godwin ID, Adkins SW (1998) An efficient interspecific hybridization protocol for Carica papaya L. × C. cauliflora Jacq. Aust J Exp Agric 38:523–530CrossRefGoogle Scholar
  107. Maktar NH, Kamis S, Mohd Yusof FZ, Hussain NH (2008) Erwinia papayae causing papaya dieback in Malaysia. New disease report. Plant Pathol 57:774CrossRefGoogle Scholar
  108. Mamanova L, Coffey AJ, Scott CE, Kozarewa I, Turner EH, Kumar A, Howard E, Shendure J, Turner DJ (2010) Target-enrichment strategies for next-generation sequencing. Nat Methods 7:111–118PubMedCrossRefGoogle Scholar
  109. Mangrauthia SK, Singh P, Praveen S (2010) Genomics of helper component proteinase reveals effective strategy for papaya ringspot virus resistance. Mol Biotechnol 44:22–29PubMedCrossRefGoogle Scholar
  110. Manshardt RM, Wenslaff TF (1989a) Zygotic polyembryony in interspecific hybrids of Carica papaya and C. cauliflora. J Am Soc Hortic Sci 114:684–689Google Scholar
  111. Manshardt RM, Wenslaff TF (1989b) Interspecific hybridization of papaya with other Carica species. J Am Soc Hortic Sci 114:689–694Google Scholar
  112. Manshardt RM, Zee FTP (1994) Papaya germplasm and breeding in Hawaii. Fruit Varieties J 48:146–152Google Scholar
  113. Maoka T, Hataya T (2005) The complete nucleotide sequence and biotype variability of papaya leaf distortion mosaic virus. Phytopathology 95:128–135PubMedCrossRefGoogle Scholar
  114. McCafferty HR, Moore PH, Zhu YJ (2006) Improved Carica papaya tolerance to carmine spider mite by the expression of Manduca sexta chitinase transgene. Transgenic Res 15:337–347PubMedCrossRefGoogle Scholar
  115. McDowell JM, Simon SA (2006) Recent insights into R gene evolution. Mol Plant Pathol 7:437–448PubMedCrossRefGoogle Scholar
  116. Mchau GRA, Coffey MD (1994) Isozyme diversity in Phytophthora palmivora: evidence for a southeast Asian centre of origin. Mycol Res 98:1035–1043CrossRefGoogle Scholar
  117. Mekako HU, Nakasone HY (1975) Interspecific hybridization among 6 Carica species. J Am Soc Hortic Sci 100:237–242Google Scholar
  118. Miksicek CH (1983) Macrofloral remains of the Pulltrouser area: settlements and fields. In: Turner II BL, Harrison PD (eds) Pulltrouser swamp: ancient Maya habitat, agriculture, and settlement in northern Belize. University of Texas Press, Austin, pp 94–104Google Scholar
  119. Miller CD (1926) The vitamins (A, B, and C) of papaya. Biochem J 20:515–518PubMedGoogle Scholar
  120. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996PubMedCrossRefGoogle Scholar
  121. Miyasaka SC, Habte M (2001) Plant mechanisms and mycorrhizal symbioses to increase phosphorus uptake efficiency. Commun Soil Sci Plant Anal 32(7/8):1101–1147CrossRefGoogle Scholar
  122. Mlot C (2004) Microbial diversity unbound. What DNA-based techniques are revealing about the planet’s hidden biodiversity. Bioscience 54:1064–1068CrossRefGoogle Scholar
  123. Mosqueda-Vázquez R, Nakasone HY (1982) Diallel analysis of root rot resistance in papaya. Hortscience 17:384–385Google Scholar
  124. Mosqueda-Vázquez R, Aragaki M, Nakasone HY (1981) Screening of Carica papaya L. seedlings for resistance to root rot caused by Phytophthora palmivora Butl. J Am Soc Hortic Sci 106:484–487Google Scholar
  125. Nadeem A, Mehmood T, Tahir M, Khalid S, Xiong Z (1997) First report of Papaya leaf curl disease in Pakistan. Disease notes. Plant Disease 81:1333CrossRefGoogle Scholar
  126. Nakasone HY, Aragaki M (1982) Current status of papaya improvement program. Hawaii Inst Trop Agric Hum Resour Res Ext Ser 033:51–55Google Scholar
  127. Nascimento RJ, Mizubuti ESG, Câmara MPS, Ferreira MF, Maymon M, Freeman S, Michereff SJ (2010) First report of papaya fruit rot caused by Colletotrichum magna in Brazil. Disease notes. Plant Disease 94:1506CrossRefGoogle Scholar
  128. National Oceanic and Atmospheric Administration (NOAA), climate data, climatological normals, normal precipitation inches, 30 year normals 1971–2000.
  129. National Research Council (1989) Lost crops of the Incas: little-known plants of the Andes with promise for worldwide cultivation. National Academy Press, Washington, DCGoogle Scholar
  130. Newcombe G, Martin F, Kohler A (2010) Defense and nutrient mutualisms in Populus. In: Jansson S, Bhalerao RP, Groove, AT (eds) Genetics and genomics of Populus. Part III. Genetics and genomics of key Populus traits. Springer, New York, pp 247–277Google Scholar
  131. Nishijima WT, Aragaki M (1973) Pathogenicity and further characterization of Calonectria crotalariae causing collar rot of papaya. Phytopathology 63:553–558CrossRefGoogle Scholar
  132. Noa-Carrazana JC, Silva-Rosales L (2001) First report of a Mexican isolate of Papaya mosaic virus in papaya (Carica papaya) and pumpkin (Cucurbita pepo). Disease notes. Plant Disease 85:558CrossRefGoogle Scholar
  133. Noorda-Nguyen K, Jia R, Aoki A, Yu Q, Nishijima W, Zhu YJ (2010) Identification of disease tolerance loci to Phytophthora palmivora in Carica papaya using molecular marker approach. Acta Hortic 851:189–196Google Scholar
  134. O’Brien CM, Drew RA (2010) Parker-assisted hybridization and backcrossing between Vasconcellea species and Carica papaya for PRSV-P resistance. Acta Hortic 859:361–368Google Scholar
  135. Ochoa J, Fonseca G, Ellis MA (2000) First report of Fusarium wilt of Babaco (Carica × heilbornii var. pentagona) in Ecuador. Plant Disease 84:199CrossRefGoogle Scholar
  136. Ogata DY, Heu RA (2001) Black spot of papaya disease, Asperisporium caricae (Speg.) Maulbl. State of Hawaii, Department of Agriculture. New pest advisory no. 2001-01Google Scholar
  137. Osborn RW, De Samblanx GW, Thevissen K, Goderis I, Torrekens S, Van Leuven F, Attenborough S, Rees SB, Broekaert WF (1995) Isolation and characterization of plant defensins from seeds of Asteraceae, Fabaceae, Hippocastanaceae and Saxifragaceae. Fed Eur Biochem Soc Lett 368:257–262CrossRefGoogle Scholar
  138. Pantoja A, Follett PA, Villanueva-Jiménez JA (2002) Pests of papaya. In: Peña JE, Sharp JL, Wysoki M (eds) Tropical fruit pests and pollinators: biology, economic importance, natural enemies and control. CABI, New York, pp 131–156 (Chapter 5)Google Scholar
  139. Parris GK (1941) Diseases of papaya in Hawaii and their control. In: Papaya production in the Hawaiian Islands. Hawaii Experiment Station Bulletin 87, pp 32–44Google Scholar
  140. Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Métraux JP, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323PubMedGoogle Scholar
  141. Persley DM, Ploetz RC (2003) Diseases of papaya. In: Ploetz, RC. (ed) Diseases of tropical fruit crops. CABI, Cambridge, pp 373–412 (Chapter 17)Google Scholar
  142. Pezet R, Pont V (1990) Ultrastructural observations of pterostilbene fungitoxicity in dormant conidia of Botrytis cinerea Pers. J Phytopathol 129:19–30CrossRefGoogle Scholar
  143. Pezet R, Gindro K, Viret O, Spring JL (2004) Glycosylation and oxidative dimerization of resveratrol are respectively associated to sensitivity and resistance of grapevine cultivars to downy mildew. Physiol Mol Plant Pathol 65:297–303CrossRefGoogle Scholar
  144. Porter BW, Aizawa KS, Zhu YJ, Christopher DA (2008) Differentially expressed and new non-protein-coding genes from a Carica papaya root transcriptome survey. Plant Sci 174:38–50CrossRefGoogle Scholar
  145. Porter BW, Paidi M, Ming R, Alam M, Nishijima WT, Zhu YJ (2009a) Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol Genet Genomics 281:609–626PubMedCrossRefGoogle Scholar
  146. Porter BW, Zhu YJ, Christopher DA (2009b) Carica papaya genes regulated by Phytophthora palmivora: a model system for genomic studies of compatible Phytophthora-plant interactions. Trop Plant Biol 2:84–97CrossRefGoogle Scholar
  147. Pourrahim R, Farzadfar S, Golnaraghi AR, Shahraeen N (2003) First report of Papaya ringspot virus on papaya in Iran. Disease notes. Plant Disease 87:1148CrossRefGoogle Scholar
  148. Preisig-Müller R, Schwekendiek A, Brehm I, Reif HJ, Kindl H (1999) Characterization of a pine multigene family containing elicitor-responsive stilbene synthase genes. Plant Mol Biol 39:221–229PubMedCrossRefGoogle Scholar
  149. Redman RS, Ranson JC, Rodriguez RJ (1999) Conversion of the pathogenic fungus Colletotrichum magna to a nonpathogenic, endophytic mutualist by gene disruption. Mol Plant Microbe Interact 12:969–975CrossRefGoogle Scholar
  150. Register JC 3rd, Beachy RN (1988) Resistance to TMV in transgenic plants results from interference with an early event in infection. Virology 166:524–532PubMedCrossRefGoogle Scholar
  151. Rimando AM, Pan Z, Polashock JJ, Dayan FE, Mizuno CS, Snook ME, Liu CJ, Baerson SR (2012) In planta production of the highly potent resveratrol analogue pterostilbene via stilbene synthase and O-methyltransferase co-expression. Plant Biotechnol J 10(3):269–283PubMedCrossRefGoogle Scholar
  152. Roberts PD, Trujillo E (1998) First report of Phytophthora nicotianae causing leaf blight, fruit rot, and root rot of papaya in American Samoa. Disease notes. Plant Disease 82:712CrossRefGoogle Scholar
  153. Rodriguez-Alvarado G, Fernandez-Pavìa SP, Geraldo-Verdugo JA, Landa-Hernandez L (2001) Pythium aphanidermatum causing collar rot on papaya in Baja California Sur, Mexico. Disease notes. Plant Disease 85:444CrossRefGoogle Scholar
  154. Rodriguez-Romero AS, Azcón R, Jaizme-Vega MDC (2011) Early mycorrhization of two tropical crops, papaya (Carica papaya L.) and pineapple [Ananas comosus (L.) Merr.], reduces the necessity of P fertilization during the nursery stage. Fruits 66:3–10CrossRefGoogle Scholar
  155. Samappito S, Page JE, Schmidt J, De-Eknamkul W, Kutchan TM (2003) Aromatic and pyrone polyketides synthesized by a stilbene synthase from Rheum tataricum. Phytochemistry 62:313–323PubMedCrossRefGoogle Scholar
  156. Sanchez M, Dianese JC, Costa CL (1991) Factors affecting the damage by Phoma caricae-papayae on papaya fruits, and detection of resistance to the fungus in Carica gaudotiana. Fitopatol Bras 16:121–129Google Scholar
  157. Sanford JC, Johnston SA (1985) The concept of parasite-derived resistance-Deriving resistance genes from the parasite’s own genome. J Theor Biol 113:395–405CrossRefGoogle Scholar
  158. Schanz S, Schröder G, Schröder J (1992) Stilbene synthase from Scots pine (Pinus sylvestris). Fed Eur Biochem Soc Lett 313:71–74CrossRefGoogle Scholar
  159. Scheldeman X, Motoche JPR, Van Damme V, Heyens V, Van Damme P (2003) Potential of highland papayas (Vasconcella spp.) in southern Ecuador. Lyonia 5:73–80Google Scholar
  160. Scheldeman X, Willemen L, Coppens d’Eeckenbrugge G, Romeijn-Peeters E, Restrepo MT, Motoche JR, Jiménez D, Lobo M, Medina CI, Reyes C, Rodríguez D, Ocampo JA, Van Damme P, Goetgebeur P (2007) Distribution, diversity and environmental adaptation of highland papayas (Vasconcellea spp.) in tropical and subtropical America. Biodivers Conserv 16:1867–1884CrossRefGoogle Scholar
  161. Schmidlin L, Poutaraud A, Claudel P, Mestre P, Prado E, Santos-Rosa M, Wiedemann-Merdinoglu S, Karst F, Merdinoglu D, Hugueney P (2008) A stress-inducible resveratrol O-methyltransferase involved in the biosynthesis of pterostilbene in grapevine. Plant Physiol 148:1630–1639PubMedCrossRefGoogle Scholar
  162. Schnee S, Viret O, Gindro K (2008) Role of stilbenes in the resistance of grapevine to powdery mildew. Physiol Mol Plant Pathol 72:128–133CrossRefGoogle Scholar
  163. Schöppner A, Kindl H (1984) Purification and properties of a stilbene synthase from induced cell suspension cultures of peanut. J Biol Chem 259:6806–6811PubMedGoogle Scholar
  164. Sémon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17:505–512PubMedCrossRefGoogle Scholar
  165. Serazetdinova L, Oldach KH, Lörz H (2005) Expression of transgenic stilbene synthases in wheat causes the accumulation of unknown stilbene derivatives with antifungal activity. J Plant Physiol 162:985–1002PubMedCrossRefGoogle Scholar
  166. Shahollari B, Vadassery J, Varma A, Oelmüller R (2007) A leucine-rich repeat protein is required for growth promotion and enhanced seed production mediated by the endophytic fungus Piriformospora indica in Arabidopsis thaliana. Plant J 50:1–13PubMedCrossRefGoogle Scholar
  167. Shen W, Yan P, Gao L, Pan X, Wu J, Zhou P (2010) Helper component-proteinase (HC-Pro) protein of Papaya ringspot virus interacts with papaya calreticulin. Mol Plant Pathol 11:335–346PubMedCrossRefGoogle Scholar
  168. Siar SV, Beligan GA, Drew RA, O’Brien C (2009) Final report: development of PRSV-P resistant papaya genotypes by introgression of genes from wild Carica species. Australian Centre for International Agricultural Research, CanberraGoogle Scholar
  169. Sobolev VS, Guo BZ, Holbrook CC, Lynch RE (2007) Interrelationship of phytoalexin production and disease resistance in selected peanut genotypes. J Agric Food Chem 55:2195–2200PubMedCrossRefGoogle Scholar
  170. Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM, Haberlach GT, Liu J, Kuang H, Austin-Phillips S, Buell CR, Helgeson JP, Jiang J (2003) Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc Natl Acad Sci USA 100:9128–9133PubMedCrossRefGoogle Scholar
  171. Sparvoli F, Martin C, Scienza A, Gavazzi G, Tonelli C (1994) Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Mol Biol 24:743–755PubMedCrossRefGoogle Scholar
  172. Stark-Lorenzen P, Nelke B, Hänßler G, Mühlbach HP, Thomzik JE (1997) Transfer of a grapevine stilbene synthase gene to rice (Oryza sativa L.). Plant Cell Rep 16:668–673CrossRefGoogle Scholar
  173. Stein E, Molitor A, Kogel KH, Waller F (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49:1747–1751PubMedCrossRefGoogle Scholar
  174. Takeguchi A, Hollyer J, Koga W, Hakoda M, Rohrbach K, Bittenbender HC, Buckley B, Friday J B, Bowen R, Manshardt R, Leary J, Teves G, Herring E, Zaleski H, Leonhardt K, Eger B (1999) History of agriculture in Hawaii. State of Hawaii Department of Agriculture.
  175. Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066PubMedCrossRefGoogle Scholar
  176. Tarnowski TLB, Ploetz RC (2010) First report of Colletotrichum capsici causing postharvest anthracnose on papaya in South Florida. Disease notes. Plant Disease 94:1065CrossRefGoogle Scholar
  177. Tennant P, Fermin G, Fitch MM, Manshardt RM, Slightom JL, Gonsalves D (2001) Papaya ringspot virus resistance of transgenic Rainbow and SunUp is affected by gene dosage, plant development, and coat protein homology. Eur J Plant Pathol 107:645–653CrossRefGoogle Scholar
  178. Tennant P, Ahmad MH, Gonsalves D (2005) Field resistance of coat protein transgenic papaya to Papaya ringspot virus in Jamaica. Plant Disease 89:841–847CrossRefGoogle Scholar
  179. Terras FR, Eggermont K, Kovaleva V, Raikhel NV, Osborn RW, Kester A, Rees SB, Torrekens S, Van Leuven F, Vanderleyden J, Cammue BPA, Broekaert WF (1995) Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7:573–588PubMedGoogle Scholar
  180. Thevissen K, Osborn RW, Acland DP, Broekaert WF (2000a) Specific binding sites for an antifungal plant defensin from Dahlia (Dahlia merckii) on fungal cells are required for antifungal activity. Mol Plant Microbe Interact 13:54–61PubMedCrossRefGoogle Scholar
  181. Thevissen K, Cammue BP, Lemaire K, Winderickx J, Dickson C, Lester RL, Ferket KK, Van Even F, Parret AH, Broekaert WF (2000b) A gene encoding a sphingolipid biosynthesis enzyme determines the sensitivity of Saccharomyces cerevisiae to an antifungal plant defensin from dahlia (Dahlia merckii). Proc Natl Acad Sci USA 97:9531–9536PubMedCrossRefGoogle Scholar
  182. Thevissen K, François IE, Takemoto JY, Ferket KK, Meert EM, Cammue BP (2003) DmAMP1, an antifungal plant defensin from dahlia (Dahlia merckii), interacts with sphingolipids from Saccharomyces cerevisiae. FEMS Microbiol Lett 226:169–173PubMedCrossRefGoogle Scholar
  183. Thomma BP, Eggermont K, Penninckx IA, Mauch-Mani B, Vogelsang R, Cammue BP, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111PubMedCrossRefGoogle Scholar
  184. Thomzik JE, Stenzel K, Stöcker R, Schreier PH, Hain R, Stahl DJ (1997) Synthesis of a grapevine phytoalexin in transgenic tomatoes (Lycopersicon esculentum Mill.) conditions resistance against Phytophthora infestans. Physiol Mol Plant Pathol 51:265–278CrossRefGoogle Scholar
  185. Tripathi S, Suzuki J, Gonsalves D (2006) Development of genetically engineered resistant papaya for Papaya ringspot virus in a timely manner-A comprehensive and successful approach. In: Ronald P (ed) Plant-pathogen interactions: methods and protocols, vol 354. The Humana Press, Totowa, pp 197–240Google Scholar
  186. Tripathi S, Suzuki JY, Ferreira SA, Gonsalves D (2008) Papaya ringspot virus-P: characteristics, pathogenicity, sequence variability and control. Mol Plant Pathol 9:269–280PubMedCrossRefGoogle Scholar
  187. Tropf S, Lanz T, Rensing SA, Schröder J, Schröder G (1994) Evidence that stilbene synthases have developed from chalcone synthases several times in the course of evolution. J Mol Evol 38:610–618PubMedCrossRefGoogle Scholar
  188. Tsay JG, Chen RS, Wang HL, Wang WL, Weng BC (2011) First report of powdery mildew caused by Erysiphe diffusa, Oidium neolycopersici, and Podosphaera xanthii on papaya in Taiwan. Disease notes. Plant Disease 95:1188CrossRefGoogle Scholar
  189. Turrini A, Sbrana C, Pitto L, Castiglione MR, Giorgetti L, Briganti R, Bracci T, Evangelista M, Nuti MP, Giovannetti M (2004a) The antifungal DM-AMP1 protein from Dahlia merckii expressed in Solanum melongena is released in root exudates and differentially affects pathogenic fungi and mycorrhizal symbiosis. New Phytol 163:393–403CrossRefGoogle Scholar
  190. Turrini A, Sbrana C, Nuti MP, Pietrangeli BM, Giovannetti M (2004b) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 266:69–75CrossRefGoogle Scholar
  191. Tuskan A, Difazio S, Jansson S, Bohlmann J, Grigoriev I et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
  192. Van der Biezen EA, Jones JD (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456PubMedCrossRefGoogle Scholar
  193. van der Vossen E, Sikkema A, Hekkert BL, Gros J, Stevens P, Muskens M, Wouters D, Pereira A, Stiekema W, Allefs S (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 36:867–882PubMedCrossRefGoogle Scholar
  194. Vega FE, Posada F, Aime MC, Pava-Ripoll M, Infante F, Rehner SA (2008) Entomopathogenic fungal endophytes. Biol Control 46:72–82CrossRefGoogle Scholar
  195. Ventura JA, Costa H, da Silva Tatagiba J (2004) Papaya diseases and integrated control. In: Naqvi SAMH (ed) Diseases of fruits and vegetables, vol II. Kluwer Academic, Dordrecht, pp 201–268Google Scholar
  196. Verma LR, Sharma RC (1999) Fungal diseases of papaya and their management. In: Verma LR, Sharma RC (eds) Diseases of horticultural crops, fruits. Indus Publishing Company, New Delhi, pp 479–492 (Chapter 21)Google Scholar
  197. Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. et sp. Nov., a new root-colonizing fungus. Mycologia 90:896–903CrossRefGoogle Scholar
  198. Vierheilig H, Alt M, Neuhaus JM, Boller T, Wiemken A (1993) Colonization of transgenic Nicotiana sylvestris plants, expressing different forms of Nicotiana tabacum chitinase, by the root pathogen Rhizoctonia solani and by mycorrhizal symbiont Glomus mosseae. Mol Plant Microbe Interact 6:261–264CrossRefGoogle Scholar
  199. Vierheilig H, Alt M, Lange J, Gut-Rella M, Wiemken A, Boller T (1995) Colonization of transgenic tobacco constitutively expressing pathogenesis-related proteins by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 61:3031–3034PubMedGoogle Scholar
  200. Vinet M, Dave SK, Specht CA, Brameld KA, Xu B, Hayward R, Fidock DA (1999) The chitinase PfCHT1 from the human malaria parasite Plasmodium falciparum lacks proenzyme and chitin-binding domains and displays unique substrate preferences. Proc Natl Acad Sci USA 96:14061–14066CrossRefGoogle Scholar
  201. Vleeshouwers VG, Raffaele S, Vossen JH, Champouret N, Oliva R, Segretin ME, Rietman H, Cano LM, Lokossou A, Kessel G, Pel MA, Kamoun S (2011) Understanding and exploiting late blight resistance in the age of effectors. Annu Rev Phytopathol 49:507–531PubMedCrossRefGoogle Scholar
  202. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391PubMedCrossRefGoogle Scholar
  203. Walton JD, Avis TJ, Alfano JR, Gijzen M, Spanu P, Hammond-Kosack K, Sánchez F (2009) Effectors, effectors et encore des effectors: the XIV international congress on molecular-plant microbe interactions, Quebec. Mol Plant Microbe Interact 22:1479–1483PubMedCrossRefGoogle Scholar
  204. Wang Y, Nowak G, Culley D, Hadwiger LA, Fristensky B (1999) Constitutive expression of pea defense gene DRR206 confers resistance to blackleg (Leptosphaeria maculans) disease in transgenic canola (Brassica napus). Mol Plant Microbe Interact 12:410–418CrossRefGoogle Scholar
  205. Wang J, Chen Z, Du J, Sun Y, Liang A (2005) Novel insect resistance in Brassica napus developed by transformation of chitinase and scorpion toxin genes. Plant Cell Rep 24:549–555PubMedCrossRefGoogle Scholar
  206. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PR (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115–118PubMedCrossRefGoogle Scholar
  207. Wilmes M, Cammue BP, Sahl HG, Thevissen K (2011) Antibiotic activities of host defense peptides: more to it than lipid bilayer perturbation. Nat Prod Rep 28:1350–1358PubMedCrossRefGoogle Scholar
  208. Yaeno T, Li H, Chaparro-Garcia A, Schornack S, Koshiba S, Watanabe S, Kigawa T, Kamoun S, Shirasu K (2011) Phosphatidylinositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc Natl Acad Sci USA 108:14682–14687PubMedCrossRefGoogle Scholar
  209. Yamazaki Y, Suh DY, Sitthithaworn W, Ishiguro K, Kobayashi Y, Shibuya M, Ebizuka Y, Sankawa U (2001) Diverse chalcone synthase superfamily enzymes from the most primitive vascular plant, Psilotum nudum. Planta 214:75–84PubMedCrossRefGoogle Scholar
  210. Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198PubMedCrossRefGoogle Scholar
  211. Yeh S-D, Gonsalves D, Wang H-L, Namba R, Chiu R-J (1988) Control of papaya ringspot virus by cross protection. Plant Disease 72:375–380CrossRefGoogle Scholar
  212. Yu CKY, Springob K, Schmidt J, Nicholson RL, Chu IK, Yip WK, Lo C (2005) A stilbene synthase gene (SbSTS1) is involved in host and nonhost defense responses in sorghum. Plant Physiol 138:393–401PubMedCrossRefGoogle Scholar
  213. Zentmyer GA (1988) Origin and distribution of four species of Phytophthora. Trans Br Mycol Soc 91:367–378CrossRefGoogle Scholar
  214. Zentmyer GA, Mitchell DJ (1985/1986) Phytophthora diseases of fruit trees in the tropics. Rev Trop Plant Pathol 2:287–309Google Scholar
  215. Zeya HI, Spitznagel JK (1963) Antibacterial and enzymatic basic proteins from leukocyte lysosomes: Separation and identification. Science 3595:1085–1087CrossRefGoogle Scholar
  216. Zhu S (2007) Evidence for myxobacterial origin of eukaryotic defensins. Immunogenetics 59:949–954PubMedCrossRefGoogle Scholar
  217. Zhu YJ, Agbayani R, Jackson MC, Tang CS, Moore PH (2004) Expression of the grapevine stilbene synthase gene VST1 in papaya provides increased resistance against diseases caused by Phytophthora palmivora. Planta 220:241–250PubMedCrossRefGoogle Scholar
  218. Zhu YJ, Agbayani R, Moore PH (2007) Ectopic expression of Dahlia merckii defensin DmAMP1 improves papaya resistance to Phytophthora palmivora by reducing pathogen vigor. Planta 226:87–97PubMedCrossRefGoogle Scholar
  219. Ziebell H, Carr JP (2010) Cross-protection: a century of mystery. Adv Virus Res 76:211–264 (Chapter 6)PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Brad W. Porter
    • 1
  • David A. Christopher
    • 1
  • Yun J. Zhu
    • 2
    Email author
  1. 1.Department of Molecular Biosciences and BioengineeringUniversity of Hawaii at ManoaHonoluluUSA
  2. 2.Hawaii Agriculture Research CenterKuniaUSA

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