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Fruit Development, Ripening and Quality Related Genes in the Papaya Genome

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Abstract

Papaya (Carica papaya L.) is the first fleshy fruit with a climacteric ripening pattern to be sequenced. As a member of the Rosids superorder in the order Brassicales, papaya apparently lacks the genome duplication that occurred twice in Arabidopsis. The predicted papaya genes that are homologous to those potentially involved in fruit growth, development, and ripening were investigated. Genes homologous to those involved in tomato fruit size and shape were found. Fewer predicted papaya expansin genes were found and no Expansin Like-B genes were predicted. Compared to Arabidopsis and tomato, fewer genes that may impact sugar accumulation in papaya, ethylene synthesis and response, respiration, chlorophyll degradation and carotenoid synthesis were predicted. Similar or fewer genes were found in papaya for the enzymes leading to volatile production than so far determined for tomato. The presence of fewer papaya genes in most fruit development and ripening categories suggests less subfunctionalization of gene action. The lack of whole genome duplication and reductions in most gene families and biosynthetic pathways make papaya a valuable and unique tool to study the evolution of fruit ripening and the complex regulatory networks active in fruit ripening.

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References

  1. Adams-Phillips L, Barry C, Kannan P, Lecercq J, Bouzayen M, Giovannoni JJ (2004) Ctr1-mediated ethylene signal transduction in tomato is encoded by a multigene family whose members display distinct regulatory features. Plant Mol Biol 54:387–404, doi:10.1023/B:PLAN.0000036371.30528.26

    Article  PubMed  CAS  Google Scholar 

  2. Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analysis reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954–2965, doi:10.1105/tpc.105.036053

    Article  PubMed  CAS  Google Scholar 

  3. Alferez F, Zacarias L (1999) Interaction between ethylene and abscisic acid in the regulation of citrus fruit maturation. In: Kanellis AK, Chang C, Klee H, Blecker AB, Pech JC, Grierson D (eds) Biology and biotechnology of the plant hormone ethylene. II. Kluwer Academic Publishers, Amsterdam, pp 183–184

    Google Scholar 

  4. Almora K, Pino JA, Hernandez M, Duarte C, Gonzalez J, Roncal E (2004) Evaluation of volatiles from ripening papaya (Carica papaya L., var. Maradol roja). Food Chem 86:127–130, doi:10.1016/j.foodchem.2003.09.039

    Article  CAS  Google Scholar 

  5. Alonso JM, Stepanova AN (2004) The ethylene signaling pathway. Science 306:1513–1515, doi:10.1126/science.1104812

    Article  PubMed  CAS  Google Scholar 

  6. Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel FM, Ecker JR (2003) Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci USA 100:2992–2997, doi:10.1073/pnas.0438070100

    Article  PubMed  CAS  Google Scholar 

  7. Andersson-Gunneras S, Hellgren JM, Bjorklund S, Regan S, Moritz T, Sundberg B (2003) Asymmetric expression of a poplar ACC oxidase controls ethylene production during gravitational induction of tension wood. Plant J 34:339–349, doi:10.1046/j.1365-313X.2003.01727.x

    Article  PubMed  CAS  Google Scholar 

  8. APG (Angiosperm Phylogeny Group) (1998) An ordinal classification for the families of flowering plants. Ann Miss Bot Gard 85:531–553, doi:10.2307/2992015

    Article  Google Scholar 

  9. APG (Angiosperm Phylogeny Group) II (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linnean Soc 141:399–436. Updated Stevens PF (2001 onwards). Angiosperm Phylogeny Website. Version 9, June 2008 http://www.mobot.org/MOBOT/research/APweb/

    Google Scholar 

  10. Armstrong GA, Hearst JE (1996) Carotenoids 2: genetics and molecular biology of carotenoid pigment biosynthesis. FASEB J 10:228–237

    PubMed  CAS  Google Scholar 

  11. Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218, doi:10.1007/BF02672069

    Article  CAS  Google Scholar 

  12. Asha VA, Sane AP, Sane PN (2007) Multiple forms of α-expansin genes are expressed during banana fruit ripening and development. Postharvest Biol Technol 45:184–192, doi:10.1016/j.postharvbio.2007.03.003

    Article  CAS  Google Scholar 

  13. Aubourg S, Lecharny A, Bohlmann J (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Genet Genomics 267:730–745, doi:10.1007/s00438-002-0709-y

    Article  PubMed  CAS  Google Scholar 

  14. Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006a) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45:982–993, doi:10.1111/j.1365-313X.2006.02666.x

    Article  PubMed  CAS  Google Scholar 

  15. Auldridge M, McCarty DR, Klee HJ (2006b) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321, doi:10.1016/j.pbi.2006.03.005

    Article  PubMed  CAS  Google Scholar 

  16. Azarkan M, Dibiani R, Baulard C, Baeyens-Volant D (2006) Effects of mechanical wounding on Carica papaya cysteine endopeptidases accumulation and activity. Int J Biol Macromol 38:216–224, doi:10.1016/j.ijbiomac.2006.02.021

    Article  PubMed  CAS  Google Scholar 

  17. Azarkan M, Dibiani R, Goormaghtigh E, Raussens V, Baeyens-Volant D (2006) The papaya Kunitz-type trypsin inhibitor is a highly stable β-sheet glycoprotein. Biochim Biophy Acta - Proteins & Proteomics 1764:1063–1072

    Article  CAS  Google Scholar 

  18. Azarkan M, El Moussaoui A, van Wuytswinkel D, Dehon G, Looze Y (2003) Fractionation and purification of the enzymes stored in the latex of Carica papaya. J Chromat B 790:229–238, doi:10.1016/S1570-0232(03)00084-9

    Article  CAS  Google Scholar 

  19. Badillo VM (1993) Caricaceae segundo esquema. Alcance 43. Universidad Central de Venezuela, Facultad de Agronoma. p111

  20. Badillo VM (2000) Carica L. vs. Vasconcella St. Hil. (Caricaceae): con la rehabilitación de este último. Ernstia 10:74–79

    Google Scholar 

  21. Baines BS, Brocklehurst K (1982) Characterization of papaya peptidase A as a cysteine proteinase of Carica papaya L. with active center properties that differ from those of papain by using 2,2′-dipyridyl disulfide and 4-chloro-7-nitrobenzofurazan as reactivity probes. Biochem J 205:205–211

    PubMed  CAS  Google Scholar 

  22. Baldwin EA, Scott JW, Shewmaker CK, Schuch W (2000) Flavor trivia and tomato aroma: biochemistry and possible mechanisms for control of important aroma components. HortScience 35:1013–1022

    CAS  Google Scholar 

  23. Barry CS, Llop-Tous MI, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123:979–986, doi:10.1104/pp.123.3.979

    Article  PubMed  CAS  Google Scholar 

  24. Bartley GE, Ishida BK (2003) Developmental gene regulation during tomato fruit ripening and in-vitro sepal morphogenesis. BMC Plant Biology 3, 4 (http://www.biomedcentral.com/ 1471-2229/3/4)

  25. Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409, doi:10.1093/jxb/erh047

    Article  PubMed  CAS  Google Scholar 

  26. Bennett RN, Kiddle G, Wallsgrove RM (1997) Biosynthesis of benzylglucosinolate, cyanogenic glucosides and phenylpropanoids in Carica papaya. Phytochemistry 45:59–66, doi:10.1016/S0031-9422(96)00787-X

    Article  CAS  Google Scholar 

  27. Biale JB (1964) Growth, maturation, and senescence in fruits. Science 146:880–888, doi:10.1126/science.146.3646.880

    Article  PubMed  CAS  Google Scholar 

  28. Binder BM, Walker JM, Gagne JM, Emborg TJ, Hemmann G, Bleecker AB, Vierstra RD (2007) The Arabidopsis EIN3 binding F-Box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 19:509–523, doi:10.1105/tpc.106.048140

    Article  PubMed  CAS  Google Scholar 

  29. Bocock PN, Morse AM, Dervinis C, Davis JM (2008) Evolution and diversity of invertase genes in Populus trichocarpa. Planta 227:565–576, doi:10.1007/s00425-007-0639-3

    Article  PubMed  CAS  Google Scholar 

  30. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133, doi:10.1073/pnas.95.8.4126

    Article  PubMed  CAS  Google Scholar 

  31. Booker J, Auldridge ME, Wills S, McCarty DR, Klee HJ, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1–20, doi:10.1016/j.cub.2004.06.061

    Article  CAS  Google Scholar 

  32. Bowers JE, Chapman AB, Rong J, Paterson AH (2003) Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438, doi:10.1038/nature01521

    Article  PubMed  CAS  Google Scholar 

  33. Bramley P, Teulieres C, Blain I, Bird C, Schuch W (1992) Biochemical characterization of transgenic tomato plants in which carotenoid synthesis has been inhibited through the expression of antisense RNA to pTOM5. Plant J 2:343–349, doi:10.1111/j.1365-313X.1992.00343.x

    Article  CAS  Google Scholar 

  34. Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11:2203–2216

    Article  PubMed  CAS  Google Scholar 

  35. Bruinsma J, Paull RE (1984) Respiration during postharvest development of soursop fruit. Annona muricata L. Plant Physiol 76:131–138

    Article  PubMed  CAS  Google Scholar 

  36. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187, doi:10.1016/0092-8674(91)90418-X

    Article  PubMed  CAS  Google Scholar 

  37. Burdock GA (2002) Fenaroli’s handbook of flavor ingredients, 4th edn. CRC Press, Boca Raton

    Google Scholar 

  38. Burg SP, Burg EA (1965) Relationship between ethylene production and ripening in bananas. Bot Gaz 126:200–204, doi:10.1086/336320

    Article  CAS  Google Scholar 

  39. Büttner M (2007) The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Lett 581:2318–2324, doi:10.1016/j.febslet.2007.03.016

    Article  PubMed  CAS  Google Scholar 

  40. Cano MP, De Ancos B, Lobo G (1995) Peroxidase and polyphenoloxidase activities in papaya during postharvest ripening and after freezing-thawing. J Fd Sci 60:815–820, doi:10.1111/j.1365-2621.1995.tb06236.x

    Article  CAS  Google Scholar 

  41. Cano MP, Lobo MG, De Ancos B, Galeazzi MAM (1996) Polyphenol oxidase from Spanish hermaphrodite and female papaya fruits (Carica papaya Cv. Sunrise, Solo Group). J Agric Food Chem 44:3075–3079, doi:10.1021/jf960119k

    Article  CAS  Google Scholar 

  42. Caspari T, Will A, Opekarova M, Sauer N, Tanner W (1994) Hexose/H + symporters in lower and higher plants. J Exp Biol 196:483–491

    PubMed  CAS  Google Scholar 

  43. Chan HT (1979) Sugar composition of papaya during development. HortScience 14:140–141

    CAS  Google Scholar 

  44. Chan HT Jr, Flath RA, Forrey RR, Cavaletto CG, Nakayama TOM, Brekke JE (1973) Development of off-odors and off-flavors in papaya puree. J Agric Food Chem 21:566–570, doi:10.1021/jf60188a018

    Article  CAS  Google Scholar 

  45. Chan YK, Paull RE (2007) Papaya Carica papaya L., Caricaceae. In: Janick J, Paull RE (eds) Encyclopedia of Fruit and Nuts. CABI, Wallingford, United Kingdom, pp 237–247

    Google Scholar 

  46. Chen NM, Paull RE (1985) Development and prevention of chilling injury in papaya fruit. J Am Soc Hortic Sci 111:639–643

    Google Scholar 

  47. Chen NJ, Paull RE (2003) Endoxylanase expressed during papaya fruit ripening: purification, cloning and characterization. Funct Plant Biol 30:433–441, doi:10.1071/FP02208

    Article  CAS  Google Scholar 

  48. Chevalier T, De Rigal D, Mbeguie-A-Mbeguie D, Gauillard F, Richard-Forget F, Fils-Lycaon BR (1999) Molecular cloning and characterization of apricot fruit polyphenol oxidase. Plant Physiol 119:1261–1269, doi:10.1104/pp.119.4.1261

    Article  PubMed  CAS  Google Scholar 

  49. Choi D, Cho DT, Lee Y (2006) Expansins: expanding importance in plant growth and development. Physiol Plant 126:511–518

    CAS  Google Scholar 

  50. Claros MG, Vincens P (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241:779–786, doi:10.1111/j.1432-1033.1996.00779.x

    Article  PubMed  CAS  Google Scholar 

  51. Claus H (2004) Laccases: structure, reactions, distribution. Micron 35:93–96, doi:10.1016/j.micron.2003.10.029

    Article  PubMed  CAS  Google Scholar 

  52. Cong B, Tanksley SD (2006) FW2.2 and cell cycle control in developing tomato fruit: a possible example of gene co-option in the evolution of a novel organ. Plant Mol Biol 62:867–880, doi:10.1007/s11103-006-9062-6

    Article  PubMed  CAS  Google Scholar 

  53. Considine MJ, Daley DO, Whelan J (2001) The expression of alternative oxidase and uncoupling protein during fruit ripening in Mango. Plant Physiol 126:1619–1629, doi:10.1104/pp.126.4.1619

    Article  PubMed  CAS  Google Scholar 

  54. Considine MJ, Holtzapffel RC, Day DA, Whelan J, Millar AH (2002) Molecular distinction between alternative oxidase from monocots and dicots. Plant Physiol 129:949–953, doi:10.1104/pp.004150

    Article  PubMed  CAS  Google Scholar 

  55. Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–296, doi:10.1104/pp.124.1.285

    Article  PubMed  CAS  Google Scholar 

  56. Cosgrove DJ (2007) Expansin Home Page. http://www.bio.psu.edu/expansins/index.htm. Cited 22 March 2008

  57. Croteau R, Lutchan TM, Lewis NG (2000) Natural Products (secondary metabolites). In: Biochemistry and Molecular Biology of Plants, Buchanan B, Gruissem W, Jones R (eds.) Rockville MD, Amer. Soc. Plant Physiol. pp1250–1318

  58. Cunningham FX Jr, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583, doi:10.1146/annurev.arplant.49.1.557

    Article  PubMed  CAS  Google Scholar 

  59. D’Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9:331–340, doi:10.1016/j.pbi.2006.03.016

    Article  PubMed  CAS  Google Scholar 

  60. Devitt LC, Sawbridge T, Holton TA, Mitchelson K, Dietzgen RG (2006) Discovery of genes associated with fruit ripening in Carica papaya using expressed sequence tags. Plant Sci 170:356–363, doi:10.1016/j.plantsci.2005.09.003

    Article  CAS  Google Scholar 

  61. Dibley SJ, Gear ML, Xiao Y, Rosche EG, Offler CE, McCurdy DW, Patrick JW (2005) Temporal and spatial expression of hexose transporters in developing tomato (Lycopersicon esculentum) fruit. Funct Plant Biol 32:777–785, doi:10.1071/FP04224

    Article  CAS  Google Scholar 

  62. Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902, doi:10.1104/pp.104.049981

    Article  PubMed  CAS  Google Scholar 

  63. Ehlting J, Mattheus N, Aeschliman DS, Li E, Hamberger B, Cullis IF, Zhuang J, Kaneda M, Mansfield SD, Samuels L, Ritland K, Ellis B, Bohlmann J, Douglas CJ (2005) Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J 42:618–640, doi:10.1111/j.1365-313X.2005.02403.x

    Article  PubMed  CAS  Google Scholar 

  64. Elhafez D, Murcha MW, Clifton R, Soole KL, Day DA, Whelan J (2006) Characterization of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant Cell Physiol 47:43–54, doi:10.1093/pcp/pci221

    Article  PubMed  CAS  Google Scholar 

  65. El Moussaoui A, Nijs M, Paul C, Wintjens R, Vincentelli J, Azarkan M, Looze Y (2001) Revisiting the enzymes stored in the laticifers of Carica papaya in the context of their possible participation in the plant defence mechanism. Cell Mol Life Sci 58:556–570, doi:10.1007/PL00000881

    Article  PubMed  Google Scholar 

  66. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    Article  PubMed  CAS  Google Scholar 

  67. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016, doi:10.1006/jmbi.2000.3903

    Article  PubMed  CAS  Google Scholar 

  68. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protocols 2:953–971, doi:10.1038/nprot.2007.131

    Article  CAS  Google Scholar 

  69. Fellman JK, Miller TW, Mattison DS, Mattheis JP (2000) Factors that influence biosynthesis of volatile flavor compounds in apple fruits. HortScience 35:1026–1033

    CAS  Google Scholar 

  70. Flath RA, Forrey RR (1977) Volatile components of papaya (Carica papaya L., Solo variety). J Agric Food Chem 25:103–109, doi:10.1021/jf60209a051

    Article  CAS  Google Scholar 

  71. Flath RA, Light DM, Jang EB, Mon TR, John JO (1990) Headspace examination of volatile emissions form ripening papaya (Carica papaya L., Solo variety). J Agric Food Chem 38:1060–1063, doi:10.1021/jf00094a032

    Article  CAS  Google Scholar 

  72. Franco MRB, Rodriguez ADB (1993) Volatile components of two pawpaw cultivars. Arq Biol Tecnol 36:613–632

    CAS  Google Scholar 

  73. Fraser PD, Truesdale MR, Bird CR, Schuch W, Bramley PM (1994) Carotenoid biosynthesis during tomato fruit development. Plant Physiol 105:405–413

    PubMed  CAS  Google Scholar 

  74. Fraser PD, Kiano JW, Truesdale MR, Schuch W, Bramley PM (1999) Phytoene synthase-2 enzyme activity in tomato does not contribute to carotenoid synthesis in ripening fruit. Plant Mol Biol 40:687–698, doi:10.1023/A:1006256302570

    Article  PubMed  CAS  Google Scholar 

  75. Frary A, Nesbitt C, Frary A, Grandillo S, van der Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88, doi:10.1126/science.289.5476.85

    Article  PubMed  CAS  Google Scholar 

  76. Frank HA, Brudvig GW (2004) Redox functions of carotenoids in photosynthesis. Biochem 43:8607–8615, doi:10.1021/bi0492096

    Article  CAS  Google Scholar 

  77. Fridman M, Zamir D (2003) Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis. Plant Physiol 131:603–609, doi:10.1104/pp.014431

    Article  PubMed  CAS  Google Scholar 

  78. Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plant by conserved MAPKK kinase. Proc Natl Acad Sci USA 98:373–378, doi:10.1073/pnas.011405198

    Article  PubMed  CAS  Google Scholar 

  79. Gear ML, McPhillips ML, Patrick JW, McCurdy DW (2000) Hexose transporters of tomato: molecular cloning, expression analysis and functional characterization. Plant Mol Biol 44:687–697, doi:10.1023/A:1026578506625

    Article  PubMed  CAS  Google Scholar 

  80. Geisler DA, Broselid C, Hederstedt L, Rasmusson AG (2007) Ca2 + -binding and Ca2 + -independent respiratory NADH and NADPH dehydrogenases of Arabidopsis thaliana. J Biol Chem 282:28455–28464, doi:10.1074/jbc.M704674200

    Article  PubMed  CAS  Google Scholar 

  81. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:S170–S180, doi:10.1105/tpc.019158

    Article  PubMed  CAS  Google Scholar 

  82. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194, doi:10.1038/nature07271

    Article  PubMed  CAS  Google Scholar 

  83. Grubb CD, Abel S (2006) Glucosinolate metabolism and its control. Trends Plant Sci 11:89–100, doi:10.1016/j.tplants.2005.12.006

    Article  PubMed  CAS  Google Scholar 

  84. Grubb CD, Zipp BJ, Ludwig-Müller J, Masuno MN, Molinski TF, Abel S (2004) Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J 40:893–908, doi:10.1111/j.1365-313X.2004.02261.x

    Article  PubMed  CAS  Google Scholar 

  85. Guo AY, He K, Liu D, Bai SN, Gu XC, Wei LP, Luo JC (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21:2568–2569, doi:10.1093/bioinformatics/bti334

    Article  PubMed  CAS  Google Scholar 

  86. Gussman CD, Goffredz JC, Gianfagna TJ (1993) Ethylene production and fruit-softening rates in several apple fruit ripening variants. HortScience 28:135–137

    Google Scholar 

  87. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  88. Hall BP, Shakeel SN, Schaller GE (2007) Ethylene receptors: Ethylene perception and signal transduction. J Plant Growth Regul 26:118–130, doi:10.1007/s00344-007-9000-0

    Article  CAS  Google Scholar 

  89. Hamberger B, Ellis M, Friedmann M, de Azevedo Souza C, Barbazuk B, Douglas CJ (2007) Genome-wide analysis of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Ozyza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can J Bot 85:1182–1201, doi:10.1139/B07–098

    Article  CAS  Google Scholar 

  90. Henry MF, Nyns EJ (1975) Cyanide-insensitive respiration. An alternative mitochondrial pathway. Subcell Biochem 4:1–65

    PubMed  CAS  Google Scholar 

  91. Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218, doi:10.1016/S1369-5266(00)00163-1

    Article  PubMed  CAS  Google Scholar 

  92. Hortensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77, doi:10.1146/annurev.arplant.57.032905.105212

    Article  PubMed  CAS  Google Scholar 

  93. Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271, doi:10.1016/S0092-8674(00)81425-7

    Article  PubMed  CAS  Google Scholar 

  94. Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR, Meyerowitz EM (1998) EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10:1321–1332

    Article  PubMed  CAS  Google Scholar 

  95. Jansen EF, Balls AK (1941) Chymopapain: a new crystalline proteinase from papaya latex. J Biol Chem 137:459–460

    CAS  Google Scholar 

  96. Ji X, Van den Ende W, Van Laere A, Cheng S, Bennett J (2005) Structure, evolution, and expression of the two invertase gene families of rice. J Mol Evol 60:615–634, doi:10.1007/s00239-004-0242-1

    Article  PubMed  CAS  Google Scholar 

  97. Kaminaga Y, Schnepp J, Peel G, Kish CM, Ben-Nissan G, Weiss D, Orlova I, Lavie O, Rhodes D, Wood K, Porterfield DM, Cooper AJL, Schloss JV, Pichersky E, Vainstein A, Dudareva N (2007) Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J Biol Chem 281:23357–23366, doi:10.1074/jbc.M602708200

    Article  CAS  Google Scholar 

  98. Katague DB, Kirch ER (1965) Chromatographic analysis of volatile components of papaya fruits. J Pharm Sci 54:891–894, doi:10.1002/jps.2600540616

    Article  PubMed  CAS  Google Scholar 

  99. Kevany B, Taylor M, Dal Cin V, Klee HJ (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J 51:458–467, doi:10.1111/j.1365-313X.2007.03170.x

    Article  PubMed  CAS  Google Scholar 

  100. Klee H, Tieman D (2002) The tomato ethylene receptor gene family: form and function. Physiol Plant 115:336–341, doi:10.1034/j.1399-3054.2002.1150302.x

    Article  PubMed  CAS  Google Scholar 

  101. Kliebenstein DJ, Kroymann J, Mitchell-Olds T (2005) The glucosinolate-myrosinase system in an ecological and evolutionary context. Curr Opin Plant Biol 8:264–271, doi:10.1016/j.pbi.2005.03.002

    Article  PubMed  CAS  Google Scholar 

  102. Komatsu A, Moriguchi T, Koyama K, Omura M, Akihama T (2002) Analysis of sucrose synthase genes in citrus suggests different roles and phylogenetic relationships. J Exp Bot 53:61–71, doi:10.1093/jexbot/53.366.61

    Article  PubMed  CAS  Google Scholar 

  103. Ku HM, Doganlar S, Chen KY, Tanksley S (1999) The genetic basis of pear-shaped tomato fruit. TAG 9:844–850, doi:10.1007/s001220051304

    Google Scholar 

  104. Ku HM, Grandillo G, Tanksley SD (2000a) fs8.1, a major QTL, sets the pattern of tomato carpel shape well before anthesis. TAG 101:873–878, doi:10.1007/s001220051555

    Article  CAS  Google Scholar 

  105. Ku HM, Vision T, Liu JP, Tanksley SD (2000b) Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc Natl Acad Sci USA 97:9121–9126, doi:10.1073/pnas.160271297

    Article  PubMed  CAS  Google Scholar 

  106. Kunieda T, Amano T, Shioi Y (2005) Search for chlorophyll degradation enzyme, Mg-dechelatase, from extracts of Chenopodium album with native and artificial substrates. Plant Sci 169:177–183, doi:10.1016/j.plantsci.2005.03.010

    Article  CAS  Google Scholar 

  107. Langenkamper G, Fung RWM, Newcomb RD, Atkinson RG, Gardner RC, MacRae EA (2002) Sucrose phosphate synthase genes in plants belong to three different families. J Mol Evol 54:322–332

    PubMed  Google Scholar 

  108. Lelievre JM, Latche A, Jones B, Bouzayen M, Pech JC (1997) Ethylene and fruit ripening. Physiol Plant 101:727–739, doi:10.1111/j.1399-3054.1997.tb01057.x

    Article  CAS  Google Scholar 

  109. Li L, Steffens JC (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215:239–247, doi:10.1007/s00425-002-0750-4

    Article  PubMed  CAS  Google Scholar 

  110. Li Y, Darley CP, Ongaro V, Fleming A, Schipper O, Baldauf SL, McQueen-Mason SJ (2002) Plant expansins are a complex multigene family with an ancient evolutionary origin. Plant Physiol 128:854–864, doi:10.1104/pp.010658

    Article  PubMed  CAS  Google Scholar 

  111. Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47–65, doi:10.1146/annurev.arplant.50.1.47

    Article  PubMed  CAS  Google Scholar 

  112. Lichtenthaler HK (2000) Non-mevalonate isoprenoid biosynthesis: Enzymes, genes and inhibitors. Biochem Soc Trans 28:785–789, doi:10.1042/BST0280785

    Article  PubMed  CAS  Google Scholar 

  113. Lippman Z, Tanksley SD (2001) Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small-fruited wild species Lycopersicon pimpinellifolium and L. esculentum var. Giant Heirloom. Genetics 158:413–422

    PubMed  CAS  Google Scholar 

  114. Liu J, Eck JV, Cong B, Tanksley SD (2002) A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc Natl Acad Sci USA 99:13302–13306, doi:10.1073/pnas.162485999

    Article  PubMed  CAS  Google Scholar 

  115. López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874, doi:10.1111/j.1469-8137.2008.02406.x

    Article  PubMed  CAS  Google Scholar 

  116. Lyons E, Pedersen B, Kane J, Freeling M (2008) The value of nonmodel genomes and an example using SynMap within CoGe to dissect the hexaploidy that predates the Rosids. Trop Plant Biol 1: (this issue)

  117. Mach JM, Castillo AR, Hoogstraten R, Greenberg JT (2001) The Arabidopsis accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc Natl Acad Sci USA 98:771–776, doi:10.1073/pnas.021465298

    Article  PubMed  CAS  Google Scholar 

  118. Mackenzie S, McIntosh L (1999) Higher plant mitochondria. Plant Cell 11:571–586

    Article  PubMed  CAS  Google Scholar 

  119. MacLeod AJ, Pieris NM (1983) Volatile components of papaya (Carica papaya L.) with particular reference to glucosinolate products. J Agric Food Chem 31:1005–1008, doi:10.1021/jf00119a021

    Article  CAS  Google Scholar 

  120. Madden TL, Tatusov RL, Zhang J (1996) Application of network BLAST server. Methods Enzymol 266:131–141, doi:10.1016/S0076-6879(96)66011-X

    Article  PubMed  CAS  Google Scholar 

  121. Manenoi A, Bayogan ERV, Thumdee S, Paull RE (2007) Utility of 1-methylcyclopropene as a papaya postharvest treatment. Postharvest Biol Technol 44:55–62, doi:10.1016/j.postharvbio.2006.11.005

    Article  CAS  Google Scholar 

  122. Manenoi A, Paull RE (2007) Papaya fruit softening, endoxylanase gene expression, protein and activity. Physiol Plant 131:470–480, doi:10.1111/j.1399-3054.2007.00967.x

    Article  PubMed  CAS  Google Scholar 

  123. Marchler-Bauer A et al (2005) CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res 33:192–196, doi:10.1093/nar/gki069

    Article  Google Scholar 

  124. Martin T, Frommer WB, Salanoubat M, Willmitzer L (1993) Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J 4:367–377, doi:10.1046/j.1365-313X.1993.04020367.x

    Article  PubMed  CAS  Google Scholar 

  125. Marusek CM, Trobaugh NM, Flurkey WH, Inlow JK (2006) Comparative analysis of polyphenol oxidase from plant and fungal species. J Inorg Biochem 100:108–123, doi:10.1016/j.jinorgbio.2005.10.008

    Article  PubMed  CAS  Google Scholar 

  126. Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochem 60:551–565, doi:10.1016/S0031-9422(02)00171-1

    Article  CAS  Google Scholar 

  127. McCaig BC, Meagher RB, Dean JFD (2005) Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana. Planta 221:619–636, doi:10.1007/s00425-004-1472-6

    Article  PubMed  CAS  Google Scholar 

  128. McDonald AE (2008) Alternative oxidase: an inter-kingdom perspective on the function and regulation of this broadly distributed ‘cyanide-resistant’ terminal oxidase. Funct Plant Biol 35:535–552, doi:10.1071/FP08025

    Article  CAS  Google Scholar 

  129. McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall expansion in plants. Plant Cell 4:1425–1433

    Article  PubMed  CAS  Google Scholar 

  130. Melo AMP, Bandeiras TM, Teixeira M (2004) New Insights into Type II NAD(P)H:quinone oxidoreductases. Microbiol Mol Biol Rev 68:603–616, doi:10.1128/MMBR.68.4.603-616.2004

    Article  PubMed  CAS  Google Scholar 

  131. Michalecka AM, Svensson AS, Johansson FI, Agius SC, Johanson U, Brennicke A, Binder S, Rasmusson AG (2003) Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol 133:642–652, doi:10.1104/pp.103.024208

    Article  PubMed  CAS  Google Scholar 

  132. Ming R et al (2008) Genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996, doi:10.1038/nature06856

    Article  PubMed  CAS  Google Scholar 

  133. Moore AL, Albury MS, Crichton PG, Affourtit C (2002) Function of the alternative oxidase: is it still a scavenger? Trends Plant Sci 7:478–481, doi:10.1016/S1360-1385(02)02366-X

    Article  PubMed  CAS  Google Scholar 

  134. Morshidi M (1996) Genetic variability in Carica papaya and related species. Dissertation, University of Hawaii at Manoa

  135. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and Rice. Plant Physiol 140:411–432, doi:10.1104/pp.105.073783

    Article  PubMed  CAS  Google Scholar 

  136. Nakasone HY, Paull RE (1998) Tropical Fruits. CAB International, Wallingford, England

    Google Scholar 

  137. Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, of 1-aminocyclopropane-1-carboxylase oxidase and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118:1295–1305, doi:10.1104/pp.118.4.1295

    Article  PubMed  CAS  Google Scholar 

  138. Newcomb RD, Crowhurst RN, Gleave AP, Rikkerink EHA, Allan AC, Beuning LL, Bowen JH, Kim E, Jamieson R, Janssen BJ, Laing WA, McArtney S, Nain B, Ross GS, Snowden KC, Souleyre EJF, Walton EF, Yauk YK (2006) Analyses of expressed sequence tags from Apple. Plant Physiol 141:147–166, doi:10.1104/pp.105.076208

    Article  PubMed  Google Scholar 

  139. Noordermeer MA, Veldink GA, Vliegenthart JFG (1999) Alfalfa contains substantial hydroperoxide lyase activity and a 3Z:2E-enal isomerase. FEBS Lett 443:201–204, doi:10.1016/S0014-5793(98)01706-2

    Article  PubMed  CAS  Google Scholar 

  140. Oberg KA, Ruysschaert JM, Azarkan M, Smolders N, Zerhouni S, Wintjens R, Amrani A, Looze Y (1998) Papaya glutamine cyclase, a plant enzyme highly resistant to proteolysis, adopts an all-b conformation. Eur J Biochem 258:214–222, doi:10.1046/j.1432-1327.1998.2580214.x

    Article  PubMed  CAS  Google Scholar 

  141. Ouaked F, Rozhon W, Lecourieux D, Hirt H (2003) A MAPK pathway mediates ethylene signaling in plants. EMBO J 22:1282–1288, doi:10.1093/emboj/cdg131

    Article  PubMed  CAS  Google Scholar 

  142. Paquette SM, Bak S, Feyereisen R (2000) Intron-exon organization and phylogeny in a large superfamily, the paralogous cytochrome P450 genes of Arabidopsis thaliana. DNA Cell Biol 19:307–317, doi:10.1089/10445490050021221

    Article  PubMed  CAS  Google Scholar 

  143. Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochem 65:1879–1893, doi:10.1016/j.phytochem.2004.06.023

    Article  CAS  Google Scholar 

  144. Patrick JW (1997) Phloem unloading: sieve element unloading and post-sieve element transport. Annu Rev Plant Physiol Plant Mol Biol 48:191–222, doi:10.1146/annurev.arplant.48.1.191

    Article  PubMed  CAS  Google Scholar 

  145. Paull RE (1993) Pineapple and Papaya. In: Seymour G, Taylor J, Tucker G (eds) Biochemistry of Fruit Ripening. Chapman & Hall, London, United Kingdom, pp 291–323

    Google Scholar 

  146. Paull RE, Chen NJ (1983) Postharvest variation in cell wall-degrading enzymes of papaya (Carica papaya L.) during fruit ripening. Plant Physiol 72:382–385

    Article  PubMed  CAS  Google Scholar 

  147. Paull RE, Chen NJ (1989) Waxing and plastic wraps influence water loss from papaya fruit during storage and ripening. J Am Soc Hortic Sci 114:937–942

    Google Scholar 

  148. Phillips DR, Rasbery JM, Bartel B, Matsuda SPT (2006) Biosynthetic diversity in plant triterpene cyclization. Curr Opin Plant Biol 9:305–314, doi:10.1016/j.pbi.2006.03.004

    Article  PubMed  CAS  Google Scholar 

  149. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243, doi:10.1016/S1369-5266(02)00251-0

    Article  PubMed  CAS  Google Scholar 

  150. Picton S, Gray J, Barton S, AbuBakar U, Lowe A, Grierson D (1993) cDNA cloning and characterisation of nove1 ripening-related mRNAs with altered patterns of accumulation in the ripening inhibitor (rin) tomato ripening mutant. Plant Mol Biol 23:193–207, doi:10.1007/BF00021431

    Article  PubMed  CAS  Google Scholar 

  151. Pino JA, Almora K, Marbot R (2003) Volatile components of papaya (Carica papaya L., Maradol variety) fruit. Flavour Fragrance J 18:492–496, doi:10.1002/ffj.1248

    Article  CAS  Google Scholar 

  152. Piotrowski M, Schemenewitz A, Lopukhina A, Müller A, Janowitz T, Weiler EW, Oecking C (2004) Desulfoglucosinolate sulfotransferases from Arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure. J Biol Chem 279:50717–50725, doi:10.1074/jbc.M407681200

    Article  PubMed  CAS  Google Scholar 

  153. Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I (2006) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12:29–36, doi:10.1016/j.tplants.2006.11.006

    Article  PubMed  CAS  Google Scholar 

  154. Pruzinska A, Anders I, Aubry S, Schenk A, Tapernoux-Luthe E, Muller T, Krautler B, Hortensteiner S (2007) In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell 19:369–387, doi:10.1105/tpc.106.044404

    Article  PubMed  CAS  Google Scholar 

  155. Qiu YX, Nishina MS, Paull RE (1995) Papaya fruit growth, calcium uptake and fruit ripening. J Am Soc Hortic Sci 120:246–253

    Google Scholar 

  156. Raes J, Rohde A, Chrisrensen JH, Van der Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071, doi:10.1104/pp.103.026484

    Article  PubMed  CAS  Google Scholar 

  157. Rask L, Andréasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J (2000) Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol 42:93–113, doi:10.1023/A:1006380021658

    Article  PubMed  CAS  Google Scholar 

  158. Rasmusson AG, Svensson AS, Knoop V, Grohmann L, Brennicke A (1999) Homologues of yeast and bacterial rotenone-insensitive NADH dehydrogenases in higher eukaryotes: two enzymes are present in potato mitochondria. Plant J 20:79–87, doi:10.1046/j.1365-313X.1999.00576.x

    Article  PubMed  CAS  Google Scholar 

  159. Roberts TH, Fredlund KM, Moller IM (1995) Direct evidence for the presence of two external NAD(P)H dehydrogenases coupled to the electron transport chain in plant mitochondria. FEBS Lett 373:307–309, doi:10.1016/0014-5793(95)01059-N

    Article  PubMed  CAS  Google Scholar 

  160. Rodman JE, Karol KG, Price RA, Sytsma KJ (1996) Molecules, morphology, and Dahlgren’s expanded order Capparales. Syst Bot 21:289–307, doi:10.2307/2419660

    Article  Google Scholar 

  161. Rodman JE, Soltis PS, Soltis DE, Sytsma KJ, Karol KG (1998) Parallel evolution of glucosinolate biosynthesis inferred from congruent nuclear and plastid gene phylogenies. Am J Bot 85:997–1006, doi:10.2307/2446366

    Article  CAS  Google Scholar 

  162. Rodrigo MJ, Marcos JF, Alférez F, Mallent MD, Zacarías L (2003) Characterization of Pinalate, a novel Citrus sinensis mutant with a fruit-specific alteration that results in yellow pigmentation and decreased ABA content. J Exp Bot 54:727–738, doi:10.1093/jxb/erg083

    Article  PubMed  CAS  Google Scholar 

  163. Rodrigo MJ, Alquezar B, Zacarias L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). J Exp Bot 57:633–643, doi:10.1093/jxb/erj048

    Article  PubMed  CAS  Google Scholar 

  164. Rodríguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283:996–998, doi:10.1126/science.283.5404.996

    Article  PubMed  Google Scholar 

  165. Ronse de Craene LP, Haston E (2006) The systematic relationships of glucosinolate-producing plants and related families: a cladistic investigation based on morphological and molecular characters. Bot J Linn Soc 151:453–494, doi:10.1111/j.1095-8339.2006.00580.x

    Article  Google Scholar 

  166. Ronse de Craene LP, Smets EF (1999) The floral development and anatomy of Carica papaya (Caricaceae). Can J Bot 77:582–298, doi:10.1139/cjb-77-4-582

    Article  Google Scholar 

  167. Rose JKC, Lee HH, Bennett AB (1997) Expression of a divergent expansin gene is fruit-specific and ripening regulated. Proc Natl Acad Sci USA 94:5955–5960, doi:10.1073/pnas.94.11.5955

    Article  PubMed  CAS  Google Scholar 

  168. Rose JKC, Cosgrove DJ, Albersheim P, Darvill AG, Bennett AB (2000) Detection of expansin proteins and activity during tomato fruit ontogeny. Plant Physiol 123:1583–1592, doi:10.1104/pp.123.4.1583

    Article  PubMed  CAS  Google Scholar 

  169. Rossetto MRM, Oliveira do Nascimento JR, Purgatto E, Fabi JP, Lajolo FM, Cordenunsi BR (2008) Benzylglucosinolate, benzylisothiocyanate, and myrosinase activity in papaya fruit during development and ripening. J Agric Food Chem 56:9592–9599, doi:10.1021/jf801934x

    Article  PubMed  CAS  Google Scholar 

  170. Roth I, Clausnitzer I (1972) Desarrollo y anatomía del fruto y la semilla de Carica papaya L. (Lechosa). Acta Bot Venez 7:187–206

    Google Scholar 

  171. Saito N, Nei M (1987) The neighbor-joining method: a new method for constructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  172. Salas CE, Gomes MTR, Hernandez M, Lopes MTP (2008) Plant cysteine proteinases: Evaluation of the pharmacological activity. Phytochem 69:2263–2269, doi:10.1016/j.phytochem.2008.05.016

    Article  CAS  Google Scholar 

  173. Sampedro J, Lee Y, Carey RE, de Pamphilis C, Cosgrove DJ (2005) Use of genomic history to improve phylogeny and understanding of births and deaths in a gene family. Plant J 44:409–419, doi:10.1111/j.1365-313X.2005.02540.x

    Article  PubMed  CAS  Google Scholar 

  174. Sampedro J, Carey RE, Cosgrove DJ (2006) Genome histories clarify evolution of the expansin superfamily: new insights from the poplar genome and pine ESTs. J Plant Res 119:11–21, doi:10.1007/s10265-005-0253-z

    Article  PubMed  CAS  Google Scholar 

  175. Sangwanangkul P, Paull RE (2005) The role of hexose transporter in sugar accumulation of papaya fruit during maturation and ripening. Acta Hortic 740:313–316

    Google Scholar 

  176. Schaller GE, Kieber JJ (2002) Ethylene. In: Somerville C, Meyerowitz E (eds) The Arabidopsis Book. Rockville, MD: American Society of Plant Biologists

  177. Schledz M, al-Babili S, von Lintig J, Haubruck H, Rabbani S, Kleinig H, Beyer P (1996) Phytoene synthase from Narcissus pseudonarcissus: functional expression, galactolipid requirement, topological distribution in chromoplasts and induction during flowering. Plant J 10:781–792, doi:10.1046/j.1365-313X.1996.10050781.x

    Article  PubMed  CAS  Google Scholar 

  178. Schonbaum GR, Bonner WD Jr, Storey BT, Bahr JT (1971) Specific inhibition of the cyanide-insensitive respiratory pathway in plant mitochondria by hydroxamic acids. Plant Physiol 47:124–128

    Article  PubMed  CAS  Google Scholar 

  179. Schreier P, Lehr M, Heidlas J, Idstein H (1985) Volatiles from papaya (Carica papaya L.) fruit: indication of precursors of terpene compounds. A Lebensm - Unters Forsch 180:297–302

    Article  CAS  Google Scholar 

  180. Schwab W, Davidovich-Rikanati R, Lewinsohn E (2008) Biosynthesis of plant-derived flavor compounds. Plant J 54:712–732, doi:10.1111/j.1365-313X.2008.03446.x

    Article  PubMed  CAS  Google Scholar 

  181. Silva E, Lourenço EJ, Neves VA (1990) Soluble and bound peroxidase from papaya fruit. Phytochem 29:1051–1056, doi:10.1016/0031-9422(90)85401-Z

    Article  Google Scholar 

  182. Shindo T, Van Der Hoorn RAL (2008) Papain-like cysteine proteases: key players at molecular battlefields employed by both plants and their invaders. Mol Plant Pathol 9:119–125

    PubMed  CAS  Google Scholar 

  183. Simkin A, Schwartz S, Auldridge M, Taylor M, Klee HJ (2004) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles B-ionone, pseudoionone and geranylacetone. Plant J 40:882–892, doi:10.1111/j.1365-313X.2004.02263.x

    Article  PubMed  CAS  Google Scholar 

  184. Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590, doi:10.1002/pmic.200300776

    Article  PubMed  CAS  Google Scholar 

  185. Speirs J, Lee E, Holt K, Yong-Duk K, Scott NS, Loveys B, Schuch W (1998) Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiol 117:1047–1058, doi:10.1104/pp.117.3.1047

    Article  PubMed  CAS  Google Scholar 

  186. Stepanova AN, Alonso JM (2005) Ethylene Signaling Pathway. Sci STKE 276:cm3, doi:10.1126/stke.2762005cm3

  187. Storey WB (1969) Papaya (Carica papaya L.). In: Ferwerda P, Wit F (eds) Outline of perennial crop breeding in the tropics. H. Veenman & Zonen, Wageningen, pp 389–407

    Google Scholar 

  188. Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–8, doi:10.1104/pp.121.1.1

    Article  PubMed  CAS  Google Scholar 

  189. Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407, doi:10.1016/S1360-1385(99)01470-3

    Article  PubMed  Google Scholar 

  190. Takita MA, Berger IJ, Basílio-Palmieri AC, Borges KM, De Souza JM, Targon MLNP (2007) Terpene production in the peel of sweet orange fruits. Genet Mol Biol 30:841–847, doi:10.1590/S1415-47572007000500012

    Article  CAS  Google Scholar 

  191. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599, doi:10.1093/molbev/msm092

    Article  PubMed  CAS  Google Scholar 

  192. Tan SC, Lam PF (1985) Effect of gamma irradiation on PAL activity and phenolic compounds in papaya (Carica papaya L.) and mango (Mangifera inidca L.) fruits. ASEAN Food J. 1:134–136

    CAS  Google Scholar 

  193. Tang CS (1970) Benzyl isothiocyanate of papaya fruit. Phytochem 10:117–121, doi:10.1016/S0031-9422(00)90258-9

    Article  Google Scholar 

  194. Taylor MAJ, Al-sheikh M, Revell DF, Sumner IG, Connerton IF (1999) cDNA cloning and expression of Carica papaya prochymopapain isoforms in Escherichia coli. Plant Sci 145:41–47, doi:10.1016/S0168-9452(99)00068-0

    Article  CAS  Google Scholar 

  195. Theologis A, Laties GG (1978) Respiratory contribution of the alternate path during various stages of ripening in avocado and banana fruits. Plant Physiol 62:249–255

    Article  PubMed  CAS  Google Scholar 

  196. Thipyapong P, Joel DM, Steffens JC (1997) Differential expression and turnover of the tomato polyphenol oxidase gene family during vegetative and reproductive development. Plant Physiol 113:707–718

    PubMed  CAS  Google Scholar 

  197. Thipyapong P, Hunt MD, Steffens JC (2004) Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta 220:105–117, doi:10.1007/s00425-004-1330-6

    Article  PubMed  CAS  Google Scholar 

  198. Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:297–304, doi:10.1016/j.pbi.2006.03.014

    Article  PubMed  CAS  Google Scholar 

  199. Tieman DM, Loucas HM, Kim JY, Clark DG, Klee HJ (2007) Tomato phenylacetaldehyde reductases catalyze the last step in the synthesis of the aroma volatile 2-phenylethanol. Phytochem 68:2660–2669, doi:10.1016/j.phytochem.2007.06.005

    Article  CAS  Google Scholar 

  200. Tompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680, doi:10.1093/nar/22.22.4673

    Article  Google Scholar 

  201. Trentmann SM, Kende H (1995) Analysis of Arabidopsis cDNA that shows homology to the tomato E8 cDNA. Plant Mol Biol 29:161–166, doi:10.1007/BF00019127

    Article  PubMed  CAS  Google Scholar 

  202. Tsuchisaka A, Yamagami T, Alonso JM, Ecker JR, Theologis A (2007) The Arabidopsis 1-Aminocyclopropane-1-Carboxylic Acid Synthase (ACS) Gene Family. Conference Proc, 18th Internatl Conference on Arabidopsis Research, 2007. TAIR Publication:501722104

  203. Tymowska-Lalanne Z, Kreis M (1998) Expression of the Arabidopsis thaliana invertase gene family. Planta 207:259–265, doi:10.1007/s004250050481

    Article  PubMed  CAS  Google Scholar 

  204. Valerio L, De Meyer M, Penel C, Dunand C (2004) Expression analysis of the Arabidopsis peroxidase multigenic family. Phytochem 65:1331–1342, doi:10.1016/j.phytochem.2004.04.017

    Article  CAS  Google Scholar 

  205. Van Droogenbroeck B, Breyne P, Goetghebeur P, Romeijn-Peeters E, Kyndt T, Gheysen G (2002) AFLP analysis of genetic relationships among papaya and its wild relatives (Caricaceae) from Ecuador. TAG 105:289–297, doi:10.1007/s00122-002-0983-4

    Article  PubMed  CAS  Google Scholar 

  206. Vanlerberghe GC, McIntosh L (1997) Alternative oxidase: From gene to function. Annu Rev Plant Physiol Plant Mol Biol 48:703–734, doi:10.1146/annurev.arplant.48.1.703

    Article  PubMed  CAS  Google Scholar 

  207. Vogel JT, Tan B-C, McCarty DR, Klee HJ (2008) The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. J Biol Chem 283:11364–11373, doi:10.1074/jbc.M710106200

    Article  PubMed  CAS  Google Scholar 

  208. Wang W, Hall AE, O’Malley R, Bleecker AB (2003) Canonical histidine kinase activity of the transmitter domain of the ETR1 ethylene receptor from Arabidopsis is not required for signal transmission. Proc Natl Acad Sci USA 100:352–357, doi:10.1073/pnas.0237085100

    Article  PubMed  CAS  Google Scholar 

  209. Wang Y, Tang XM, Cheng ZK, Mueller L, Giovannoni J, Tanksley SD (2006) Euchromatin and pericentromeric heterochromatin: Comparative composition in the tomato genome. Genetics 172:2529–2540, doi:10.1534/genetics.106.055772

    Article  PubMed  CAS  Google Scholar 

  210. Watling JR, Robinson SA, Seymour RS (2006) Contribution of the alternative pathway to respiration during thermogenesis in flowers of the sacred lotus. Plant Physiol 140:1367–1373, doi:10.1104/pp.105.075523

    Article  PubMed  CAS  Google Scholar 

  211. Wittstock U, Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263–270, doi:10.1016/S1360-1385(02)02273-2

    Article  PubMed  CAS  Google Scholar 

  212. Wu G-L, Zhang X-Y, Zhang L-Y, Pan Q-H, Shen Y-Y, Zhang D-P (2004) Phloem unloading in developing walnut fruit is symplasmic in the seed pericarp and apoplasmic in the fleshy pericarp. Plant Cell Physiol 45:1461–1470, doi:10.1093/pcp/pch169

    Article  PubMed  CAS  Google Scholar 

  213. Wüthrich KL, Bovet L, Hunziker PE, Donnison IS, Hörtensteiner S (2000) Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism. Plant J 21:189–198, doi:10.1046/j.1365-313x.2000.00667.x

    Article  PubMed  Google Scholar 

  214. Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319:1527–1530, doi:10.1126/science.1153040

    Article  PubMed  CAS  Google Scholar 

  215. Xue J, Jørgensen M, Pihlgren U, Rask L (1995) The myrosinase gene family in Arabidopsis thaliana: gene organization, expression and evolution. Plant Mol Biol 27:911–922, doi:10.1007/BF00037019

    Article  PubMed  CAS  Google Scholar 

  216. Yabumoto K, Yamaguchi M, Jennings WG (1977) Biosynthesis of some volatiles constituents of `muskmelon Cucumis melo. Chemische Mikrobiologische Technologische Lebensraum 5:53–56

    CAS  Google Scholar 

  217. Yamagami T, Tsuchisaka A, Yamada K, Haddon WF, Harden LA, Theologis A (2003) Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J Biol Chem 278:49102–49112, doi:10.1074/jbc.M308297200

    Article  PubMed  CAS  Google Scholar 

  218. Yamamoto HY (1964) Comparison of the carotenoids in yellow- and red-fleshed Carica papaya. Nature 201:1049–1050, doi:10.1038/2011049a0

    Article  PubMed  CAS  Google Scholar 

  219. Yip WK, Dong JG, Kenny JW, Thompson GA, Yang SF (1990) Characterization and sequencing of the active site of 1-aminocyclopropane-1-carboxylate synthase. Proc Natl Acad Sci USA 87:7930–7934, doi:10.1073/pnas.87.20.7930

    Article  PubMed  CAS  Google Scholar 

  220. Yoo A, Seo YS, Jung JW, Sung SK, Kim WT, Lee W, Yang DR (2006) Lys296 and Arg299 residues in the C-terminus of MD-ACO1 are essential for a 1-aminocyclopropane-1-carboxylate oxidase enzyme activity. J Struct Biol 156:407–420, doi:10.1016/j.jsb.2006.08.012

    Article  PubMed  CAS  Google Scholar 

  221. Zeevart JAD, Creelman RA (1988) Metabolism and physiology of abscisic acid. Ann Rev Plant Physiol Plant Mo1 Biol 39:439–473

    Article  Google Scholar 

  222. Zhang L-Y, Peng Y-B, Pelleschi-Travier S, Fan Y, Lu Y-F, Lu Y-M, Gao X-P, Shen Y-Y, Delrot S, Zhang D-P (2004) Evidence for apoplasmic phloem unloading in developing apple fruit. Plant Physiol 135:574–586, doi:10.1104/pp.103.036632

    Article  PubMed  CAS  Google Scholar 

  223. Zhang X-Y, Wang X-L, Wang X-F, Xia G-H, Pan Q-H, Fan R-C, Wu F-Q, Yu X-C, Zhang D-P (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol 142:220–232, doi:10.1104/pp.106.081430

    Article  PubMed  CAS  Google Scholar 

  224. Zhou LL, Paull RE (2001) Sucrose metabolism during papaya (Carica papaya) fruit growth and ripening. J Am Soc Hortic Sci 126:351–357

    CAS  Google Scholar 

  225. Zhou L, Chen CC, Ming R, Christopher DA, Paull RE (2003) Apoplastic invertase and its enhanced expression and post-translational control during papaya fruit maturation and ripening. J Am Soc Hortic Sci 128:628–635

    CAS  Google Scholar 

  226. Zimmerman DC, Vick BA, Borg TK (1974) Intracellular distribution of hydroperoxide isomerase. Plant Physiol 53:1–4

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Tropical Plant and Soil Sciences, University of Hawaii at Manoa, Honolulu, HI, 96822, USA

    Robert E. Paull, Beth Irikura, Pingfang Wu, Helen Turano, Nancy Jung Chen & Ching Man Wai

  2. Department of Molecular Biosciences and Bioengineering, University of Hawaii at Manoa, Honolulu, HI, 96822, USA

    Andrea Blas & Gernot Presting

  3. Department of Horticulture and Landscape Architecture, Washington State University, Pullman, WA, 99164, USA

    John K. Fellman

  4. Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Andrea R. Gschwend & Ray Ming

  5. Hawaii Agriculture Research Center, Aiea, HI, 96701, USA

    Qingyi Yu

  6. Advanced Studies in Genomics, Proteomics and Bioinformatics, University of Hawaii, Honolulu, HI, 96822, USA

    Maqsudul Alam

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  1. Robert E. Paull
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Correspondence to Robert E. Paull.

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Communicated by Dr. Paul Moore

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Supplementary Table 1

List of predicted papaya expansins genes, the whole genome shotgun sequence accession number in NCBI (WGS Accession), coding sequence for amino acids (CDS), the number of introns in the nucleotide sequence (introns), amino acids (aa), whether a secretory sequence was predicted (secretory) its location (ER endoplasmic retriculum), presence of discrete portion of protein possessing its own function and the superfamily (domain), similarity in peptide sequence with another species (homology), E-value was the expectation value for homology, and the number of papaya expressed sequence tags (EST) detected of at least 500 bases and 99% identity. (DOC 49 KB)

Supplementary Table 2

Predicted papaya ethylene response factors (ERF), the whole genome shotgun sequence accession number in NCBI (WGS Accession), coding sequence for amino acids (CDS), the number of introns in the nucleotide sequence (introns), amino acids (aa), presence of discrete portion of protein possessing its own function and the superfamily (domain), similarity in peptide sequence with another species (homology), extent the sequences were invariant (identity), E-value was the expectation value for homology, and the number of papaya expressed sequence tags (EST) detected of at least 500 bases and 99% identity. (DOC 54.5 KB)

Supplementary Table 3

Latex associated genes, the whole genome shotgun sequence accession number in NCBI (WGS Accession), coding sequence for amino acids (CDS), amino acids (aa), whether a secretory sequence was predicted (secretory) its location (mito mitchondria), presence of discrete portion of protein possessing its own function and the superfamily (domain), similarity in peptide sequence with another species (homology), extent the sequences were invariant (identity), E-value was the expectation value for homology, and the number of papaya expressed sequence tags (EST) detected of at least 500 bases and 99% identity. (DOC 24 KB)

Supplementary Table 4

Predicted papaya genes for lignin biosynthesis, the whole genome shotgun sequence accession number in NCBI (WGS Accession), coding sequence for amino acids (CDS), the number of introns in the nucleotide sequence (introns), amino acids (aa), presence of discrete portion of protein possessing its own function and the superfamily (domain), similarity in peptide sequence with another species (homology), extent the sequences were invariant (identity), E-value was the expectation value for homology, and the number of papaya expressed sequence tags (EST) detected of at least 500 bases and 99% identity. (DOC 54 KB)

Supplementary Table 5

Predicted peroxidases (Peroxidase Superfamily) genes in the papaya genome, the whole genome shotgun sequence accession number in NCBI (WGS Accession), coding sequence for amino acids (CDS), amino acids (aa), similarity in peptide sequence with another species (homology), extent the sequences were invariant (identity), E-value was the expectation value for homology, and the number of papaya expressed sequence tags (EST) detected of at least 500 bases and 99% identity. (DOC 66.5 KB)

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Paull, R.E., Irikura, B., Wu, P. et al. Fruit Development, Ripening and Quality Related Genes in the Papaya Genome. Tropical Plant Biol. 1, 246–277 (2008). https://doi.org/10.1007/s12042-008-9021-2

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