Tree Genetics & Genomes

, Volume 8, Issue 6, pp 1261–1279 | Cite as

The interaction of Theobroma cacao and Moniliophthora perniciosa, the causal agent of witches’ broom disease, during parthenocarpy

  • Rachel L. Melnick
  • Jean-Philippe Marelli
  • Richard C. Sicher
  • Mary D. Strem
  • Bryan A. Bailey
Original Paper


Witches’ broom disease of Theobroma cacao L. is caused by the hemibiotrophic basidiomycete Moniliophthora perniciosa. Infection of flower cushions by M. perniciosa results in parthenocarpy. Healthy and parthenocarpic immature cacao pods were obtained from seven cacao clones. Microscopic observations of parthenocarpic pods from two clones confirmed that fruits lack viable seed. Septate mycelia colonized parthenocarpic pods, but were absent from healthy pods. Parthenocarpic pods had increased concentrations of leucine, methionine, serine, phenylalanine, and valine. Major transport metabolites sucrose and asparagine were decreased by 63 and 40 %, respectively, during parthenocarpy. M. perniciosa expressed sequence tags (ESTs) related to detoxification (MpSOD2 and MpCTA1) and nutrient acquisition (MpAS, MpAK, MpATG8, MpPLY, and MpPME) were induced in parthenocarpic pods. Most M. perniciosa ESTs related to plant hormone biosynthesis were repressed (MpGAox, MpCPS, MpDES, MpGGPPS, and MpCAO) in parthenocarpic pods. RT-qPCR analysis was conducted for 54 defense-related cacao ESTs and 93 hormone-related cacao ESTs. Specific cacao ESTs related to plant defense were induced (TcPR5, TcChi4, TcThau-ICS) while others were repressed (TcPR1, TcPR6, TcP12, and TcChiB). Cacao ESTs related to GA biosynthesis (TcGA20OX1B) were repressed in parthenocarpic pods. Cacao ESTs putatively related to maintaining cytokinin (TcCKX3 and TcCKX5) and IAA (TcGH3.17a, TcGH3.1, TcARF18) homeostasis were induced in parthenocarpic pods, suggesting an attempt to regulate cytokinin and auxin concentrations. In conclusion, M. perniciosa expresses specific sets of transcripts targeting nutrient acquisition and survival while altering the host physiology without causing significant necrosis resulting in parthenocarpy. Only a general host defense response is elicited.


Parthenocarpy Cacao Moniliophthora perniciosa Witches’ broom Plant–microbe interaction 



The USDA is an equal opportunity provider and employer.

Supplementary material

11295_2012_513_MOESM1_ESM.pdf (165 kb)
ESM 1 (PDF 164 kb)
11295_2012_513_MOESM2_ESM.pdf (179 kb)
ESM 2 (PDF 178 kb)
11295_2012_513_MOESM3_ESM.pdf (99 kb)
ESM 3 (PDF 98 kb)


  1. Aime MC, Phillips-Mora W (2005) The causal agents of witches’ broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia 97(5):1012–1022. doi: 10.3852/mycologia.97.5.1012 PubMedCrossRefGoogle Scholar
  2. Argout X, Salse J, Aury J-M, Guiltinan MJ, Droc G, Gouzy J, Allegre M, Chaparro C, Legavre T, Maximova SN, Abrouk M, Murat F, Fouet O, Poulain J, Ruiz M, Roguet Y, Rodier-Goud M, Barbosa-Neto JF, Sabot F, Kudrna D, Ammiraju JSS, Schuster SC, Carlson JE, Sallet E, Schiex T, Dievart A, Kramer M, Gelley L, Shi Z, Berard A, Viot C, Boccara M, Risterucci AM, Guignon V, Sabau X, Axtell MJ, Ma Z, Zhang Y, Brown S, Bourge M, Golser W, Song X, Clement D, Rivallan R, Tahi M, Akaza JM, Pitollat B, Gramacho K, D’Hont A, Brunel D, Infante D, Kebe I, Costet P, Wing R, McCombie WR, Guiderdoni E, Quetier F, Panaud O, Wincker P, Bocs S, Lanaud C (2011) The genome of Theobroma cacao. Nat Genet 43(2):101–108. doi: 10.1038/ng.736 PubMedCrossRefGoogle Scholar
  3. Bae H, Kim S-H, Kim MS, Sicher RC, Lary D, Strem MD, Natarajan S, Bailey BA (2008) The drought response of Theobroma cacao (cacao) and the regulation of genes involved in polyamine biosynthesis by drought and other stresses. Plant Physiol Bioch 46(2):174–188. doi: 10.1016/j.plaphy.2007.10.014 CrossRefGoogle Scholar
  4. Bae H, Sicher RC, Kim MS, Kim S-H, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60(11):3279–3295. doi: 10.1093/jxb/erp165 PubMedCrossRefGoogle Scholar
  5. Bailey BA, Bae H, Strem MD, Antúnez de Mayolo G, Guiltinan MJ, Verica JA, Maximova SN, Bowers JH (2005) Developmental expression of stress response genes in Theobroma cacao leaves and their response to Nep1 treatment and a compatible infection by Phytophthora megakarya. Plant Physiol Bioch 43(6):611–622. doi: 10.1016/j.plaphys.2005.04.006 CrossRefGoogle Scholar
  6. Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J, Samuels GJ, Choi IY, Holmes KA (2006) Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224(6):1449–1464. doi: 10.1007/s00425-006-0314-0 PubMedCrossRefGoogle Scholar
  7. Baker RP, Hasenstein KH, Zavada MS (1997) Hormonal changes after compatible and incompatible pollination in Theobroma cacao L. HortScience 32(7):1231–1234Google Scholar
  8. Bartel B (1997) Auxin biosynthesis. Ann Rev Plant Physiol 48(1):51–66. doi: 10.1146/annurev.arplant.48.1.51 CrossRefGoogle Scholar
  9. Bartrina I, Otto E, Strnad M, Werner T, Schmülling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23(1):69–80. doi: 10.1105/tpc.110.079079 PubMedCrossRefGoogle Scholar
  10. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88(1):57–63. doi: 10.1016/s0092-8674(00)81858-9 PubMedCrossRefGoogle Scholar
  11. Carter CJ, Thornburg RW (2004) Tobacco nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiol 134(1):460–469. doi: 10.1104/pp. 103.027482 PubMedCrossRefGoogle Scholar
  12. Chaves FC, Gianfagna TJ (2006) Necrotrophic phase of Moniliophthora perniciosa causes salicylic acid accumulation in infected stems of cacao. Physiol Mol Plant Pathol 69(1–3):104–108. doi: 10.1016/j.pmpp. 2007.02.003 CrossRefGoogle Scholar
  13. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833. doi: 10.1038/35081161 PubMedCrossRefGoogle Scholar
  14. Davies PJ (ed) (2010) The plant hormones: their nature, occurrence, and functions, vol 3. Plant hormones biosynthesis, signal transduction, action! Springer, Dordrecht. doi: 10.1007/978-1-4020-2686-7_1
  15. Emery NA (2006) Cytokinin and seed development. In: Basra AS (ed) Handbook of seed science and technology. Food Products, Binghamton, pp 63–94Google Scholar
  16. Evans HC, Holmes KA, Reid AP (2003) Phylogeny of the frosty pod rot pathogen of cocoa. Plant Pathol 52(4):476–485. doi: 10.1046/j.1365-3059.2003.00867.x CrossRefGoogle Scholar
  17. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12(4):599–610. doi: 10.1105/tpc.12.4.599 PubMedGoogle Scholar
  18. Goodwin PH, Li J, Jin S (2000) Evidence for sulfate derepression of an arylsulfatase gene of Colletotrichum gloeosporioides f. sp. malvae during infection of round-leaved mallow, Malva pusilla. Physiol Mol Plant Pathol 57(4):169–176. doi: 10.1006/pmpp.2000.0295 CrossRefGoogle Scholar
  19. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10(5):453–460. doi: 10.1016/j.pbi.2007.08.014 PubMedCrossRefGoogle Scholar
  20. Hebbar KP (2007) Cacao diseases: a global perspective from an industry point of view. Phytopathology 97(12):1658–1663. doi: 10.1094/PHYTO-97-12-1658 PubMedCrossRefGoogle Scholar
  21. Hegnauer H, Nyhlén LE, Rast DM (1985) Ultrastructure of native and synthetic Agaricus bisporus melanins—implications as to the compartmentation of melanogenesis in fungi. Exp Mycol 9(3):1–29. doi: 10.1016/0147-5975(85)90018-0 CrossRefGoogle Scholar
  22. Hirai MY, Yano M, Goodenowe DB, Kanaya S, Kimura T, Awazuhara M, Arita M, Fujiwara T, Saito K (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci USA 101(27):10205–10210. doi: 10.1073/pnas.0403218101 PubMedCrossRefGoogle Scholar
  23. Iriti M, Rossoni M, Borgo M, Ferrara L, Faoro F (2005) Induction of resistance to gray mold with benzothiadiazole modifies amino acid profile and increases proanthocyanidins in grape: primary versus secondary metabolism. J Agric Food Chem 53(23):9133–9139. doi: 10.1021/jf050853g PubMedCrossRefGoogle Scholar
  24. Iwahori S, Tominaga S, Yamasaki T (1988) Stimulation of fruit growth of kiwifruit, Actinidia chinensis Planch., by N-(2-chloro-4-pyridyl)-N′-phenylurea, a diphenylurea-derivative cytokinin. Sci Hort 35(1–2):109–115. doi: 10.1016/0304-4238(88)90042-8 CrossRefGoogle Scholar
  25. Jez JM, Penning TM (2001) The aldo-keto reductase (AKR) superfamily: an update. Chemi-Biol 130–132:499–525. doi: 10.1016/s0009-2797(00)00295-7 Google Scholar
  26. Katagari F, Glazebrook J (2009) Pattern discovery in expression profiling data. Curr Protoc Mol Biol 22:22.5.1–22.5.11. doi: 0.1002/0471142727.mb2205s69 Google Scholar
  27. Kerk D, Bulgrien J, Smith DW, Gribskov M (2003) Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria. Plant Physiol 131(3):1209–1219. doi: 10.1104/pp. 102.016006 PubMedCrossRefGoogle Scholar
  28. Kilaru A, Bailey BA, Hasenstein KH (2007) Moniliophthora perniciosa produces hormones and alters endogenous auxin and salicylic acid in infected cocoa leaves. FEMS Microbiol Lett 274(2):238–244. doi: 10.1111/j.1574-6968.2007.00837.x PubMedCrossRefGoogle Scholar
  29. Kim IS, Okubo H, Fujieda K (1992) Endogenous levels of IAA in relation to parthenocarpy in cucumber (Cucumis sativus L.). Sci Hort 52(1–2):1–8. doi: 10.1016/0304-4238(92)90002-t CrossRefGoogle Scholar
  30. Lange T, Hedden P, Graebe JE (1994) Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. Proc Natl Acad Sci USA 91(18):8552–8556PubMedCrossRefGoogle Scholar
  31. Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG (2007) Asparagine in plants. Ann App Biol 150(1):1–26. doi: 10.1111/j.1744-7348.2006.00104.x CrossRefGoogle Scholar
  32. Leal GA, Albuquerque PSB, Figueira A (2007) Genes differentially expressed in Theobroma cacao associated with resistance to witches’ broom disease caused by Crinipellis perniciosa. Mol Plant Pathol 8(3):279–292. doi: 0.1111/j.1364-3703.2007.00393.x PubMedCrossRefGoogle Scholar
  33. Leal GA, Gomes LH, Albuquerque PSB, Tavares FCA, Figueira A (2010) Searching for Moniliophthora perniciosa pathogenicity genes. Fungal Biol 114(10):842–854. doi: 10.1016/j.funbio.2010.07.009 PubMedCrossRefGoogle Scholar
  34. Levine B, Klionsky DJ (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6(4):463–477. doi: 10.1016/s1534-5807(04)00099-1 PubMedCrossRefGoogle Scholar
  35. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90(5):929–938. doi: 10.1016/s0092-8674(00)80357-8 PubMedCrossRefGoogle Scholar
  36. Lima JO, Pereira JF, Rincones J, Barau JG, Araújo EF, Pereira GAG, QueirozI MV (2009) The glyceraldehyde-3-phosphate dehydrogenase gene of Moniliophthora perniciosa, the causal agent of witches’ broom disease of Theobroma cacao. Genet Mol Biol 132(2):362–366CrossRefGoogle Scholar
  37. Lindberg G, Molin K (1949) Notes on the physiology of the cocoa parasite Marasmius perniciosus. Physiol Plantarum 2(2):138–144CrossRefGoogle Scholar
  38. Marelli J-P, Maximova S, Gramacho K, Kang S, Guiltinan M (2009) Infection biology of Moniliophthora perniciosa on Theobroma cacao and alternate solanaceous hosts. Trop Plant Biol 2(3):149–160. doi: 10.1007/s12042-009-9038-1 CrossRefGoogle Scholar
  39. Maroto JV, Miguel A, Lopez-Galarza S, San Bautista A, Pascual B, Alagarda J, Guardiola JL (2005) Parthenocarpic fruit set in triploid watermelon induced by CPPU and 2,4-D applications. Plant Growth Regul 45(3):209–213. doi: 10.1007/s10725-005-3992-x CrossRefGoogle Scholar
  40. Martin RC, Mok MC, Mok DWS (1999) Isolation of a cytokinin gene, ZOG1, encoding zeatin O-glucosyltransferase from Phaseolus lunatus. Procthe Natl Acad Sci USA 96(1):284–289. doi: 10.1073/pnas.96.1.284 CrossRefGoogle Scholar
  41. Martinelli F, Uratsu SL, Reagan RL, Chen Y, Tricoli D, Fiehn O, Rocke DM, Gasser CS, Dandekar AM (2009) Gene regulation in parthenocarpic tomato fruit. J Exp Bot 60(13):3873–3890. doi: 10.1093/jxb/erp227 PubMedCrossRefGoogle Scholar
  42. Matsuzaki F, Shimizu M, Wariishi H (2008) Proteomic and metabolomic analyses of the white-rot fungus Phanerochaete chrysosporium exposed to exogenous benzoic acid. J Proteome Res 7(6):2342–2350. doi: 10.1021/pr700617s PubMedCrossRefGoogle Scholar
  43. Meinhardt LW, Bellato CM, Rincones J, Azevedo RA, Cascardo JCM, Pereira GAG (2006) In vitro production of biotrophic-like cultures of Crinipellis perniciosa, the casual agent of witches’ broom disease of Theobroma cacao. Curr Microbiol 52(3):191–196. doi: 0.1007/s00284-005-0182-z PubMedCrossRefGoogle Scholar
  44. Meinhardt L, Rincones J, Bailey B, Aime M, Griffith G, Zhang D, Pereira G (2008) Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao: what’s new from this old foe? Mol Plant Pathol 9(5):577–588. doi: 10.1111/j.1364-3703.2008.00496.x PubMedCrossRefGoogle Scholar
  45. Mende K, Homann V, Tudzynski B (1997) The geranylgeranyl diphosphate synthase gene of Gibberella fujikuroi: isolation and expression. Mol Gen Genet 255(1):96–105. doi: 10.1007/s004380050477 PubMedCrossRefGoogle Scholar
  46. Mondego J, Carazzolle M, Costa G, Formighieri E, Parizzi L, Rincones J, Cotomacci C, Carraro D, Cunha A, Carrer H, Vidal R, Estrela R, Garcia O, Thomazella D, de Oliveira B, Pires A, Rio M, Araujo M, de Moraes M, Castro L, Gramacho K, Goncalves M, Neto J, Neto A, Barbosa L, Guiltinan M, Bailey B, Meinhardt L, Cascardo J, Pereira G (2008) A genome survey of Moniliophthora perniciosa gives new insights into Witches’ Broom Disease of cacao. BMC Genomics 9(1):548. doi: 10.1186/1471-2164-9-548 PubMedCrossRefGoogle Scholar
  47. Peretó JG, Beltrán JP, García-Martínez JL (1988) The source of gibberellins in the parthenocarpic development of ovaries on topped pea plants. Planta 175(4):493–499. doi: 10.1007/bf00393070 CrossRefGoogle Scholar
  48. Pettipher GL (1986) Analysis of cocoa pulp and the formulation of a standardised artificial cocoa pulp medium. J Sci Food Agric 37(3):297–309. doi: 10.1002/jsfa.2740370315 CrossRefGoogle Scholar
  49. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45. doi: 10.1093/nar/29.9.e45 PubMedCrossRefGoogle Scholar
  50. Pungartnik C, Melo SCO, Basso TS, Macena WG, Cascardo JCM, Brendel M (2009) Reactive oxygen species and autophagy play a role in survival and differentiation of the phytopathogen Moniliophthora perniciosa. Fungal Genet Biol 46(6–7):461–472. doi: 10.1016/j.fgb.2009.03.007 PubMedCrossRefGoogle Scholar
  51. Richardson M, Valdes-Rodriguez S, Blanco-Labra A (1987) A possible function for thaumatin and a TMV-induced protein suggested by homology to a maize inhibitor. Nature 327:432–434CrossRefGoogle Scholar
  52. Rieu I, Powers SJ (2009) Real-time quantitative RT-PCR: design, calculations, and statistics. Plant Cell 21(4):1031–1033. doi: 10.1105/tpc.109.066001 PubMedCrossRefGoogle Scholar
  53. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13(1):11–29. doi: 10.1105/tpc.13.1.11 PubMedGoogle Scholar
  54. Santos RX, Melo SCO, Cascardo JCM, Brendel M, Pungartnik C (2008) Carbon source-dependent variation of acquired mutagen resistance of Moniliophthora perniciosa: similarities in natural and artificial systems. Fungal Genet Biol 45(6):851–860. doi: 10.1016/j.fgb.2008.02.005 PubMedCrossRefGoogle Scholar
  55. Scarpari LM, Meinhardt LW, Mazzafera P, Pomella AWV, Schiavinato MA, Cascardo JCM, Pereira GAG (2005) Biochemical changes during the development of witches’ broom: the most important disease of cocoa in Brazil caused by Crinipellis perniciosa. J Exp Bot 56(413):865–877. doi: 10.1093/jxb/eri079 PubMedCrossRefGoogle Scholar
  56. Schmülling T, Werner T, Riefler M, Krupková E, Bartrina y Manns I (2003) Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis, and other species. Journal of Plant Research 116(3):241–252. doi: 10.1007/s10265-003-0096-4 PubMedCrossRefGoogle Scholar
  57. Schwan RF (1998) Cocoa fermentations conducted with a defined microbial cocktail inoculum. Appl Environ Microbiol 64(4):1477–1483PubMedGoogle Scholar
  58. Seo HS, Song JT, Cheong J-J, Lee Y-H, Lee Y-W, Hwang I, Lee JS, Choi YD (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci 98(8):4788–4793. doi: 10.1073/pnas.081557298 PubMedCrossRefGoogle Scholar
  59. Serrani JC, Sanjuán R, Ruiz-Rivero O, Fos M, García-Martínez JL (2007) Gibberellin regulation of fruit set and growth in tomato. Plant Physiol 145(1):246–257. doi: 10.1104/pp. 107.098335 PubMedCrossRefGoogle Scholar
  60. Sharma SS, Dietz K-J (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57(4):711–726. doi: 10.1093/jxb/erj073 PubMedCrossRefGoogle Scholar
  61. Shi Z, Maximova S, Liu Y, Verica J, Guiltinan M (2010) Functional analysis of the Theobroma cacao NPR1 gene in Arabidopsis. BMC Plant Biol 10(1):248. doi: 10.1186/1471-2229-10-248 PubMedCrossRefGoogle Scholar
  62. Spoel S, Koornneef A, Claessens S, Korzelius J, Van Pelt J, Mueller M, Buchala A, Metraux J, Brown R, Kazan K (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15(3):760–770. doi: 10.1105/tpc.009159 PubMedCrossRefGoogle Scholar
  63. Srinivasan U, Staines HJ, Bruce A (1992) Influence of media type on antagonistic modes of Trichoderma sp against wood decay basidiomycetes. Mat Organ 27(4):301–321Google Scholar
  64. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17(2):616–627. doi: 10.1105/tpc.104.026690 PubMedCrossRefGoogle Scholar
  65. Tudzynski B, Kawaide H, Kamiya Y (1998) Gibberellin biosynthesis in Gibberella fujikuroi: cloning and characterization of the copalyl diphosphate synthase gene. Curr Genet 34(3):234–240. doi: 10.1007/s002940050392 PubMedCrossRefGoogle Scholar
  66. Tudzynski B, Mihlan M, Rojas MC, Linnemannstöns P, Gaskin P, Hedden P (2003) Characterization of the final two genes of the gibberellin biosynthesis gene cluster of Gibberella fujikuroi. J Biol Chem 278(31):28635–28643. doi: 10.1074/jbc.M301927200 PubMedCrossRefGoogle Scholar
  67. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ (2006) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312(5773):580–583. doi: 10.1126/science.1124550 PubMedCrossRefGoogle Scholar
  68. Verica JA, Maximova SN, Strem MD, Carlson JE, Bailey BA, Guiltinan MJ (2004) Isolation of ESTs from cacao (Theobroma cacao L.) leaves treated with inducers of the defense response. Plant Cell Rep 23:404–413. doi: 10.1007/s00299-004-0852-5 PubMedCrossRefGoogle Scholar
  69. Xu Y, Chang P, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6(8):1077–1085. doi: 10.1105/tpc.6.8.1077 PubMedGoogle Scholar
  70. Zaparoli G, Garcia O, Medrano F, Tiburcio R, Costa G, Pereira G (2009) Identification of a second family of genes in Moniliophthora perniciosa, the causal agent of Witches’ Broom disease in cacao, encoding necrosis inducing proteins similar to cerato platanins. Mycol Res 113(1):61–72PubMedCrossRefGoogle Scholar
  71. Zhang C, Lee U, Tanabe K (2008) Hormonal regulation of fruit set, parthenogenesis induction and fruit expansion in Japanese pear. Plant Growth Regula 55(3):231–240. doi: 10.1007/s10725-008-9279-2 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag (outside the USA) 2012

Authors and Affiliations

  • Rachel L. Melnick
    • 1
  • Jean-Philippe Marelli
    • 2
  • Richard C. Sicher
    • 3
  • Mary D. Strem
    • 1
  • Bryan A. Bailey
    • 1
  1. 1.USDA-ARS Sustainable Perennial Crops LabBeltsvilleUSA
  2. 2.Mars Center for Cocoa ScienceItajuipeBrazil
  3. 3.USDA-ARS Crop Systems & Global Change LabBeltsvilleUSA

Personalised recommendations