The Endophytic Trichoderma hamatum Isolate DIS 219b Enhances Seedling Growth and Delays the Onset of Drought Stress in Theobroma cacao

  • Bryan A. Bailey
  • Hanhong Bae
  • Rachel Melnick
  • Jayne Crozier
Part of the Forestry Sciences book series (FOSC, volume 80)


Theobroma cacao (cacao) is a tropical understory tree with sensitivity to drought. Cacao responds to drought by decreases in net photosynthesis, PS II efficiency, stomatal conductance, water potential and changes in leaf florescence. Drought also alters cacao gene expression as well as leaf glucose and free amino acid content. In recent years an incredible diversity of fungal endophytes has been identified in association with cacao. These endophytes are being studied for the benefits they provide to cacao including tolerance to biotic and abiotic stresses. During establishment of the endophytic association between cacao and fungal endophytes both plant and fungal gene expression are altered. The endophytic Trichoderma hamatum isolate DIS 219b delays the onset of drought stress in cacao. This delay manifests itself through enhanced root growth, maintenance of stomatal conductance, water potential, net photosynthesis, and PSII efficiency, changes in free amino acid concentrations, and a delay in drought-induced changes in leaf gene expression. The cacao plant and DIS 219b adapt to each other and this adaptation may contribute to the observed plant growth promotion and the delay in onset of drought stress. The increase in root growth is thought to increase water uptake and availability, delaying the time point where the water supply becomes limiting and drought stress occurs.


Drought Stress Endophytic Fungus Plant Growth Promotion Drought Response Trichoderma Species 
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.



major intrinsic protein


blue-green fluorescence




expression sequence tag


ornithine decarboxylase


arginine decarboxylase


S-adenosylmethionine decarboxylase




putative sorbitol transporter


osmotin-like protein


putative alkaline/neutral invertase


putatively encoding a cellulose synthase




allene oxide cyclase


a tonoplast intrinsic protein


receptor-like protein kinase


putative mitogen-activated protein


serine/threonine protein kinase


nitrate reductase


histidine kinase


sensor type histidine kinase


mitogen-activated protein kinase


protein phosphatase


C2H2 zinc finger protein


abscisic acid


vesicular-arbuscular mycorrhiza










gamma-aminobutyric acid






  1. Adams P, De-Leij FAAM, Lynch JM (2007) Trichoderma harzianum Rifai 1295–22 mediates growth promotion of crack willow (Salix fragilis) saplings in both clean and metal-contaminated soil. Microb Ecol 54:306–313PubMedCrossRefGoogle Scholar
  2. Arnold AE, Mejía LC, Kyllo D et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci 100:15649–15654PubMedCrossRefGoogle Scholar
  3. Augé RM (2001) Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  4. Bae B, Kim S-H, Kim M-S et al (2008) The drought response of Theobroma cacao (cacao) and the regulation of genes involved in polyamine biosynthesis by drought and other stresses. Plant Physiol Biochem 46:174–188PubMedCrossRefGoogle Scholar
  5. Bae H, Sicher RC, Kim MS et al (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 60:3279–3295PubMedCrossRefGoogle Scholar
  6. Bailey BA, Lumsden RD (1998) Direct effects of Trichoderma and Gliocladium on plant growth and resistance to pathogens. In: Kubicek CP, Harman GE (eds) Trichoderma and Gliocladium, vol 2. Taylor and Francis, Bristol, pp 185–204Google Scholar
  7. Bailey BA, Bae H, Strem MD et al (2006) Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224:1449–1464PubMedCrossRefGoogle Scholar
  8. Bailey BA, Bae H, Strem MD et al (2008) Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biol Control 46:24–35CrossRefGoogle Scholar
  9. Bailey BA, Strem MD, Wood D (2009) Trichoderma species form endophytic associations within Theobroma cacao trichomes. Mycol Res 113:1365–1376PubMedCrossRefGoogle Scholar
  10. Beck EH, Fettig S, Knake C et al (2007) Specific and unspecific responses of plants to cold and drought stress. J Biosci 32:501–510PubMedCrossRefGoogle Scholar
  11. Belsky JM, Siebert SF (2003) Cultivating cacao: implications of sun grown cacao on local food security and environmental sustainability. Agric Hum Values 20:277–285CrossRefGoogle Scholar
  12. Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci 101:9909–9914PubMedCrossRefGoogle Scholar
  13. Carter CJ, Thornburg RW (2004) Tobacco nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiol 134:460–469PubMedCrossRefGoogle Scholar
  14. Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160PubMedCrossRefGoogle Scholar
  15. D’Angeli S, Altamura MM (2007) Osmotin induces cold protection in olive trees by affecting programmed cell death and cytoskeleton organization. Planta 225:1147–1163PubMedCrossRefGoogle Scholar
  16. Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants. J Biol Chem 277:30859–30869PubMedCrossRefGoogle Scholar
  17. Evans HC, Holmes KA, Thomas SE (2003) Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycol Prog 2:149–160CrossRefGoogle Scholar
  18. Fait A, Yellin A, Fromm H (2005) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Lett 579:415–420PubMedCrossRefGoogle Scholar
  19. Ferrario-Méry S, Valadier M-H, Foyer CH (1998) Overexpression of nitrate reductase in tobacco delays drought-induced decreases in nitrate reductase activity and mRNA. Plant Physiol 117:293–302PubMedCrossRefGoogle Scholar
  20. Foyer CH, Valadier MH, Migge A et al (1998) Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiol 117:283–292PubMedCrossRefGoogle Scholar
  21. Garg AK, Kim J-K, Owens TG et al (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci 99:15898–15900PubMedCrossRefGoogle Scholar
  22. Geisbrecht BV, Zhu D, Schulz K et al (1998) Molecular characterization of Saccharomyces cerevisiae Δ3, Δ2-enoyl-CoA isomerase. J Biol Chem 273:33184–33191PubMedCrossRefGoogle Scholar
  23. Grishutin SG, Gusakov AV, Markov AV et al (2004) Specific xyloglucanases as a new class of polysaccharide-degrading enzymes. Biochim Biophys Acta 1674:263–281Google Scholar
  24. Hanada RE, Jorge Souza TD, Pomella AW et al (2008) Trichoderma martiale sp. nov., a new endophyte from sapwood of Theobroma cacao with a potential for biological control. Mycol Res 112:1335–1343PubMedCrossRefGoogle Scholar
  25. Harman GE, Howell CR, Viterbo A et al (2004a) Trichoderma spp.: opportunistic avirulent plant symbionts. Nat Rev Microbiol 2:43–56PubMedCrossRefGoogle Scholar
  26. Harman GE, Petzoldt R, Comis A et al (2004b) Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathol 94:147–153CrossRefGoogle Scholar
  27. Hause B, Hause G, Kutter C et al (2003) Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol 44:643–648PubMedCrossRefGoogle Scholar
  28. Ho S-L, Chao Y-C, Tong W-F et al (2001) Sugar coordinately and differentially regulates growth- and stress-related gene expression via a complex signal transduction network and multiple control mechanisms. Plant Physiol 125:877–890PubMedCrossRefGoogle Scholar
  29. Holmes KA, Schroers H-J, Thomas SE et al (2004) Taxonomy and biocontrol potential of a new species of Trichoderma from the Amazon basin in South America. Mycol Prog 3:199–210CrossRefGoogle Scholar
  30. Hummel I, Couée I, El Amrani A et al (2002) Involvement of polyamines in root development at low temperature in the subantarctic cruciferous species Pringlea antiscorbutica. J Exp Bot 53:1463–1473PubMedCrossRefGoogle Scholar
  31. Ishida T, Kurata T, Okada K et al (2008) A genetic regulatory network in the development of trichomes and root hairs. Ann Rev Plant Bio 59:365–386CrossRefGoogle Scholar
  32. Jasinski M, Ducos E, Martinoia E et al (2003) The ATP-binding cassette transporters: structure, function and gene family comparison between rice and Arabidopsis. Plant Physiol 131:1169–1177PubMedCrossRefGoogle Scholar
  33. Keil A, Zeller M, Wida A et al (2008) What determines farmers’ resilience towards ENSO-related drought? An empirical assessment in central Sulawesi, Indonesia. Clim Change 86:291–307CrossRefGoogle Scholar
  34. Kim SH, Hong JK, Lee SC et al (2004) CAZFP1, Cys2/His2-type zinc-finger transcription factor gene functions as a pathogen-induced early-defense gene in Capsicum annuum. Plant Mol Biol 55:883–904PubMedGoogle Scholar
  35. Li Y, Lee KK, Walsh S et al (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a relevance vector machine. Genome Res 16:414–427PubMedCrossRefGoogle Scholar
  36. Lichtenthaler HK, Miehé JA (1997) Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci 2:316–320CrossRefGoogle Scholar
  37. Lindstrom JT, Sun S, Belanger FC (1993) A novel fungal protease expressed in endophytic infection of Poa species. Plant Physiol 102:645–650PubMedGoogle Scholar
  38. Malinowski DP, Belesky DP (2000) Adaptation of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940CrossRefGoogle Scholar
  39. Mazzucotelli E, Tartari A, Cattivelli L et al (2006) Metabolism of γ-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot 57:3755–3766PubMedCrossRefGoogle Scholar
  40. McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389PubMedCrossRefGoogle Scholar
  41. Melnick RL, Zidack NK, Bailey BA et al (2008) Bacterial endophytes: Bacillus spp. from vegetable crops as potential biological control agents of black pod rot of cacao. Biol Control 46:46–56CrossRefGoogle Scholar
  42. Mohd Razi I, Abd Halim H, Kamariah D et al (1992) Growth, plant water relation and photosynthesis rate of young Theobroma cacao as influenced by water stress. Pertanika 15:93–97Google Scholar
  43. Morris PC (2001) MAP kinase signal transduction pathways in plants. New Phytol 151:67–89CrossRefGoogle Scholar
  44. Moser G, Leuschner C, Hertel D et al (2010) Response of cocoa trees (Theobroma cacao) to a 13-month desiccation period in Sulawesi, Indonesia. Agroforest Syst 79:171–187CrossRefGoogle Scholar
  45. Passioura JB (1996) Drought and drought tolerance. Plant Growth Regul 20:79–83CrossRefGoogle Scholar
  46. Patade VY, Bhargava S, Suprasanna P (2009) Halopriming imparts tolerance to salt and PEG induced drought stress in sugarcane. Agr Ecosyst Environ 134:24–28CrossRefGoogle Scholar
  47. Resende MLV, Nojosa GBA, Cavalcanti LS et al (2002) Induction of resistance in cocoa against Crinipellis perniciosa and Verticillium dahliae by acibenzolar-S-methyl (ASM). Plant Pathol 51:621–628CrossRefGoogle Scholar
  48. Rubini MR, Silva-Ribeiro RT, Pomella AWV et al (2005) Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of witches’ broom disease. Int J Biol Sci 1:24–33PubMedGoogle Scholar
  49. Saez A, Apostolova N, Gonzalez-Guzman M et al (2004) Gain-of function and loss-of-function phenotypes of the protein phosphatase 2 C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J 37:354–369PubMedCrossRefGoogle Scholar
  50. Samuels GJ, Ismaiel A (2009) Trichoderma evansii and T. lieckfeldtiae: two new T. hamatum-like species. Mycologia 101:142–156PubMedCrossRefGoogle Scholar
  51. Samuels GJ, Pardo-Schultheiss R, Hebbar KP et al (2000) Trichoderma stromaticum sp. nov., a parasite of the cacao witches broom pathogen. Mycol Res 104:760–764CrossRefGoogle Scholar
  52. Samuels GJ, Dodd SL, Lu B-S et al (2006a) The Trichoderma koningii aggregate species. Stud Mycol 56:67–133PubMedCrossRefGoogle Scholar
  53. Samuels GJ, Suarez C, Solis K et al (2006b) Trichoderma theobromicola and T. paucisporum: two new species isolated from cacao in South America. Mycol Res 110:381–392PubMedCrossRefGoogle Scholar
  54. Selote DS, Khanna-Chopra R (2006) Drought acclimation confers oxidative stress tolerance by inducing co-ordinated antioxidant defense at cellular and subcellular level in leaves of wheat seedlings. Phys Plant 127:494–506CrossRefGoogle Scholar
  55. Shelp BJ, Bown AW, McLean MD (1999) Metabolism and function of gamma-aminobutyric acid. Trends Plant Sci 4:446–452PubMedCrossRefGoogle Scholar
  56. Sherameti I, Shahollari B, Venus Y et al (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J Biol Chem 280:26241–26247PubMedCrossRefGoogle Scholar
  57. Shimada Y, Wu G-J, Watanabe A (1998) A protein encoded by din1, a dark-inducible and senescence-associated gene of radish, can be imported by isolated chloroplasts and has sequence similarity to sulfide dehydrogenase and other small stress proteins. Plant Cell Physiol 39:139–143PubMedGoogle Scholar
  58. Simon-Sarkadi L, Kocsy G, Várhegyi Á et al (2006) Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Biol Plant 50:793–796CrossRefGoogle Scholar
  59. Smart LB, Moskal WA, Cameron KD et al (2001) MIP genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 42:686–693PubMedCrossRefGoogle Scholar
  60. Steyaert JM, Stewart A, Ridgway HJ (2004) Co-expression of two genes, a chitinase (chit42) and proteinase (prb1), implicated in mycroparasitisim by Trichoderma hamatum. Mycologia 96:1245–1252PubMedCrossRefGoogle Scholar
  61. Sturm A (1999) Invertases: primary structures, functions, and roles in plant development, and sucrose partitioning. Plant Physiol 121:1–7PubMedCrossRefGoogle Scholar
  62. Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195PubMedCrossRefGoogle Scholar
  63. Watari J, Kobae Y, Yamaki S et al (2004) Identification of sorbitol transporters expressed in the phloem of apple source leaves. Plant Cell Physiol 45:1032–1041PubMedCrossRefGoogle Scholar
  64. Wood GAR, Lass RA (2001) Cacao, 4th edn. Blackwell, Oxford, p 620Google Scholar
  65. Yang SH, Berberich T, Miyazaki A et al (2003) Ntdin, a tobacco senescence-associated gene, is involved in molybdenum cofactor biosynthesis. Plant Cell Physiol 44:1037–1044PubMedCrossRefGoogle Scholar
  66. Yedidia I, Benhamou N, Kapulnik Y et al (2000) Induction and accumulation of PR protein activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol Plant Physiol Biochem 38:863–873CrossRefGoogle Scholar
  67. Zhu J-K (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Bryan A. Bailey
    • 1
  • Hanhong Bae
    • 2
  • Rachel Melnick
    • 1
  • Jayne Crozier
    • 3
  1. 1.United States Department of Agriculture-Agricultural Research Service, Sustainable Perennial Crops Laboratory (USDA-ARS)BARC-WestBeltsvilleUSA
  2. 2.School of BiotechnologyYeungnam UniversityGyeongsanRepublic of Korea
  3. 3.CABI Caribbean & Latin America – CATIE Office, Centro Agronómico Tropica de Investigación y Enseñanza (CATIE)CartagoCosta Rica

Personalised recommendations