Abstract
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.
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- MIP:
-
major intrinsic protein
- BGF:
-
blue-green fluorescence
- PA:
-
polyamine
- EST:
-
expression sequence tag
- TcODC :
-
ornithine decarboxylase
- TcADC :
-
arginine decarboxylase
- TcSAMDC :
-
S-adenosylmethionine decarboxylase
- TcTPP :
-
trehalose-6-phosphatase
- TcSOT :
-
putative sorbitol transporter
- TcPR5 :
-
osmotin-like protein
- TcNI :
-
putative alkaline/neutral invertase
- TcCESA3 :
-
putatively encoding a cellulose synthase
- TcLOX :
-
13-lipoxygenase
- AOC:
-
allene oxide cyclase
- TcTIP :
-
a tonoplast intrinsic protein
- TcRPK :
-
receptor-like protein kinase
- TcMKK4 :
-
putative mitogen-activated protein
- TcSTK :
-
serine/threonine protein kinase
- NR:
-
nitrate reductase
- HK:
-
histidine kinase
- TcHK :
-
sensor type histidine kinase
- TcMAPK3 :
-
mitogen-activated protein kinase
- TcPP2C :
-
protein phosphatase
- TcZFP :
-
C2H2 zinc finger protein
- ABA:
-
abscisic acid
- VAM:
-
vesicular-arbuscular mycorrhiza
- ASP:
-
asparagine
- HIS:
-
histidine
- ARG:
-
arginine
- PRO:
-
proline
- GABA:
-
gamma-aminobutyric acid
- VAL:
-
valine
- LEU:
-
leucine
References
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 54:306–313
Arnold AE, Mejía LC, Kyllo D et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci 100:15649–15654
Augé RM (2001) Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11:3–42
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 46:174–188
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 60:3279–3295
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 185–204
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 224:1449–1464
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 46:24–35
Bailey BA, Strem MD, Wood D (2009) Trichoderma species form endophytic associations within Theobroma cacao trichomes. Mycol Res 113:1365–1376
Beck EH, Fettig S, Knake C et al (2007) Specific and unspecific responses of plants to cold and drought stress. J Biosci 32:501–510
Belsky JM, Siebert SF (2003) Cultivating cacao: implications of sun grown cacao on local food security and environmental sustainability. Agric Hum Values 20:277–285
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 101:9909–9914
Carter CJ, Thornburg RW (2004) Tobacco nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiol 134:460–469
Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160
D’Angeli S, Altamura MM (2007) Osmotin induces cold protection in olive trees by affecting programmed cell death and cytoskeleton organization. Planta 225:1147–1163
Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants. J Biol Chem 277:30859–30869
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 2:149–160
Fait A, Yellin A, Fromm H (2005) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Lett 579:415–420
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 117:293–302
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 117:283–292
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 99:15898–15900
Geisbrecht BV, Zhu D, Schulz K et al (1998) Molecular characterization of Saccharomyces cerevisiae Δ3, Δ2-enoyl-CoA isomerase. J Biol Chem 273:33184–33191
Grishutin SG, Gusakov AV, Markov AV et al (2004) Specific xyloglucanases as a new class of polysaccharide-degrading enzymes. Biochim Biophys Acta 1674:263–281
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 112:1335–1343
Harman GE, Howell CR, Viterbo A et al (2004a) Trichoderma spp.: opportunistic avirulent plant symbionts. Nat Rev Microbiol 2:43–56
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 94:147–153
Hause B, Hause G, Kutter C et al (2003) Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol 44:643–648
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 125:877–890
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 3:199–210
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 53:1463–1473
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 59:365–386
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 131:1169–1177
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 86:291–307
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 55:883–904
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 16:414–427
Lichtenthaler HK, Miehé JA (1997) Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci 2:316–320
Lindstrom JT, Sun S, Belanger FC (1993) A novel fungal protease expressed in endophytic infection of Poa species. Plant Physiol 102:645–650
Malinowski DP, Belesky DP (2000) Adaptation of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940
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 57:3755–3766
McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389
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 46:46–56
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 15:93–97
Morris PC (2001) MAP kinase signal transduction pathways in plants. New Phytol 151:67–89
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 79:171–187
Passioura JB (1996) Drought and drought tolerance. Plant Growth Regul 20:79–83
Patade VY, Bhargava S, Suprasanna P (2009) Halopriming imparts tolerance to salt and PEG induced drought stress in sugarcane. Agr Ecosyst Environ 134:24–28
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 51:621–628
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 1:24–33
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 37:354–369
Samuels GJ, Ismaiel A (2009) Trichoderma evansii and T. lieckfeldtiae: two new T. hamatum-like species. Mycologia 101:142–156
Samuels GJ, Pardo-Schultheiss R, Hebbar KP et al (2000) Trichoderma stromaticum sp. nov., a parasite of the cacao witches broom pathogen. Mycol Res 104:760–764
Samuels GJ, Dodd SL, Lu B-S et al (2006a) The Trichoderma koningii aggregate species. Stud Mycol 56:67–133
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 110:381–392
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 127:494–506
Shelp BJ, Bown AW, McLean MD (1999) Metabolism and function of gamma-aminobutyric acid. Trends Plant Sci 4:446–452
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 280:26241–26247
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 39:139–143
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 50:793–796
Smart LB, Moskal WA, Cameron KD et al (2001) MIP genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 42:686–693
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 96:1245–1252
Sturm A (1999) Invertases: primary structures, functions, and roles in plant development, and sucrose partitioning. Plant Physiol 121:1–7
Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195
Watari J, Kobae Y, Yamaki S et al (2004) Identification of sorbitol transporters expressed in the phloem of apple source leaves. Plant Cell Physiol 45:1032–1041
Wood GAR, Lass RA (2001) Cacao, 4th edn. Blackwell, Oxford, p 620
Yang SH, Berberich T, Miyazaki A et al (2003) Ntdin, a tobacco senescence-associated gene, is involved in molybdenum cofactor biosynthesis. Plant Cell Physiol 44:1037–1044
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 38:863–873
Zhu J-K (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273
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Bailey, B.A., Bae, H., Melnick, R., Crozier, J. (2011). The Endophytic Trichoderma hamatum Isolate DIS 219b Enhances Seedling Growth and Delays the Onset of Drought Stress in Theobroma cacao . In: Pirttilä, A., Frank, A. (eds) Endophytes of Forest Trees. Forestry Sciences, vol 80. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1599-8_10
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