Skip to main content

Advertisement

Log in

Analysis of expressed sequence tags derived from a compatible Mycosphaerella fijiensis–banana interaction

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Mycosphaerella fijiensis, a hemibiotrophic fungus, is the causal agent of black leaf streak disease, the most serious foliar disease of bananas and plantains. To analyze the compatible interaction of M. fijiensis with Musa spp., a suppression subtractive hybridization (SSH) cDNA library was constructed to identify transcripts induced at late stages of infection in the host and the pathogen. In addition, a full-length cDNA library was created from the same mRNA starting material as the SSH library. The SSH procedure was effective in identifying specific genes predicted to be involved in plant–fungal interactions and new information was obtained mainly about genes and pathways activated in the plant. Several plant genes predicted to be involved in the synthesis of phenylpropanoids and detoxification compounds were identified, as well as pathogenesis-related proteins that could be involved in the plant response against M. fijiensis infection. At late stages of infection, jasmonic acid and ethylene signaling transduction pathways appear to be active, which corresponds with the necrotrophic life style of M. fijiensis. Quantitative PCR experiments revealed that antifungal genes encoding PR proteins and GDSL-like lipase are only transiently induced 30 days post inoculation (dpi), indicating that the fungus is probably actively repressing plant defense. The only fungal gene found was induced 37 dpi and encodes UDP-glucose pyrophosphorylase, an enzyme involved in the biosynthesis of trehalose. Trehalose biosynthesis was probably induced in response to prior activation of plant antifungal genes and may act as an osmoprotectant against membrane damage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

BLSD:

Black leaf streak disease

CTAB:

Cetyl trimethyl ammonium bromide

Dpi:

Days post inoculation

EST:

Expressed sequence tag

ET:

Ethylene

FA:

Fatty acid

HCN:

Hydrogen cyanide

Hpi:

Hours post inoculation

INIBAP:

International network for the improvement of banana and plantain

ITS:

Internal transcribed spacer

JA:

Jasmonate

JA-Ile:

Jasmonyl-isoleucine

NCBI:

National Center for Biotechnology Information

NR:

Non-redundant

PCR:

Polymerase chain reaction

PDB:

Potato dextrose broth

PR:

Pathogenesis related

qPCR:

Quantitative polymerase chain reaction

RT:

Reverse transcriptase

SA:

Salicylic acid

SSH:

Suppression subtractive hybridization

References

  • Abad LR, D’Urzo MP, Liu D, Narasimhan ML, Reuveni M, Zhu JK, Niu X, Singh NK, Hasegawa PM, Bressan RA (1996) Antifungal activity of tobacco osmotin has specificity and involves plasma membrane permeabilization. Plant Sci 118:11–23

    CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    PubMed  CAS  Google Scholar 

  • Alvarado Y, Leiva M, Rodríguez MA, Acosta M, Cruz M, Portal N, Kosky R, García L, Bermúdez I, Padrón J (2003) Early evaluation of black leaf streak resistance by using mycelia suspensions of Mycosphaerella fijiensis. In: Jacome L, Lepoivre P, Marin D, Ortiz R, Romero R, Escalant JV (eds) Mycosphaerella leaf spot diseases of bananas: present status and outlook. Proceedings of the second international workshop on Mycosphaerella leaf spot diseases, San José, pp 169–175

  • Antonini E, Brunori M, Greenwood C, Malmstrom BG, Rotilio GC (1971) The interaction of cyanide with cytochrome oxidase. Eur J Biochem 23:396–400

    PubMed  CAS  Google Scholar 

  • Azhar M, Heslop-Harrison JS (2008) Genomes, diversity and resistance gene analogues in Musa species. Cytogenet Genome Res 121:59–66

    PubMed  CAS  Google Scholar 

  • Bennett M, Mehta M, Grant M (2005) Biophoton imaging: a non-destructive method for assaying R gene responses. Mol Plant–Microbe Interact 18:95–102

    PubMed  CAS  Google Scholar 

  • Bormann C, Baier D, Horr I, Raps C, Berger J, Jung G, Schwarz H (1999) Characterization of a novel, antifungal, chitin-binding protein from Streptomyces tendae Tu901 that interferes with growth polarity. J Bacteriol 181:7421–7429

    PubMed  CAS  Google Scholar 

  • Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580

    PubMed  CAS  Google Scholar 

  • Busogoro JP, Etamé JJ, Hareliman G, Lognay G, Messiaen J, Lepoivre P, van Cutsem P (2004) Experimental evidence for the action of M. fijiensis toxins on banana photosynthetic apparatus. In: Jain SM, Swennen R (eds) Banana improvement: cellular, molecular biology, and induced mutations. Science Publishers Inc, Enfield, pp 171–181

    Google Scholar 

  • Carlier J, Lebrun MH, Zapater MF, Dubois C, Mourichon X (1996) Genetic structure of the global population of banana black leaf streak fungus, Mycosphaerella fijiensis. Mol Ecol 5:499–510

    Google Scholar 

  • Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257

    PubMed  CAS  Google Scholar 

  • Cho Y, Hou S, Zhong S (2008) Analysis of expressed sequence tags from the fungal banana pathogen Mycosphaerella fijiensis. Open Mycol J 2:61–73

    CAS  Google Scholar 

  • Cruz-Cruz CA, Ramírez-Tec G, García-Sosa K, Escalante-Erosa F, Hill L, Osbourn AE, Peña-Rodríguez LM (2010) Phytoanticipins from banana (Musa acuminata cv. Grande Naine) plants, with antifungal activity against Mycosphaerella fijiensis, the causal agent of black sigatoka. Eur J Plant Pathol 126:459–463

    CAS  Google Scholar 

  • Davidson RM, Reeves PA, Manosalva PM, Leach JE (2009) Germins: a diverse protein family important for crop improvement. Plant Sci 177:499–510

    CAS  Google Scholar 

  • Diatchenko L, Lau YFC, Campbell AP (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030

    PubMed  CAS  Google Scholar 

  • Dixon RA, Achnine L, Kota P, Chang-Jun L, Reddy MSS, Wang L (2002) The phenylpropanoid pathway and plant defense a genomics perspective. Mol Plant Pathol 3:371–390

    PubMed  CAS  Google Scholar 

  • Doehlemann G, Berndt P, Hahn M (2006) Different signalling pathways involving a G (alpha) protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol Microbiol 59:821–835

    PubMed  CAS  Google Scholar 

  • Dunwell JM, Gibbings JG, Mahmood T, Saqlan-Naqvi SM (2008) Germin and germin-like proteins: evolution, structure, and function. Crit Rev Plant Sci 27:342–375

    CAS  Google Scholar 

  • Edreva A (2005) Pathogenesis-related proteins: research progress in the last 15 years. Gen Appl Plant Physiol 31:105–124

    CAS  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R

    PubMed  CAS  Google Scholar 

  • Endah R, Beyene G, Kiggundu A, van den Berg N, Schlüter U, Kunert K, Chikwamba R (2008) Elicitor and fusarium-induced expression of NPR1-like genes in banana. Plant Physiol Biochem 46:1007–1014

    PubMed  CAS  Google Scholar 

  • Fahrendorf T, Ni W, Shorrosh BS, Dixon RA (1995) Stress responses in alfalfa (Medicago sativa L.) XIX. Transcriptional activation of oxidative pentose phosphate pathway genes at the onset of the isoflavonoid phytoalexin response. Plant Mol Biol 28:885–900

    PubMed  CAS  Google Scholar 

  • Ferreira R, Monteiro S, Freitas R, Santos C, Borges A, Chen Z, Batista L, Duarte J, Teixeira A (2007) The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 8:677–700

    PubMed  CAS  Google Scholar 

  • Foster AJ, Jenkinson JM, Talbot NJ (2003) Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. EMBO J 22:225–235

    PubMed  CAS  Google Scholar 

  • Frendo P, Harrison J, Norman C, Hernández-Jiménez MJ, Van de Sype G, Gilabert A, Puppo A (2005) Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Mol Plant–Microbe Interact 18:168–174

    Google Scholar 

  • Gao XP, Wang XF, Lu YF, Zhang LY, Shen YY, Liang Z, Zhang DP (2004) Jasmonic acid is involved in the water-stress-induced betaine accumulation in pear leaves. Plant Cell Environ 27:497–507

    CAS  Google Scholar 

  • Glazebrook J (1999) Genes controlling expression of defence responses in Arabidopsis. Curr Opin Plant Biol 2:280–286

    PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann Rev Phytopathol 43:205–227

    CAS  Google Scholar 

  • Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420

    PubMed  CAS  Google Scholar 

  • Gundlach H, Müller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci USA 89:2389–2393

    PubMed  CAS  Google Scholar 

  • Gurskaya NG, Diachenko L, Chenchik A, Siebert PD, Khaspekov GL, Lukyanov K, Vagner LL, Ermolaeva OD, Lukyanov S, Sverdlov ED (1996) The equalizing cDNA subtraction based on selective suppression of polymerase chain reaction: cloning of the Jurkat cells transcripts induced by phytohemaglutinin and phorbol 12-myristate 13-acetate. Anal Biochem 240:90–97

    PubMed  CAS  Google Scholar 

  • Hammond-Kosack KE, Kanyuka K (2007) Resistance genes (R genes) in plants. Encyclopedia of life sciences. John Wiley and Sons, ltd, London

    Google Scholar 

  • Harelimana G, Lepoivre P, Jijakli H, Mourichon X (1997) Use of Mycosphaerella fijiensis toxins for selection of banana cultivars resistant to black leaf streak. Euphytica 96:125–128

    Google Scholar 

  • Hayden HL, Carlier J, Aitken EAB (2003) The genetic structure of Mycosphaerella fijiensis from Australia, Papua New Guinea and the Pacific Islands. Plant Pathol 52:703–712

    CAS  Google Scholar 

  • Hidalgo W, Duque L, Saez J, Arango R, Gil J, Rojano B, Schneider B, Otálvaro F (2009) Structure-activity relationship in the interaction of substituted perinaphthenones with Mycosphaerella fijiensis. J Agric Food Chem 57:7417–7421

    PubMed  CAS  Google Scholar 

  • Horry JP, Jay M (1990) An evolutionary background of bananas as deduced from flavonoid diversification. In: Jarret RL (ed) Identification of genetic diversity in the genus Musa. INIBAP, Montpellier, pp 41–45

    Google Scholar 

  • Hoss R, Helbig J, Bochow H (2000) Function of host and fungal metabolites in resistance response of banana and plantain in the black sigatoka disease pathosystem (Musa spp.–Mycosphaerella fijiensis). J Phytopathol 148:387–394

    CAS  Google Scholar 

  • Hrazdina G, Jensen RA (1992) Spatial organization of enzymes in plant metabolic pathways. Annu Rev Plant Phys 43:241–267

    CAS  Google Scholar 

  • Huang X, Madan A (1999) CAP3: a DIVA sequence assembly program. Genome Res 9:868–877

    PubMed  CAS  Google Scholar 

  • Islas-Flores I, Peraza-Echevarria L, Canto-Canché B, Rodríguez-García CM (2006) Extraction of high-quality, melanin-free RNA from Mycosphaerella fijiensis for cDNA preparation. Mol Biotechnol 34:45–50

    PubMed  CAS  Google Scholar 

  • Johanson A, Jeger MJ (1993) Use of PCR for detection of Mycosphaerella fijiensis and M. musicola, the causal agents of sigatoka leaf spots on banana and plantain. Mycol Res 97:670–674

    Google Scholar 

  • Kachroo A, Venugopal SC, Lapchyk L, Falcone D, Hildebrand D, Kachroo P (2004) Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc Natl Acad Sci USA 101:5152–5157

    PubMed  CAS  Google Scholar 

  • Kader JC (1996) Lipid-transfer proteins in plants. Annu Rev Plant Phys 47:627–654

    CAS  Google Scholar 

  • Khayat E (2004) Discovery of functional genes in the Musa genome. In: Jain SM, Swennen R (eds) Banana improvement: cellular, molecular biology, and induced mutations. Science Publishers Inc, Enfield, pp 321–329

    Google Scholar 

  • Knaggs AR (2003) The biosynthesis of shikimate metabolites. Nat Prod Rep 20:119–136

    PubMed  CAS  Google Scholar 

  • Kombrink E, Somssich IE (1997) Pathogenesis-related proteins and plant defense. In: Carrol GC, Tudzynski P (eds) The mycota V part A, plant relationships. Springer-Verlag, Berlin, pp 107–128

    Google Scholar 

  • Kwon SJ, Jin HC, Lee S, Nam MH, Chung JH, Kwon SI, Ryu C, Park OK (2009) GDSL lipase-like 1 regulates systemic resistance associated with ethylene signaling in Arabidopsis. Plant J 58:235–245

    PubMed  CAS  Google Scholar 

  • Lepoivre P, Busogoro JP, Etame JJ, El Hadrami A, Carlier J, Harelimana G, Mourichon X, Panis B, Riveros AS, Salle G, Strosse H, Swennen R (2003) Banana–Mycosphaerella fijiensis interactions. In: Jacome L, Lepoivre P, Marin D, Ortiz R, Romero R, Escalant JV (eds) Mycosphaerella leaf spot diseases of bananas: present status and outlook. Proceedings of the second international workshop on Mycosphaerella leaf spot diseases, San José, pp 151–159

  • Li C, Liu G, Xu C, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA (2003) The tomato suppressor of prosystemin-mediated response2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15:1646–1661

    PubMed  CAS  Google Scholar 

  • Liao Z, Chen M, Gong Y, Tang F, Sun X, Tang K (2004) Rapid isolation of high-quality total RNA from Taxus and Ginkgo. Prep Biochem Biotechnol 34:209–214

    PubMed  CAS  Google Scholar 

  • Liebman JF, Greenberg A (1988) Mechanistic principles of enzyme activity. VCH Publishers, New York

    Google Scholar 

  • Liu X, Huang B, Lin J, Fei J, Chen Z, Pang P, Sun X, Tang T (2006) A novel pathogenesis-related protein (SsPR10) from Solanum surattense with ribonucleolytic and antimicrobial activity is stress and pathogen-inducible. J Plant Physiol 163:546–556

    PubMed  CAS  Google Scholar 

  • Livingstone JR, Maruo T, Yoshida I, Tarui Y, Hirooka K, Yamamoto Y, Tsutui N, Hirasawa E (2003) Purification and properties of betaine aldehyde dehydrogenase from Avena sativa. J Plant Res 116:133–140

    PubMed  CAS  Google Scholar 

  • Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8:532–540

    PubMed  CAS  Google Scholar 

  • Lorito M, Woo SL, D’Ambrosio M, Harman GE, Hayes CK, Kubicek CP, Scala F (1996) Synergistic interaction between cell wall degrading enzymes and membrane affecting compounds. Mol Plant–Microbe Interact 9:206–313

    CAS  Google Scholar 

  • Lowe RG, Lord M, Rybak K, Trengove RD, Oliver RP, Solomon PS (2009) Trehalose biosynthesis is involved in sporulation of Stagonospora nodorum. Fungal Genet Biol 46:381–389

    PubMed  CAS  Google Scholar 

  • Marín DH, Romero RA, Guzmán M, Sutton TB (2003) Black sigatoka: an increasing threat to banana cultivation. Plant Dis 87:208–222

    Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Phys 47:127–158

    CAS  Google Scholar 

  • May MJ, Vernoux T, Leaver C, Van Montague M, Inze D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667

    CAS  Google Scholar 

  • McCue KF, Conn EE (1989) Induction of 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase by fungal elicitor in cultures of Petroselinum crispum. Proc Natl Acad Sci USA 86:7374–7377

    PubMed  CAS  Google Scholar 

  • McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25:79–82

    PubMed  CAS  Google Scholar 

  • Meredith DS, Lawrence JS (1969) Black leaf streak disease of bananas (Mycosphaerella fijiensis): symptoms of disease in Hawaii, and notes on conidial state of causal fungus. Trans Br Mycol Soc 52:459–476

    Google Scholar 

  • Miller RNG, Bertioli DJ, Baurens FC, Santos CMR, Alves PC, Martins N, Togawa RC, Souza M, Pappas G Jr (2008) Analysis of non-TIR NBS-LRR resistance gene analogs in Musa acuminata Colla: isolation, RFLP marker development, and physical mapping. BMC Plant Biol 8:15

    PubMed  Google Scholar 

  • Mobambo KN, Gauhl F, Swennen R, Pasberg-Gauhl C (1996) Assessment of the cropping cycle effects of black leaf streak severity and yield decline of plantain and plantain hybrids. Int J Pest Manag 42:1–7

    Google Scholar 

  • Molina A, Segura A, Garcia-Olmedo F (1993) Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett 316:119–122

    PubMed  CAS  Google Scholar 

  • Mourichon X, Peter D, Zapater MF (1987) Inoculation experimentale de M. fijiensis Morelet sur jeunes plantules de bananier issues de culture in vitro. Fruits 42:195–198

    Google Scholar 

  • Neuefeind T, Reinemer P, Bieseler B (1997) Plant glutathione S-transferases and herbicide detoxification. Biol Chem 378:199–205

    PubMed  CAS  Google Scholar 

  • Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39:500–507

    CAS  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304

    PubMed  CAS  Google Scholar 

  • Oh IS, Park AR, Bae MS, Kwon SJ, Kim YS, Lee JE, Kang NY, Lee S, Cheong H, Park OK (2005) Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 17:2832–2847

    PubMed  CAS  Google Scholar 

  • Otálvaro F, Echeverri F, Quiñones W, Torres F, Schneider B (2002) Correlation between phenylphenalenone phytoalexins and phytopathological properties in Musa and the role of a dihydrophenylphenalene triol. Molecules 7:331–340

    Google Scholar 

  • Otálvaro F, Nanclares J, Vásquez LE, Quiñones W, Echeverri F, Arango R, Schneider B (2007) Phenalenone-type compounds from Musa acuminata var. ‘Yangambi km5′ (AAA) and their activity against Mycosphaerella fijiensis. J Nat Prod 70:887–890

    PubMed  Google Scholar 

  • Pasberg-Gauhl C, Gauhl F, Jones D (2000) Fungal disease of foliage. Sigatoka leaf spots. Black leaf streak. Distribution and economic importance. In: Jones DR (ed) Diseases of banana, abacá and enset. CABI Publishing, Wallingford, pp 37–44

    Google Scholar 

  • Pei X, Li S, Jiang Y, Zhang Y, Wang Z, Jia S (2007) Isolation, characterization and phylogenetic analysis of the resistance gene analogues (RGAs) in banana (Musa spp.). Plant Sci 172:1166–1174

    CAS  Google Scholar 

  • Peiser G, Wang TT, Hoffman NE, Yang SF, Liu HW, Walsh CT (1984) Formation of cyanide from carbon 1 of 1-aminocyclopropane-1-carboxylic acid during its conversion to ethylene. Proc Natl Acad Sci USA 81:3059–3063

    PubMed  CAS  Google Scholar 

  • Peraza-Echeverria S, James-Kay A, Canto-Canché B, Castillo-Castro E (2007) Structural and phylogenetic analysis of Pto-type disease resistance gene candidates in banana. Mol Genet Genomics 278:443–453

    PubMed  CAS  Google Scholar 

  • Piotrowski M, Volmer JJ (2006) Cyanide metabolism in higher plants: cyanoalanine hydratase is a NIT4 homolog. Plant Mol Biol 61:111–122

    PubMed  CAS  Google Scholar 

  • Pozo MJ, van Loon LC, Pieterse CMJ (2005) Jasmonates signals in plant–microbe interactions. J Plant Growth Regul 23:211–222

    Google Scholar 

  • Pyee J, Yu H, Kolattukudy PE (1994) Identification of a lipid transfer protein as a major protein in the surface wax of broccoli (Brassica oleracea) leaves. Arch Biochem Biophys 311:460–468

    PubMed  CAS  Google Scholar 

  • Quiñones W, Escobar G, Echeverri F, Torres F, Rosero Y, Arango V, Cardona G, Gallego A (2000) Synthesis and antifungal activity of Musa phytoalexins and structural analogs. Molecules 5:974–980

    Google Scholar 

  • Rasmussen S, Dixon RA (1999) Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11:1537–1552

    PubMed  CAS  Google Scholar 

  • Ratnakumar S, Tunnacliffe A (2006) Intracellular trehalose is neither necessary nor sufficient for desiccation tolerance in yeast. FEMS Yeast Res 6:902–913

    PubMed  CAS  Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411

    PubMed  CAS  Google Scholar 

  • Roberts WK, Selitrennikoff CP (1990) Zeamatin, an antifungal protein from maize with membrane permeabilizing activity. J Gen Microbiol 136:1771–1778

    CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Sánchez-Rodríguez A, Portal O, Rojas LE, Ocaña B, Mendoza-Rodríguez M, Acosta-Suárez M, Jiménez E, Höfte M (2008) An efficient method for the extraction of high-quality fungal total RNA to study the Mycosphaerella fijiensisMusa spp. interaction. Mol Biotechnol 40:299–305

    PubMed  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660

    PubMed  CAS  Google Scholar 

  • Segura A, Moreno F, García-Olmedo F (1993) Purification and antipathogenic activity of lipid transfer proteins (LTPs) from the leaves of Arabidopsis and spinach. FEBS Lett 332:243–246

    PubMed  CAS  Google Scholar 

  • Sels J, Mathys J, De Coninck B, Cammue BPA, De Bolle M (2008) Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem 46:941–950

    PubMed  CAS  Google Scholar 

  • Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang I, Lee JS, Choi YD (2001) Jasmonic Itranferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98:4788–4793

    PubMed  CAS  Google Scholar 

  • Somssich IK, Halbrock K (1998) Pathogen defense in plants a paradigm of biological complexity. Trends Plant Sci 3:86–90

    Google Scholar 

  • Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71

    PubMed  CAS  Google Scholar 

  • Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127

    PubMed  CAS  Google Scholar 

  • Stergiopoulos I, van den Burg HA, Okmen B, Beenen HG, van Liere S, Kema GH, de Wit PJ (2010) Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proc Natl Acad Sci USA 107:7610–7615

    PubMed  CAS  Google Scholar 

  • Sterk P, Booij H, Schellekens GA, Van Kammen A, De Vries SC (1991) Cell-specific expression of the carrot EP2 lipid transfer protein. Plant Cell 3:907–921

    PubMed  CAS  Google Scholar 

  • Strosse H, Van den Houwe I, Panis B (2004) Banana cell and tissue culture-review. In: Jain SM, Swennen R (eds) Banana improvement: cellular, molecular biology, and induced mutations. Science Publishers Inc, Enfield, pp 1–12

    Google Scholar 

  • Takayama K, Armstrong EL (1976) Isolation, characterization, and function of 6 mycolyl-6-acetyltrehalose in the H37Ra strain of Myocobacterium tuberculosis. Biochemistry 15:441–447

    PubMed  CAS  Google Scholar 

  • Theis T, Stahl U (2004) Antifungal proteins: targets, mechanisms and prospective applications. Cell Mol Life Sci 61:437–455

    PubMed  CAS  Google Scholar 

  • Thevelein JM (1984) Regulation of trehalose mobilization in fungi. Microb Rev 48:42–59

    CAS  Google Scholar 

  • Thomma BPHJ, Penninckx IAMA, Broekaert WF, Cammue BPA (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68

    PubMed  CAS  Google Scholar 

  • Umemura K, Ogawa N, Shimura M, Koga J, Usami H, Kono T (2003) Possible role of phytocassane, rice phytoalexin, in disease resistance of rice against the blast fungus Magnaporthe grisea. Biosci Biotechnol Biochem 67:899–902

    PubMed  CAS  Google Scholar 

  • van Etten HD, Mansfield JW, Bailey JA, Farmer EE (1994) Two classes of plant antibiotics: phytoalexins versus phytoanticipins. Plant Cell 6:1191–1192

    Google Scholar 

  • van Loon LC (2000) Systemic induced resistance. In: Slusarenko AJ, Fraser RSS, van Loon LC (eds) Mechanisms of resistance to plant diseases. Kluwer Academic Publishers, Dordrecht, pp 521–574

    Google Scholar 

  • van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Ann Rev Phytopathol 44:135–162

    Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (2000) Early accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction. Plant Physiol 123:1289–1300

    PubMed  CAS  Google Scholar 

  • Ververidis F, Trantas E, Douglas C, Vollmer G, Kretzschmar G, Panopoulos N (2007) Biotechnology of flavonoids and other phenylpropanoid-derived natural products. Part II: Reconstruction of multienzyme pathways in plants and microbes. Biotechnol J 2:1235–1249

    PubMed  CAS  Google Scholar 

  • von Dahl CC, Winz R, Halitschke R, Kühnemann F, Gase K, Baldwin IT (2007) Tuning the herbivore-induced ethylene burst: the role of transcripts accumulation and ethylene perception in Nicotiana attenuata. Plant J 51:293–307

    Google Scholar 

  • Wang Z, Thornton CR, Kersshaw MJ, Debao Li, Talbot NJ (2003) The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol Microbiol 47:1601–1612

    PubMed  CAS  Google Scholar 

  • Wang YD, Yuan YJ, Wu JC (2004) Induction studies of methyl jasmonate and salicylic acid on taxane production in suspension cultures of Taxus chinensis var. mairei. Biochem Eng J 19:259–265

    Google Scholar 

  • Weber H (2002) Fatty acid-derived signals in plants. Trends Plant Sci 7:217–224

    PubMed  CAS  Google Scholar 

  • Wingate VPM, Lawton MA, Lamb CJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210

    PubMed  CAS  Google Scholar 

  • Wuyts N, Lognay G, Verscheure M, Marlier M, De Waele D, Swennen R (2007) Potential physical and chemical barriers to infection by the burrowing nematode Radopholus similis in roots of susceptible and resistant banana (Musa spp.). Plant Pathol 56:878–890

    CAS  Google Scholar 

  • Yaeno T, Matsuda O, Iba K (2004) Role of chloroplast trienoic fatty acids in plant disease defense response. Plant J 40:931–941

    PubMed  CAS  Google Scholar 

  • Yang Q, Gong ZZ (2002) Purification and characterization of an ethylene-induced antifungal protein from leaves of guilder rose (Hydrangea macrophylla). Protein Expr Purif 24:76–82

    PubMed  CAS  Google Scholar 

  • Yang L, Guan T, Gerace L (1997) Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis. J Cell Biol 137:1199–1210

    PubMed  CAS  Google Scholar 

  • Yip WK, Yang SF (1998) Ethylene biosynthesis in relation to cyanide metabolism. Bot Bull Acad Sin 39:1–7

    CAS  Google Scholar 

  • Yun DJ, Zhao Y, Pardo JM, Narasimhan ML, Damsz B, Lee H, Abad LR, D’Urzo MP, Hasegawa PM, Bressan RA (1997) Stress proteins on the yeast cell surface determine resistance to osmotin, a plant antifungal protein. Proc Natl Acad Sci USA 94:7082–7087

    PubMed  CAS  Google Scholar 

  • Zhao JT, Huang X, Chen YP, Chen YF, Huang XL (2009) Molecular cloning and characterization of an ortholog of NPR1 gene from Dongguan Dajiao (Musa spp. ABB). Plant Mol Biol Rep 27:243–249

    CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Yelenys Alvarado-Capó (Instituto de Biotecnología de las Plantas, Cuba) for fruitful discussions concerning the design of the cDNA libraries construction. We are grateful to Luis Perez Vicente (INISAV, Cuba) and Joke Pannecoucque (Ghent University, Belgium) for critical comments on the manuscript. This research was performed in the frame of the Institutional University Cooperation Programme with Universidad Central “Marta Abreu” de Las Villas, supported by the Flemish Interuniversity Council (IUC UCLV/VLIR). This work also was supported in part by INIBAP (currently Bioversity International) through the project ‘Molecular analysis of Mycosphaerella fijiensis–banana interactions’ (LOA 2003-04). David De Vleesschauwer is indebted to the FWO-Vlaanderen for a postdoctoral fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Monica Höfte.

Additional information

Communicated by E. Guiderdoni.

O. Portal and Y. Izquierdo contributed equally to the article.

A contribution to the Special Issue: Plant Biotechnology in Support of the Millennium Development Goals.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Portal, O., Izquierdo, Y., De Vleesschauwer, D. et al. Analysis of expressed sequence tags derived from a compatible Mycosphaerella fijiensis–banana interaction. Plant Cell Rep 30, 913–928 (2011). https://doi.org/10.1007/s00299-011-1008-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-011-1008-z

Keywords

Navigation