Abstract
Black pepper (Piper nigrum L.) is one of the most widely used spices in the world. Root rot disease is induced by Fusarium solani f. sp. piperis and causes severe yield losses of this crop in the Amazon region. In this work we used the suppression subtractive hybridization to identify differentially expressed sequences in roots of black pepper infected by F. solani f. sp. piperis. Sequences coding for putative proteins related to oxidative burst and defense response, such as superoxide dismutase, cytochrome p450, and alpha-amylase inhibitors/lipid transfer protein, comprised 28.4% of SSH clones according to computational analyses. Furthermore, semi-quantitative RT-PCR assays showed accumulation of putative cysteine proteinase inhibitor and pathogenesis-related protein 4 transcripts at late stage of infection that can help to explain the success of this pathogen in causing root rot disease in black pepper. The results obtained here contribute to improve our understanding about this plant–pathogen interaction.
References
Albuquerque FC, Ferraz S (1976) Características morfológicas e fisiológicas de Nectria haematococca f. sp. piperis e sua patogenicidade à pimenta do reino (Piper nigrum L.). Experientia 22:133–151
Albuquerque FC, Duarte MLR, Benchimol RL, Endo T (2001) Resistência de piperáceas nativas da Amazônia à infecção causada por Nectria heamatococca f. sp. piperis. Acta Amaz 31:341–348
Alex SM, Dicto J, Purushothama MG, Manjula S (2008) Differential expression of metallothionein type-2 homologues in leaves and roots of black pepper (Piper nigrum L). Genet Mol Biol 31:551–554
Alfano JR, Collmer A (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683–1698
Altschul SF, Madden TL, Shaffer AA, Zhang J, Zangh Z, Miller W, Lipman DJ (1997) Gapped Blast and PSI-BLAST, a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:1–20
Aslam M, Sinha VB, Singh RK, Anandhan S, Pande V, Ahmed Z (2010) Isolation of cold stress-responsive genes from Lepidium latifolium by suppressive subtraction hybridization. Acta Physiol Plant 32:205–210
Bell JN, Ryder TB, Wingate VP, Bailey JA, Lamb CJ (1986) Differential accumulation of plant defense gene transcripts in a compatible and an incompatible plant–pathogen interaction. Mol Cell Biol 6:1615–1623
Carnaúba JP, Sobral MF, da Rocha Amorim EP, Silva IO (2007) Report of Fusarium solani f. sp. piperis in Piper nigrum in the state of Alagoas. Summa Phytopathol 33:96–97
Degenhardt J, Al-Masri AN, Kürkcüoglu S, Szankowski I, Gau AE (2005) Characterization by suppression subtractive hybridization of transcripts that are differentially expressed in leaves of apple scab-resistant and susceptible cultivars of Malus domestica. Mol Genet Genomics 273:326–335
Desender S, Andrivon D, Val F (2007) Activation of defence reactions in Solanaceae: where is the specificity? Cell Microbiol 9:21–30
Develey-Rivière MP, Galiana E (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytol 175:405–416
Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (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
Espelie KE, Franceschi VR, Kolattukudy PE (1986) Immunocytochemical localization and time course of appearance of an anionic peroxidase associated with suberization in wound-healing potato tuber tissue. Plant Physiol 81:487–492
Fan F, Li X-W, Wu Y-M, Xia Z-S, Li J-J, Zhu W, Liu J-X (2010) Differential expression of expressed sequence tags in alfalfa roots under aluminum stress. Acta Physiol Plant. doi: 10.1007/s11738-010-0577-8
Fekete C, Fung RWM, Szabód Z, Qiu W, Chang L, Schachtman DP, Kovács LG (2009) Up-regulated transcripts in a compatible powdery mildew–grapevine interaction. Plant Physiol Biochem 47:732–738
Geddes J, Eudes F, Laroche A, Selinger LB (2008) Differential expression of proteins in response to the interaction between the pathogen Fusarium graminearum and its host, Hordeum vulgare. Proteomics 8:545–554
Ghose K, Dey S, Barton H, Loake GJ, Basu D (2008) Differential profiling of selected defence-related genes induced on challenge with Alternaria brassiciola in resistant white mustard and their comparative expression pattern in susceptible India mustard. Mol Plant Pathol 9:763–775
Gor MC, Ismail I, Mustapha WAW, Zainal Z, Noor NM, Othman R, Hussein ZAM(2010) Identification of cDNAs for jasmonic acid-responsive genes in Polygonum minus roots by suppression subtractive hybridization. Acta Physiol Plant doi: 10.1007/s11738-010-0546-2
Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress. Plant Physiol 103:1067–1073
Hamada M, Uchida T, Tsuda M (1988) Ascospore dispersion of the causal agent of Nectria Blight of Piper nigrum. Annals of the Phytopathological Society of Japan 54(3):303–308
Hirsch J, Deslandes L, Feng DX, Balagué C, Marco Y (2002) Delayed symptom development in ein2–1, an Arabidopsis ethylene-insensitive mutant, in response to bacterial wilt caused by Ralstonia solanacearum. Phytopathology 92:1142–1148
Ikeda K (2010) Role of perithecia as an inoculum source for stem rot type of pepper root rot caused by Fusarium solani f. sp. piperis (teleomorph: Nectria haematococca f. sp. piperis). J Gen Plant Pathol 76:241–246
Jakobek JL, Smith JA, Lindgren PB (1993) Suppression of bean defense by Pseudomonas syringae. Plant Cell 5:57–63
Jaramillo MA, Manos PS (2001) Phylogeny and patterns of diversity in the genus Piper (Piperaceae). Am J Bot 88:706–716
Jones JDG, Dunsumuir P, Bedbrook J (1985) High level expression of introduced chimaeric genes in regenerated transformed plants. EMBO J 4:2411–2418
Joshi BN, Sainani MN, Bastawade KB, Gupta VS, Ranjekar PK (1998) Cysteine protease inhibitor from Pearl Millet: a new class of antifungal protein. Biochem Biophys Res Commun 246:382–387
Kim YC, Kim SY, Paek KH, Choi D, Park JM (2006) Suppression of CaCYP1, a novel cytochrome P450 gene, compromises the basal pathogen defense response of pepper plants. Biochem Biophys Res Commun 345:638–645
Kobae Y, Sekino T, Yoshioka H, Nakagawa T, Martinoia E, Maeshima M (2006) Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol 47:309–318
Kué J (1997) Molecular aspects of plant responses to pathogens. Acta Physiol Plant 19:551–559
Latha AM, Rao KV, Reddy VD (2005) Production of transgenic plants resistant to leaf blast disease in finger millet (Eleusine coracana (L.) Gaertn.). Plant Sci 169:657–667
Li X, Xia B, Jiang Y, Wu Q, Wang C, He L, Peng F, Wang R (2010) A new pathogenesis-related protein, LrPR4, from Lycoris radiata, and its antifungal activity against Magnaporthe grisea. Mol Biol Rep 37:995–1001
Luo M, Kong X, Huo N, Zhou R, Jia J (1990) Gene expression profiling related to powdery mildew resistance in wheat with the method of suppression subtractive hybridization. Chin Sci Bull 47:1990–1994
Mandal S, Das RK, Mishra S (2011) Differential occurrence of oxidative burst and antioxidative mechanism in compatible and incompatible interactions of Solanum lycopersicum and Ralstonia solanacearum. Plant Physiol Biochem 49:117–123
Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu U, Muller-Rober B, Schulz B (2002) Multifunctionality of plant ABC transporters-more than just detoxifiers. Planta 214:345–355
Monk SL, Fagerstedt KV, Crawford RMM (1989) Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress. Physiol Plant 76:456–459
Mukherjee AK, Lev S, Gepstein S, Horwitz BA (2009) A compatible interaction of Alternaria brassicicola with Arabidopsis thaliana ecotype DiG: evidence for a specific transcriptional signature. BMC Plant Biol 9:31
Nascimento SB, Cascardo JCM, de Menezes IC, Duarte MLR, Darnet SH, Harada ML, de Souza CRB (2009) Identifying sequences potentially related to resistance response of Piper tuberculatum to Fusarium solani f. sp. piperis by suppression subtractive hybridization. Protein Pept Lett 12:1429–1434
O’Donnel K (2000) Molecular phylogeny of the Nectria haematococca–Fusarium solani species complex. Mycologia 92:919–938
Oh BJ, Ko MK, Kim YS, Kim KS, Kostenyuk I, Kee HK (1999) A cytochrome P450 gene is differentially expressed in compatible and incompatible interactions between pepper (Capsicum annuum) and the anthracnose fungus, Colletotrichum gloeosporioides. Mol Plant Microbe Interact 12:1044–1052
Pagano EA, Chueca A, Lopez-Gorge J (2000) Expression of thioredoxins f and m, and of their targets fructose-1, 6-bisphosphatase and NADP-malate dehydrogenase, in pea plants grown under normal and light/temperature stress conditions. J Exp Bot 51:1299–1307
Rinaldi C, Kohler A, Frey P, Duchaussoy F, Ningre N, Couloux A, Wincker P, Le Thiec D, Fluch S, Martin F, Duplessis S (2007) Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melampsora larici-populina. Plant Physiol 144:347–366
Roberts MR, Salinas J, Collinge DB (2002) 14-3-3 proteins and the response to abiotic and biotic stress. Plant Mol Biol 50:1031–1039
Sánchez-Fernández R, Davies TG, Coleman JO, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244
Schlink K (2010) Down-regulation of defense genes and resource allocation into infected roots as factors for compatibility between Fagus sylvatica and Phytophthora citricola. Funct Integr Genomics 10:253–264
Soltis PA, Soltis DE, Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402–404
Subramanian B, Bansal VK, Kav NNV (2005) Proteome-level investigation of Brassica carinata-derived resistance to Leptosphaeria maculans. J Agric Food Chem 53:313–324
Torii KU (2004) Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int Rev Cytol 234:1–46
Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308(5724):1036–1040
Zhu T, Song TF, Zheng Z (2006) Molecular characterization of the rice pathogenesis related protein, OsPR-4b and its antifungal activity against Rhizoctonia solani. J Phytopathol 154:378–384
Zuo KJ, Qin J, Zhao JY, Ling H, Zhang LD, Cao YF, Tang KX (2007) Over-expression of GbERF2 transcription factors in tobacco enhanced brown spots disease resistance by activating expression of downstream genes. Gene 391:80–90
Acknowledgments
Research supported by: the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes), the Fundação de Amparo à Pesquisa do Estado do Pará (FAPESPA), and the Universidade Federal do Pará (UFPA), Brazil. The authors thank Maria de Lourdes Reis Duarte for providing the fungus strain and Soelange Bezerra do Nascimento for help in the plant material preparation.
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Communicated by T. Moriguchi.
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de Souza, C.R.B., Brígida, A.B.S., Santos, R.C.d. et al. Identification of sequences expressed during compatible black pepper—Fusarium solani f. sp. piperis interaction. Acta Physiol Plant 33, 2553–2560 (2011). https://doi.org/10.1007/s11738-011-0788-7
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DOI: https://doi.org/10.1007/s11738-011-0788-7