cDNA-AFLP analysis of gene expression changes in apple trees induced by phytoplasma infection during compatible interaction

Aldaghi, Majid; Bertaccini, Assunta; Lepoivre, Philippe

doi:10.1007/s10658-012-9970-z

Article (Scientific journals)

cDNA-AFLP analysis of gene expression changes in apple trees induced by phytoplasma infection during compatible interaction

Aldaghi, Majid; Bertaccini, Assunta; Lepoivre, Philippe

2012 • In European Journal of Plant Pathology, 134, p. 117-130

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/130156

DOI
10.1007/s10658-012-9970-z

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

N°467 - Aldaghi 2012.pdf

Publisher postprint (662.83 kB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

apple; Ca. P. mali; cDNA-AFLP; Gene; Interaction; qRT-PCR

Abstract :

[en] Abstract In order to gain insight into molecular and physiological changes in apple trees during compatible interaction with two ‘Candidatus Phytoplasma mali’ strains (AP and AT), cDNA-Amplified Fragment Length Polymorphism (cDNA-AFLP) technique was used. A rootstock of apple (MM106) susceptible to ‘Ca. P. mali’ was used to extend the range of the potential host responses by the maximum number of identified genes that will be deregulated by phytoplasma in apple. Gene expression comparisons were studied in three directions: healthy versus infected samples, symptomatic versus nonsymptomatic sample, and AP-infected versus ATinfected sample. Forty-five genes whose steady-state levels of expression significantly changed in response to phytoplasma infection were identified. Among their partial cDNA sequences, only 27 showed similarity to DNA or protein data bases; of these, 18 were related to known genes in plants, and the rest were related to unknown or hypothetical proteins. Eighteen out of 45 did not show any similarity with sequences in data bases (potential novel genes). Quantitative real-time RT-PCR (qRT-PCR) was used to confirm differential expression of AFLP identified genes, and showed the similar profile expression for 11 known genes among 18, and for 13 unknown, hypothetical or novel genes among 27. Changes in gene expression involved a wide spectrum of biological functions, including processes of metabolism, cell defence, senescence, photosynthesis, transport, transcription, signal transduction and protein synthesis. This is the first study of global gene profiling in plants in response to phytoplasma infections using cDNA-AFLP, and a model is proposed to explain the mode of action of the ‘Ca. P. mali’ in apple.

Disciplines :

Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Aldaghi, Majid

Bertaccini, Assunta

Lepoivre, Philippe ; Université de Liège - ULiège > Sciences agronomiques > Phytopathologie

Language :

English

Title :

cDNA-AFLP analysis of gene expression changes in apple trees induced by phytoplasma infection during compatible interaction

Publication date :

2012

Journal title :

European Journal of Plant Pathology

ISSN :

0929-1873

eISSN :

1573-8469

Publisher :

Springer Science, Dordrecht, Netherlands

Volume :

134

Pages :

117-130

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 07 September 2012

Statistics

Number of views

157 (1 by ULiège)

Number of downloads

323 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389-3402.
Bachem, C. W. B., Oomen, R. J. F. J., & Visser, R. G. F. (1998). Transcript imaging with cDNA-AFLP: a step-by-step protocol. Plant Molecular Biology Reporter, 16, 157-173.
Bertaccini, A. (2007). Phytoplasmas: diversity, taxonomy, and epidemiology. Frontiers in Bioscience, 12, 673-689.
Bertamini, M., Muthuchelian, K., & Nedunchezhian, N. (2004). Effect of grapevine leafroll on the photosynthesis of field grown grapevine plants (Vitis vinifera L. cv. Lagrein). Journal of Phytopathology, 152, 145-152.
Breyne, P., & Zabeau, M. (2001). Genome-wide expression analysis of plant cell cycle modulated genes. Current Opinion in Plant Biology, 4, 136-142.
Brown, D. E., Rashotte, A. M., Murphy, A. S., Normanly, J., Tague, B. W., Peer, W. A., Taiz, L., & Muday, G. K. (2001). Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiology, 126, 524-535.
Campalans, A., Pages, M., & Messeguer, R. (2001). Identification of differentially expressed genes by the cDNA-AFLP technique during dehydration of almond. Tree Physiology, 21, 633-643.
Carginale, V., Maria, G., Capasso, C., Ionata, E., La Cara, F., Pastore, M., Bertaccini, A., & Capasso, A. (2004). Identification of genes expressed in response to phytoplasma infection in leaves of Prunus armeniaca by messenger RNA differential display. Gene, 332, 29-34.
Choi, Y. H., Tapias, E. C., Kim, H. K., Lefeber, A. W. M., Erkelens, C., Verhoeven, J. T. J., Brzin, J., Zel, J., & Verpoorte, R. (2004). Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using H-NMR spectroscopy and multivariate data analysis. Plant Physiology, 135, 2398-2410.
Chong, J., Baltz, R., Schmitt, C., Beffa, R., Fritig, B., & Saindrenan, P. (2002). Downregulation of a pathogen-responsive tobacco UDP-Glc: phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. The Plant Cell, 14, 1-15.
Collinge, M., & Bolle, r. T. (2001). Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Molecular Biology, 46, 521-529.
Donson, J., Fang, Y., Espiritu-Santo, G., Xing, W., Salazar, A., Miyamoto, S., Armendarez, V., & Volkmuth, W. (2002). Comprehensive gene expression analysis by transcript profiling. Plant Molecular Biology, 48, 75-95.
Durrant, W., Rowland, O., Piedras, P., Hammond-Kosack, K. E., & Jones, J. D. G. (2000). cDNA-AFLP reveals a striking overlap in race specific resistance and wound response gene expression profiles. The Plant Cell, 12, 963-977.
EPPO/CABI. (2006). Apple proliferation phytoplasma. In: Quarantine Pests for Europe, 2nd edn (pp. 959-962). Wallingford (GB): CAB International.
Frisinghelli, C., Delaiti, L., Grando, M. S., Forti, D., & Vindimian, M. E. (2000). Cacopsylla costalis (Flor 1861), as a vector of apple proliferation in Trentino. Journal of Phytopathology, 148, 425-431.
Frolov, A. E., Godwin, A. K., & Favorova, O. O. (2003). Differential gene expression analysis by DNA microarray technology and its application in molecular oncology. Molecular Biology, 37, 486-494.
Glazebrook, J. (2001). Genes controlling expression of defense responses in Arabidopsis-2001 status. Current Opinion in Plant Biology, 4, 301-308.
Goossens, K., van Poucke, M., van Soom, A., Vandesompele, J., van Zeveren, A., & Peelman, L. J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Developmental Biology, 5, 27. doi: 10. 1186/1471-213X-5-27.
Hernandez-Nistal, J., Labrador, E., Martin, I., Jiménez, T., & Dopico, B. (2006). Transcriptional profiling of cell wall protein genes in chickpea embryonic axes during germination and growth. Plant Physiology and Biochemistry, 44, 684-692.
Hoshi, A., Oshima, K., Kakizawa, S., Ishii, Y., Ozeki, J., Hashimoto, M., Komatsu, K., Kagiwada, S., Yamaji, Y., & Namba, S. (2009). A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. Proceedings of the National Academy of Sciences of USA, 106, 6416-6421.
IRPCM Phytoplasma/Spiroplasma Working Team-Phytoplasma Taxonomy Group. (2004). 'Candidatus Phytoplasma', a taxon for the wall-less, non-helical prokaryotes that colonize plant phloem and insects. International Journal of Systematic and Evolutionary Microbiology, 54, 1243-1255.
Jabs, T., Tschope, M., Colling, C., Hahlbrock, K., & Scheel, D. (1997). Elicitor-stimulated ion fluxes and O 2 - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proceedings of the National Academy of Sciences of USA, 94, 4800-4805.
Jagoueix-Eveillard, S., Tarendau, F., Guolter, K., Danet, J. L., Bové, J. M., & Garnier, M. (2001). Catharanthus roseus genes regulated differentially by mollicute infections. Molecular Plant-Microbe Interaction, 14, 225-233.
Jarausch, W., Lansac, M., & Dosba, F. (1996). Long-term maintenance of nonculturable apple-proliferation phytoplasmas in their micropropagated natural host plant. Plant Pathology, 45, 778-786.
Junqueira, A., Bedendo, I., & Pascholati, S. (2004). Biochemical changes in corn plants infected by the maize bushy stunt phytoplasma. Physiological and Molecular Plant Pathology, 65, 181-185.
Kearns, M. A., Monks, D. E., Fang, M., Rivas, M. P., Courtney, P. D., Chen, J., Prestwich, G. D., Theibert, A. B., Dewey, R. E., & Bankaitis, V. A. (1998). Novel developmentally regulated phosphoinositide binding proteins from soybean whose expression bypasses the requirement for an essential phosphatidylinositol transfer protein in yeast. The EMBO Journal, 17, 4004-4017.
Kvint, K., Nachin, L., Diez, A., & Nystrom, T. (2003). The bacterial universal stress protein: function and regulation. Current Opinion in Microbiology, 6, 140-145.
Lievens, S., Goormachtig, S., & Holsters, M. (2001). A critical evaluation of differential display as a tool to identify genes involved in legume nodulation: looking back and looking forward. Nucleic Acids Research, 29, 3459-3468.
Loi, N., Carraro, L., Musetti, R., Pertot, I., & Osler, R. (1995). Dodder transmission of two different MLOs from plum trees affected by "leptonecrosis". Acta Horticulturae, 386, 465-470.
Massart, S., & Jijakli, M. H. (2005). Identification of differentially expressed genes by cDNA-amplified fragment length polymorphism in the biocontrol agent Pichia anomala (strain Kh5). Phytopathology, 96, 80-86.
Maust, B. E., Espadas, F., Talavera, C., Aguilar, M., Santamaria, J. M., & Oropeza, C. (2003). Changes in carbohydrate metabolism in coconut palms infected with the lethal yellowing phytoplasma. Phytopathology, 93, 976-981.
Mayda, E., Marqués, C., Conejero, V., & Vera, P. (2000). Expression of a pathogen-induced gene can be mimicked by auxin insensitivity. Molecular Plant-Microbe Interaction, 13, 23-31.
Mills, J. C., Roth, K. A., Cagan, R. L., & Gordon, J. I. (2001). DNA microarrays and beyond: completing the journey from tissue to cell. Nature Cell Biology, 3, E175-E178.
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 Letters, 316, 119-122.
Moser, M., Sprenger, C., Bisognin, C., Velasco, R., & Jarausch, W. (2007). Gene expression study in different 'Ca. Phytoplasma mali'-infected micropropagated Malus genotypes. Bulletin of Insectology, 60, 207-208.
Musetti, R., Sanita di Toppi, L., Ermacora, P., & Favali, M. A. (2004). Recovery in apple trees infected with the apple proliferation phytoplasma: an ultrastructural and biochemical study. Phytopathology, 94, 203-208.
Musetti, R., Favali, M. A., & Pressacco, L. (2000). Histopathology and polyphenol content in plants infected by phytoplasma. Cytobios, 102, 133-147.
Neill, S. J., & Burnett, E. C. (1999). Regulation of gene expression during water-deficit stress. Plant Growth Regulation, 29, 23-33.
Ooka, H., Satoh, K., Doi, K., Nagata, T., Otomo, Y., Murakami, K., Matsubara, K., Osato, N., Kawai, J., Carninci, P., et al. (2003). Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Research, 10, 239-247.
Pracros, P., Renaudin, J., Eveillard, S., Mouras, A., & Hernould, M. (2006). Tomato flower abnormalities induced by stolbar phytoplasma infection are associated with changes in expression of floral development genes. Molecular Plant-Microbe Interaction, 19, 62-68.
Quirino, B. F., Normanly, J., & Amasino, R. M. (1999). Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Molecular Biology, 40, 267-278.
Ramakers, C., Ruijter, J. M., Lekanne Deprez, R. H., & Moorman, A. F. M. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters, 339, 62-66.
Reijans, M., Lascaris, R., Groeneger, A. O., Wittenberg, A., Wesselink, E., van Oeveren, J., et al. (2003). Quantitative comparison of cDNA-AFLP, microarrays, and GeneChip expression data in Saccharomyces cerevisiae. Genomics, 82, 606-618.
Ren, T., Qu, F., & Morris, T. J. (2000). HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. The Plant Cell, 12, 1917-1925.
Rodriguez, P. L. (1998). Protein phosphatase 2 C (PP2C) function in higher plants. Plant Molecular Biology, 38, 919-927.
Schweighofer, A., Hirt, H., & Meskiene, I. (2004). Plant PP2C phosphatases: emerging functions in stress signaling. TRENDS in Plant Science, 9, 236-243.
Seemüller, E., Lorenz, K. H., & Lauer, U. (1998). Pear decline resistance in Pyrus communis rootstocks and progenies of wild and ornamental Pyrus taxa. Acta Horticulturae, 472, 681-690.
Seemüller, E., Marcone, C., Lauer, U., Ragozzino, A., & Goschl, M. (1998). Current status of molecular classification of the phytoplasmas. Journal of Plant Pathology, 80, 3-26.
Souer, E., von Houwelingen, A., Kloos, D., Mol, J., & Koes, R. (1996). The No Apical Meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell, 85, 159-170.
Spoel, S. H., Koornneef, A., Claessens, S. M. C., Korzelius, J. P., van Pelt, M. J., Mueller, A. J., et al. (2003). NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. The Plant Cell, 15, 760-770.
Szymanski, M., Deniziak, M., & Barciszewski, J. (2000). The new aspects of aminoacyl-tRNA synthetases. Acta Biochimica Polonica, 47, 821-834.
Tan, P. Y., & Whitlow, T. (2001). Physiological responses of Catharanthus roseus (periwinkle) to ash yellows phytoplasmal infection. New Phytologist, 150, 757-769.
Uwer, U., Willmitzer, L., & Altmann, T. (1998). Inactivation of a glycyl-tRNA synthetase leads to an arrest in plant embryo development. The Plant Cell, 10, 1277-1294.
Vandesompele, J., De Paepe, A., & Speleman, F. (2002). Elimination of primer dimer artifacts and genomic coamplification using a two step SYBR Green I real-time RT-PCR. Analytical Biochemistry, 303, 95-98.
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., van Roy, N., De Paepe, A., & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR by geometric averaging of multiple internal control genes. Genome Biology, 3, research0034. 1-0034. 12.
Venkatesh, B., Hettwer, U., Koopmann, B., & Karlovsky, P. (2005). Conversion of cDNA differential display results (DDRT-PCR) into quantitative transcription profiles. BMC Genomics, 6, 51. doi: 10. 1186/1471-2164-6-51.
Walker, N. J. (2002). A technique whose time has come. Science, 296, 557-559.
Wan, J., Dunning, F. M., & Bent, A. F. (2002). Probing plant-pathogen interactions and downstream defense signaling using DNA microarrays. Functional and Integrative Genomics, 2, 259-273.
Xie, Q., Sanz-Burgos, A. P., Guo, H., Garcia, J. A., & Gutierrez, C. (1999). GRAB proteins, novel members of the NAC domain family, isolated by their interaction with a geminivirus protein. Plant Molecular Biology, 39, 647-656.
Xiong, L., Schumaker, K. S., & Zhu, J. K. (2002). Cell signaling during cold, drought, and salt stress. The Plant Cell, 14, S165-S183.
Yang, Q., Reinhard, K., Schiltz, E., & Matern, U. (1997). Characterization and heterologous expression of hydroxycinnamoyl/benzoyl-CoA: anthranilate N-hydroxycinnamoyl-benzoyl-transferase from elicited cell cultures of carnation, Dianthus caryophyllus L. Plant Molecular Biology, 35, 777-789.
Yang, L., Zheng, B., Mao, C., Yi, K., Liu, F., Wu, Y., Tao, Q., & Wu, P. (2003). cDNA-AFLP analysis of inducible gene expression in rice seminal root tips under a water deficit. Gene, 314, 141-148.