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Basal differences in the transcriptional profiles of tomato leaves associated with the presence/absence of the resistance gene Mi-1 and changes in these differences after infestation by the whitefly Bemisia tabaci

Published online by Cambridge University Press:  09 December 2019

Clara I. Rodríguez-Alvarez ,
Irene López-Vidriero ,
José M. Franco-Zorrilla  and
Gloria Nombela Open the ORCID record for Gloria Nombela [Opens in a new window]
Clara I. Rodríguez-Alvarez
Affiliation:
Department of Plant Protection Institute for Agricultural Sciences (ICA), Spanish National Research Council (CSIC), Serrano 115 Dpdo., Madrid28006, Spain
Irene López-Vidriero
Affiliation:
Genomics Unit, Centro Nacional de Biotecnología (CNB), Spanish National Research Council (CSIC), Darwin 3, Madrid28049, Spain
José M. Franco-Zorrilla
Affiliation:
Genomics Unit, Centro Nacional de Biotecnología (CNB), Spanish National Research Council (CSIC), Darwin 3, Madrid28049, Spain
Gloria Nombela*
Affiliation:
Department of Plant Protection Institute for Agricultural Sciences (ICA), Spanish National Research Council (CSIC), Serrano 115 Dpdo., Madrid28006, Spain
*
Author for correspondence: Gloria Nombela, Email: gnombela@ica.csic.es
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Abstract

The tomato Mi-1 gene mediates plant resistance to whitefly Bemisia tabaci, nematodes, and aphids. Other genes are also required for this resistance, and a model of interaction between the proteins encoded by these genes was proposed. Microarray analyses were used previously to identify genes involved in plant resistance to pests or pathogens, but scarcely in resistance to insects. In the present work, the GeneChip™ Tomato Genome Array (Affymetrix®) was used to compare the transcriptional profiles of Motelle (bearing Mi-1) and Moneymaker (lacking Mi-1) cultivars, both before and after B. tabaci infestation. Ten transcripts were expressed at least twofold in uninfested Motelle than in Moneymaker, while other eight were expressed half or less. After whitefly infestation, differences between cultivars increased to 14 transcripts expressed more in Motelle than in Moneymaker and 14 transcripts less expressed. Half of these transcripts showed no differential expression before infestation. These results show the baseline differences in the tomato transcriptomic profile associated with the presence or absence of the Mi-1 gene and provide us with valuable information on candidate genes to intervene in either compatible or incompatible tomato–whitefly interactions.

Keywords

Bemisia tabaciMi-1 geneplant resistancetomatotranscriptional profilewhiteflies
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 4 , August 2020 , pp. 463 - 479
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Copyright
Copyright © Cambridge University Press 2019

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References

Aarts, JMMJG, Hontelez, JGJ, Fischer, P, Verkerk, R, van Kammen, A and Zabel, P (1991) Acid phosphatase-1 1, a tightly linked molecular marker for root-knot nematode resistance in tomato: from protein to gene, using PCR and degenerate primers containing deoxyinosine. Plant Molecular Biology 16, 647–661.CrossRefGoogle ScholarPubMed
Achard, P, Cheng, H, De Grauwe, L, Decat, J, Schoutteten, H, Moritz, T, Van Der Straeten, D, Peng, J and Harberd, NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91–94.CrossRefGoogle ScholarPubMed
Aharoni, A and Vorst, O (2001) DNA microarrays for functional plant genomics. Plant Molecular Biology 48, 99–118.CrossRefGoogle Scholar
Alkharouf, NW, Klink, VP, Chouikha, IB, Beard, HS, MacDonald, MH, Meyer, S, Knap, HT, Khan, R and Matthews, BF (2006) Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224, 838–852.CrossRefGoogle Scholar
Babiychuk, E, Kushnir, S, Belles-Boix, E, Van Montagu, M and Inze, D (1995) Arabidopsis thaliana NADPH oxidoreductase homologs confer tolerance of yeasts toward the thiol-oxidizing drug diamide. Journal of Biological Chemistry 270, 26224–26231.CrossRefGoogle ScholarPubMed
Balaji, V, Mayrose, M, Sherf, O, Jacob-Hirsch, J, Eichenlaub, R, Iraki, N, Manulis-Sasson, S, Rechavi, G, Barash, I and Sessa, G (2008) Tomato transcriptional changes in response to Clavibacter michiganensis subsp. michiganensis reveal a role for ethylene in disease development. Plant Physiology 146, 1797–1809.CrossRefGoogle ScholarPubMed
Barcala, M, García, A, Cabrera, J, Casson, S, Lindsey, K, Favery, B, García-Casado, G, Solano, R and Escobar, C (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant Journal 61, 698–712.CrossRefGoogle ScholarPubMed
Bari, R and Jones, JDG (2009) Role of plant hormones in plant defence responses. Plant Molecular Biology 69, 473–488.CrossRefGoogle ScholarPubMed
Bar-Or, C, Kapulnik, Y and Koltai, H (2005) A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root knot nematode Meloidogyne javanica. European Journal of Plant Pathology 111, 181–192.CrossRefGoogle Scholar
Baumann, MJ, Eklöf, JM, Michel, G, Kallas, AM, Teeri, TT, Czjzek, M and Brumer, H (2007) Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases: biological implications for cell wall metabolism. The Plant Cell 19, 1947–1963.CrossRefGoogle ScholarPubMed
Bechtold, U, Murphy, DJ and Mullineaux, PM (2004) Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. The Plant Cell 16, 908–919.CrossRefGoogle ScholarPubMed
Bendix, CL (2015) The time has come: of GIGANTEA paralogs and grass circadian clocks. University of California, Berkeley, 224 pp.Google Scholar
Benjamini, Y and Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289–300.CrossRefGoogle Scholar
Berrar, DP, Downes, CS and Dubitzky, W (2003) Multiclass cancer classification using gene expression profiling and probabilistic neural networks. Pacific Symposium on Biocomputing 8, 5–16.Google Scholar
Bhattarai, KK, Atamian, HS, Kaloshian, I and Eulgem, T (2010) WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. Plant Journal 63, 229–240.CrossRefGoogle ScholarPubMed
Bhattarai, KK, Li, Q, Liu, Y, Dinesh-Kumar, SP and Kaloshian, I (2007) The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiology 144, 312–323.CrossRefGoogle ScholarPubMed
Bhattarai, KK, Xie, Q-G, Mantelin, S, Bishnoi, U, Girke, T, Navarre, DA and Kaloshian, I (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Molecular Plant-Microbe Interactions 21, 1205–1214.CrossRefGoogle ScholarPubMed
Biermann, BJ, Morehead, TA, Tate, SE, Price, JR, Randall, SK and Crowell, DN (1994) Novel isoprenylated proteins identified by an expression library screen. Journal of Biological Chemistry 269, 25251–25254.Google ScholarPubMed
Bolle, C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218, 683–692.CrossRefGoogle ScholarPubMed
Bonshtien, A, Lev, A, Gibly, A, Debbie, P, Avni, A and Sessa, G (2005) Molecular properties of the Xanthomonas avrrxv effector and global transcriptional changes determined by its expression in resistant tomato plants. Molecular Plant-Microbe Interactions: MPMI 18, 300–310.CrossRefGoogle ScholarPubMed
Boyko, EV, Smith, CM, Thara, VK, Bruno, JM, Deng, Y, Starkey, SR and Klaahsen, DL (2006) Molecular basis of plant gene expression during aphid invasion: wheat Pto- and Pti-like sequences are involved in interactions between wheat and Russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology 99, 1430–1445.CrossRefGoogle Scholar
Busi, MV, Bustamante, C, D'Angelo, C, Hidalgo-Cuevas, M, Boggio, SB, Valle, EM and Zabaleta, E (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Molecular Biology 52, 801–815.Google ScholarPubMed
Casteel, CL, Walling, LL and Paine, TD (2006) Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene. Entomologia Experimentalis et Applicata 121, 67–72.CrossRefGoogle Scholar
Cho, SK, Jung, KW, Jeung, JU, Kang, KH, Shim, KS, You, MK, Yoo, KS, Ok, SH and Shin, JS (2005) Analysis of differentially expressed transcripts from planthopper-infested wild rice (Oryza minuta). Plant Cell Reports 24, 59–67.CrossRefGoogle Scholar
Coelho, AC, Horta, M, Neves, D and Cravador, A (2006) Involvement of a cinnamyl alcohol dehydrogenase of Quercus suber in the defence response to infection by Phytophthora cinnamomi. Physiological and Molecular Plant Pathology 69, 62–72.CrossRefGoogle Scholar
De Barro, PJ, Liu, S-S, Boykin, LM and Dinsdale, AB (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1–19.CrossRefGoogle ScholarPubMed
De Bruyne, L, Höfte, M and De Vleesschauwer, D (2014) Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Molecular Plant 7, 943–959.CrossRefGoogle ScholarPubMed
De Vos, M, Jae, HK and Jander, G (2007) Biochemistry and molecular biology of Arabidopsis-aphid interactions. BioEssays 29, 871–883.CrossRefGoogle ScholarPubMed
Delp, G, Gradin, T, Åhman, I and Jonsson, LMV (2009) Microarray analysis of the interaction between the aphid Rhopalosiphum padi and host plants reveals both differences and similarities between susceptible and partially resistant barley lines. Molecular Genetics and Genomics 281, 233–248.CrossRefGoogle ScholarPubMed
Di Laurenzio, L, Wysocka-Diller, J, Malamy, JE, Pysh, L, Helariutta, Y, Freshour, G, Hahn, MG, Feldmann, KA and Benfey, PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423–433.CrossRefGoogle ScholarPubMed
Ding, Y, Wei, W, Wu, W, Davis, RE, Jiang, Y, Lee, IM, Hammond, RW, Shen, L, Sheng, JP and Zhao, Y (2013) Role of gibberellic acid in tomato defence against potato purple top phytoplasma infection. Annals of Applied Biology 162, 191–199.CrossRefGoogle Scholar
Dixon, RA (2001) Natural products and plant disease resistance. Nature 411, 843–847.CrossRefGoogle ScholarPubMed
Dropkin, V (1969) The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 59, 1632–1637.Google Scholar
Dykema, PE, Sipes, PR, Marie, A, Biermann, BJ, Crowell, DN and Randall, SK (1999) A new class of proteins capable of binding transition metals. Plant Molecular Biology 41, 139–150.CrossRefGoogle ScholarPubMed
Eckardt, NA (2003) Viral defense and counterdefense: a role for adenosine kinase in innate defense and RNA silencing. Plant Cell 15, 2758–2762.CrossRefGoogle Scholar
Egelund, J, Skjot, M, Geshi, N, Ulvskov, P and Petersen, BL (2004) A complementary bioinformatics approach to identify potential plant cell wall glycosyltransferase-encoding genes. Plant Physiology 136, 2609–2620.CrossRefGoogle ScholarPubMed
Estrada-Hernández, MG, Valenzuela-Soto, JH, Ibarra-Laclette, E and Délano-Frier, JP (2009) Differential gene expression in whitefly Bemisia tabaci-infested tomato (Solanum lycopersicum) plants at progressing developmental stages of the insect's life cycle. Physiologia Plantarum 137, 44–60.CrossRefGoogle ScholarPubMed
FAOSTAT (2001) FAOSTAT Online Database. Available at http://www.fao.org/land-water/databases-and-software/crop-information/tomato/en.Google Scholar
Farré, EM and Liu, T (2013) The PRR family of transcriptional regulators reflects the complexity and evolution of plant circadian clocks. Current Opinion in Plant Biology 16, 621–629.CrossRefGoogle ScholarPubMed
Fernandez-Pozo, N, Menda, N, Edwards, JD, Saha, S, Tecle, IY, Strickler, SR, Bombarely, A, Fisher-York, T, Pujar, A, Foerster, H, Yan, A and Mueller, LA (2015) The Sol Genomics Network (SGN) – from genotype to phenotype to breeding. Nucleic Acids Research 43, D1036–D1041.CrossRefGoogle ScholarPubMed
Finnegan, EJ, Peacock, WJ and Dennis, ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proceedings of the National Academy of Sciences 93, 8449–8454.CrossRefGoogle ScholarPubMed
Fukuda, Y (1996) Coordinated activation of chitinase genes and extracellular alkalinization in suspension-cultured tobacco cells. Bioscience, Biotechnology, and Biochemistry 60, 2005–2010.CrossRefGoogle Scholar
Gady, ALF, Vriezen, WH, Van de Wal, MHBJ, Huang, P, Bovy, AG, Visser, RGF and Bachem, CWB (2012) Induced point mutations in the phytoene synthase 1 gene cause differences in carotenoid content during tomato fruit ripening. Molecular Breeding: New Strategies in Plant Improvement 29, 801–812.CrossRefGoogle ScholarPubMed
Goggin, FL, Shah, G, Williamson, VM and Ullman, DE (2004) Developmental regulation of Mi-mediated aphid resistance is independent of Mi-1.2 transcript levels. Molecular Plant-Microbe Interactions: MPMI 17, 532–536.CrossRefGoogle ScholarPubMed
Hammes, UZ, Schachtman, DP, Berg, RH, Nielsen, E, Koch, W, McIntyre, LM and Taylor, CG (2005) Nematode-induced changes of transporter gene expression in Arabidopsis roots. Molecular Plant-Microbe Interactions: MPMI 18, 1247–1257.CrossRefGoogle ScholarPubMed
Harberd, NP (2003) Relieving DELLA restraint. Science 299, 1853–1854.CrossRefGoogle ScholarPubMed
Ho, J-Y, Weide, R, Ma, HM, van Wordragen, MF, Lambert, KN, Koornneef, M, Zabel, P and Williamson, VM (1992) The root-knot nematode resistance gene (Mi) in tomato: construction of a molecular linkage map and identification of dominant cDNA markers in resistant genotypes. The Plant Journal 2, 971–982.Google ScholarPubMed
Hor, L, Dobson, RCJ, Downton, MT, Wagner, J, Hutton, CA and Perugini, MA (2013) Dimerization of bacterial diaminopimelate epimerase is essential for catalysis. Journal of Biological Chemistry 288, 9238–9248.CrossRefGoogle ScholarPubMed
Huang, S, Chen, X, Zhong, X, Li, M, Ao, K, Huang, J and Li, X (2016) Plant TRAF proteins regulate NLR immune receptor turnover. Cell Host and Microbe 19, 204–215.CrossRefGoogle ScholarPubMed
Hwang, CF and Williamson, VM (2003) Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi. Plant Journal 34, 585–593.CrossRefGoogle ScholarPubMed
Ibrahim, HMM, Hosseini, P, Alkharouf, NW, Hussein, EHA, Gamal El-Din, AEKY, Aly, MAM and Matthews, BF (2011) Analysis of Gene expression in soybean (Glycine max) roots in response to the root knot nematode Meloidogyne incognita using microarrays and KEGG pathways. BMC Genomics 12, 220–236.CrossRefGoogle ScholarPubMed
Irizarry, RA, Bolstad, BM, Collin, F, Cope, LM, Hobbs, B and Speed, TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Research 31, e15.CrossRefGoogle ScholarPubMed
Jabs, T, Tschope, M, Colling, C, Hahlbrock, K and Scheel, D (1997) Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proceedings of the National Academy of Sciences 94, 4800–4805.CrossRefGoogle ScholarPubMed
Jammes, F, Lecomte, P, Almeida-Engler, J, Bitton, F, Martin-Magniette, ML, Renou, JP, Abad, P and Favery, B (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant Journal 44, 447–458.CrossRefGoogle ScholarPubMed
Jiang, C and Fu, X (2007) GA action: turning on de-DELLA repressing signaling. Current Opinion in Plant Biology 10, 461–465.CrossRefGoogle ScholarPubMed
Kalinina, EV, Chernov, NN and Saprin, AN (2008) Involvement of thio-, peroxi-, and glutaredoxins in cellular redox-dependent processes. Biochemistry. Biokhimiia 73, 1493–1510.CrossRefGoogle ScholarPubMed
Kaloshian, I and Walling, LL (2005) Hemipterans as plant pathogens. Annual Review of Phytopathology 43, 491–521.CrossRefGoogle ScholarPubMed
Kaloshian, I, Yaghoobi, J, Liharska, T, Hontelez, J, Hanson, D, Hogan, P, Jesse, T, Wijbrandi, J, Simons, G, Vos, P, Zabel, P and Williamson, VM (1998) Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Molecular and General Genetics 257, 376–385.CrossRefGoogle ScholarPubMed
Kaur, N, Pandey, A, Shivani Kumar, P, Pandey, P, Kesarwani, AK, Mantri, SS, Awasthi, P and Tiwari, S (2017) Regulation of banana phytoene synthase (MaPSY) expression, characterization and their modulation under various abiotic stress conditions. Frontiers in Plant Science 8, 462.CrossRefGoogle ScholarPubMed
Kempema, LA, Cui, X, Holzer, FM and Walling, LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiology 143, 849–865.CrossRefGoogle ScholarPubMed
Kiedrowski, S, Kawalleck, P, Hahlbrock, K, Somssich, IE and Dangl, JL (1992) Rapid activation of a novel plant defense gene is strictly dependent on the Arabidopsis RPM1 disease resistance locus. The EMBO Journal 11, 4677–4684.CrossRefGoogle ScholarPubMed
Kim, J and Kim, HY (2006) Molecular characterization of a bHLH transcription factor involved in Arabidopsis abscisic acid-mediated response. Biochimica et Biophysica Acta – Gene Structure and Expression 1759, 191–194.CrossRefGoogle ScholarPubMed
Kim, SG, Kim, ST, Wang, Y, Kim, SK, Lee, CH, Kim, KK, Kim, JK, Lee, SY and Kang, KY (2010) Overexpression of rice isoflavone reductase-like gene (OsIRL) confers tolerance to reactive oxygen species. Physiologia Plantarum 138, 1–9.CrossRefGoogle ScholarPubMed
Korth, KL (2003) Profiling the response of plants to herbivorous insects. Genome Biology 4, 221.CrossRefGoogle ScholarPubMed
Kusano, T, Tateda, C, Berberich, T and Takahashi, Y (2009) Voltage-dependent anion channels: their roles in plant defense and cell death. Plant Cell Reports 28, 1301–1308.CrossRefGoogle ScholarPubMed
Kuśnierczyk, A, Winge, P, Midelfart, H, Armbruster, WS, Rossiter, JT and Bones, AM (2007) Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. Journal of Experimental Botany 58, 2537–2552.CrossRefGoogle ScholarPubMed
Lacomme, C and Roby, D (1999) Identification of new early markers of the hypersensitive response in Arabidopsis thaliana. FEBS Letters 459, 149–153.CrossRefGoogle ScholarPubMed
Langlois-Meurinne, M, Gachon, CMM and Saindrenan, P (2005) Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv tomato in Arabidopsis. Plant Physiology 139, 1890–1901.CrossRefGoogle ScholarPubMed
Lao, NT, Long, D, Kiang, S, Coupland, G, Shoue, DA, Carpita, NC and Kavanagh, TA (2003) Mutation of a family 8 glycosyltransferase gene alters cell wall carbohydrate composition and causes a humidity-sensitive semi-sterile dwarf phenotype in Arabidopsis. Plant Molecular Biology 53, 647–661.CrossRefGoogle ScholarPubMed
Laterrot, H (1987) Near isogenic tomato lines in Moneymaker type with different genes for disease resistances. Report of the Tomato Genetics Cooperative 37, 91.Google Scholar
Li, Y, Zou, J, Li, M, Bilgin, DD, Vodkin, LO, Hartman, GL and Clough, SJ (2008) Soybean defense responses to the soybean aphid. New Phytologist 179, 185–195.CrossRefGoogle ScholarPubMed
Liu, C, Pedersen, C, Schultz-Larsen, T, Aguilar, GB, Madriz-Ordeñana, K, Hovmøller, MS and Thordal-Christensen, H (2016) The stripe rust fungal effector PEC6 suppresses pattern-triggered immunity in a host species-independent manner and interacts with adenosine kinases. The New Phytologist 7, 14034.CrossRefGoogle Scholar
Logemann, E, Reinold, S, Somssich, IE and Hahlbrock, K (1997) A novel type of pathogen defense-related cinnamyl alcohol dehydrogenase. Biological Chemistry 378, 909–913.CrossRefGoogle ScholarPubMed
Martin, GB, Bogdanove, AJ and Sessa, G (2003) Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology 54, 23–61.CrossRefGoogle ScholarPubMed
Martínez de Ilarduya, O and Kaloshian, I (2001) Mi-1.2 transcripts accumulate ubiquitously in resistant Lycopersicon esculentum. Journal of Nematology 33, 116–120.Google Scholar
Martínez de Ilarduya, O, Moore, AE and Kaloshian, I (2001) The tomato Rme1 locus is required for Mi-1-mediated resistance to root-knot nematodes and the potato aphid. Plant Journal 27, 417–425.CrossRefGoogle Scholar
Martínez de Ilarduya, O, Xie, Q and Kaloshian, I (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Molecular Plant-Microbe Interactions: MPMI 16, 699–708.CrossRefGoogle ScholarPubMed
Martínez de Ilarduya, O, Nombela, G, Hwang, C-F, Williamson, VM, Muñiz, M and Kaloshian, I (2004) Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway. Molecular Plant-Microbe Interactions: MPMI 17, 55–61.CrossRefGoogle ScholarPubMed
Marzluf, GA (1997) Molecular genetics of sulfur assimilation in filamentous fungi and yeast. Annual Review of Microbiology 51, 73–96.CrossRefGoogle ScholarPubMed
Mazel, A and Levine, A (2002) Induction of glucosyltransferase transcription and activity during superoxide-dependent cell death in Arabidopsis plants. Plant Physiology and Biochemistry 40, 133–140.CrossRefGoogle Scholar
McKenzie, CL, Bausher, M, Albano, JP, Shatters, RG, Sinisterra, XH and Powell, CA (2005) Deciphering changes in plant physiological response to whitefly feeding using microarray technology. Acta Horticulturae (ISHS) 695, 347–351.CrossRefGoogle Scholar
McMillan, GP, Hedley, D, Fyffe, L and Pérombelon, MCM (1993) Potato resistance to soft-rot erwinias is related to cell wall pectin esterification. Physiological and Molecular Plant Pathology 42, 279–289.CrossRefGoogle Scholar
Meissner, D, Albert, A, Böttcher, C, Strack, D and Milkowski, C (2008) The role of UDP-glucose:hydroxycinnamate glucosyltransferases in phenylpropanoid metabolism and the response to UV-B radiation in Arabidopsis thaliana. Planta 228, 663–674.CrossRefGoogle ScholarPubMed
Messeguer, R, Ganal, M, de Vicente, MC, Young, ND, Bolkan, H and Tanksley, SD (1991) High resolution RFLP map around the root knot nematode resistance gene (Mi) in tomato. Theoretical and Applied Genetics 82, 529–536.CrossRefGoogle Scholar
Meyer, Y, Siala, W, Bashandy, T, Riondet, C, Vignols, F and Reichheld, JP (2008) Glutaredoxins and thioredoxins in plants. Biochimica et Biophysica Acta – Molecular Cell Research 1783, 589–600.CrossRefGoogle ScholarPubMed
Milligan, SB, Bodeau, J, Yaghoobi, J, Kaloshian, I, Zabel, P and Williamson, VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. The Plant Cell Online 10, 1307–1320.CrossRefGoogle ScholarPubMed
Min, X, Okada, K, Brockmann, B, Koshiba, T and Kamiya, Y (2000) Molecular cloning and expression patterns of three putative functional aldehyde oxidase genes and isolation of two aldehyde oxidase pseudogenes in tomato. Biochimica et Biophysica Acta – Gene Structure and Expression 1493, 337–341.CrossRefGoogle ScholarPubMed
Mitchell, HJ, Hall, JL and Barber, MS (1994) Elicitor-induced cinnamyl alcohol dehydrogenase activity in lignifying wheat (Triticum aestivum L.) leaves. Plant Physiology 104, 551–556.CrossRefGoogle ScholarPubMed
Mueller, LA, Solow, TH, Taylor, N, Skwarecki, B, Buels, R, Binns, J, Lin, C, Wright, MH, Ahrens, R, Wang, Y, Herbst, EV, Keyder, ER, Menda, N, Zamir, D and Tanksley, SD (2005) The SOL genomics network. A Comparative Resource for Solanaceae Biology and Beyond. Plant Phisiology 138, 1310–1317.CrossRefGoogle ScholarPubMed
Muñiz, M and Nombela, G (2001) Bemisia tabaci: a new clip-cage for biological studies. European Whitefly Studies Network, 1–2.Google Scholar
Navarro, L, Bari, R, Achard, P, Lisón, P, Nemri, A, Harberd, NP and Jones, JDG (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Current Biology 18, 650–655.CrossRefGoogle ScholarPubMed
Nombela, G, Beitia, F and Muñiz, M (2000) Variation in tomato host response to Bemisia tabaci (Hemiptera: Aleyrodidae) in relation to acyl sugar content and presence of the nematode and potato aphid resistance gene Mi. Bulletin of Entomological Research 90, 161–167.CrossRefGoogle ScholarPubMed
Nombela, G, Beitia, F and Muñiz, M (2001) A differential interaction study of Bemisia tabaci Q-biotype on commercial tomato varieties with or without the Mi resistance gene, and comparative host responses with the B-biotype. Entomologia Experimentalis et Applicata 98, 339–344.CrossRefGoogle Scholar
Nombela, G, Williamson, VM and Muñiz, M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Molecular Plant-Microbe Interactions: MPMI 16, 645–649.CrossRefGoogle ScholarPubMed
Okada, SF, O'Neal, WK, Huang, P, Nicholas, RA, Ostrowski, LE, Craigen, WJ, Lazarowski, ER and Boucher, RC (2004) Voltage-dependent anion channel-1 (VDAC-1) contributes to ATP release and cell volume regulation in murine cells. The Journal of General Physiology 124, 513–526.CrossRefGoogle ScholarPubMed
Oliveros, JC (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams. BioinfoGP of CNB-CSIC. Available at http://bioinfogp.cnnb.csic.es/tools/venny/index.ht.Google Scholar
Pascual, L, Blanca, JM, Cañizares, J and Nuez, F (2009) Transcriptomic analysis of tomato carpel development reveals alterations in ethylene and gibberellin synthesis during pat3/pat4 parthenocarpic fruit set. BMC Plant Biology 9, 18 pp.CrossRefGoogle ScholarPubMed
Peng, J, Carol, P, Richards, DE, King, KE, Cowling, RJ, Murphy, GP and Harberd, NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes and Development 11, 3194–3205.CrossRefGoogle ScholarPubMed
Peng, J, Yu, DS, Wang, LQ, Xie, MM, Yuan, CY, Wang, Y, Tang, DY, Zhao, XY and Liu, XM (2012) Arabidopsis F-box gene FOA1 involved in ABA signaling. Science China Life Sciences 55, 497–506.CrossRefGoogle ScholarPubMed
Persson, B, Kallberg, Y, Bray, JE, Bruford, E, Dellaporta, SL, Favia, AD, Duarte, RG, Jörnvall, H, Kavanagh, KL, Kedishvili, N, Kisiela, M, Maser, E, Mindnich, R, Orchard, S, Penning, TM, Thornton, JM, Adamski, J and Oppermann, U (2009) The SDR (short-chain dehydrogenase/reductase and related enzymes) nomenclature initiative. Chemico-Biological Interactions 178, 94–98.CrossRefGoogle ScholarPubMed
Piedras, P, Hammond-Kosack, KE, Harrison, K and Jones, JDG (1998) Rapid, Cf-9- and Avr9-dependent production of active oxygen species in tobacco suspension cultures. Molecular Plant-Microbe Interactions 11, 1155–1166.CrossRefGoogle Scholar
Portillo, M, Cabrera, J, Lindsey, K, Topping, J, Andrés, MF, Emiliozzi, M, Oliveros, JC, García-Casado, G, Solano, R, Koltai, H, Resnick, N, Fenoll, C and Escobar, C (2013) Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. New Phytologist 197, 1276–1290.CrossRefGoogle ScholarPubMed
Puthoff, DP, Nettleton, D, Rodermel, SR and Baum, TJ (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. The Plant Journal 33, 911–921.CrossRefGoogle ScholarPubMed
Qi, YH, Kawano, N, Yamauchi, Y, Ling, JQ, Li, DB and Tanaka, K (2005) Identification and cloning of a submergence-induced gene OsGGT (glycogenin glucosyltransferase) from rice (Oryza sativa L.) by suppression subtractive hybridization. Planta 221, 437–445.CrossRefGoogle ScholarPubMed
Qin, F, Sakuma, Y, Tran, L, Maruyama, K, Kidokoro, S, Fujita, Y, Fujita, M, Umezawa, T, Sawano, Y, Miyazono, K, Tanokura, M, Shinozaki, K and Yamaguchi-Shinozaki, K (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. The Plant Cell Online 20, 1693–1707.CrossRefGoogle ScholarPubMed
Raiola, A, Lionetti, V, Elmaghraby, I, Immerzeel, P, Mellerowicz, EJ, Salvi, G, Cervone, F and Bellincampi, D (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Molecular Plant-Microbe Interactions: MPMI 24, 432–440.CrossRefGoogle ScholarPubMed
Rantong, G, Van Der Kelen, K, Van Breusegem, F and Gunawardena, AHLAN (2016) Identification of differentially expressed genes during lace plant leaf development. International Journal of Plant Sciences 177, 419–431.CrossRefGoogle Scholar
Rensink, WA and Buell, CR (2005) Microarray expression profiling resources for plant genomics. Trends in Plant Science 10, 603–609.CrossRefGoogle ScholarPubMed
Reuber, TL and Ausubel, FM (1996) Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. The Plant Cell 8, 241–249.Google ScholarPubMed
Rezzonico, F, Rupp, O and Fahrentrapp, J (2017) Pathogen recognition in compatible plant-microbe interactions. Scientific Reports 7, 6383.CrossRefGoogle ScholarPubMed
Roberts, PA and Thomason, IJ (1986) Variability in reproduction of isolates of Meloidogyne incognita and M. javanica on resistant tomato genotypes. Plant Disease 70, 547–551.CrossRefGoogle Scholar
Rodríguez-Álvarez, CI, López-Climent, MF, Gómez-Cadenas, A, Kaloshian, I and Nombela, G (2015) Salicylic acid is required for Mi-1-mediated resistance of tomato to whitefly Bemisia tabaci, but not for basal defense to this insect pest. Bulletin of Entomological Research 105, 574–582.CrossRefGoogle Scholar
Rodríguez-Álvarez, CI, Muñiz, M and Nombela, G (2017) Effect of plant development (age and size) on the Mi-1-mediated resistance of tomato to whitefly Bemisia tabaci. Bulletin of Entomological Research 107, 768–776.CrossRefGoogle ScholarPubMed
Rong, W, Luo, M, Shan, T, Wei, X, Du, L, Xu, H and Zhang, Z (2016) A wheat cinnamyl alcohol dehydrogenase TaCAD12 contributes to host resistance to the sharp eyespot disease. Frontiers in Plant Science 7, 1723.CrossRefGoogle ScholarPubMed
Rossi, M, Goggin, FL, Milligan, SB, Kaloshian, I, Ullman, DE and Williamson, VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences 95, 9750–9754.CrossRefGoogle ScholarPubMed
Roth, R, Boudet, AM and Pont-Lezica, R (1997) Lignification and cinnamyl alcohol dehydrogenase activity in developing stems of tomato and poplar: a spatial and kinetic study through tissue printing. Journal of Experimental Botany 48, 247–254.CrossRefGoogle Scholar
Sasikumar, AN, Perez, WB and Kinzy, TG (2012) The many roles of the eukaryotic elongation factor 1 complex. Wiley Interdisciplinary Reviews: RNA 3, 543–555.CrossRefGoogle ScholarPubMed
Schaff, JE, Nielsen, DM, Smith, CP, Scholl, EH and Bird, DM (2007) Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiology 144, 1079–1092.CrossRefGoogle ScholarPubMed
Schaller, A and Frasson, D (2001) Induction of wound response gene expression in tomato leaves by ionophores. Planta 212, 431–435.CrossRefGoogle ScholarPubMed
Schaller, A and Oecking, C (1999) Modulation of plasma membrane H+ -ATPase activity differentially activates wound and pathogen defense responses in tomato plants. The Plant Cell 11, 263–272.Google ScholarPubMed
Scheel, D (1998) Resistance response physiology and signal transduction. Current Opinion in Plant Biology 1, 305–310.CrossRefGoogle ScholarPubMed
Schmelzer, E, Kruger-Lebus, S and Hahlbrock, K (1989) Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. The Plant Cell 1, 993–1001.CrossRefGoogle ScholarPubMed
Seifert, GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Current Opinion in Plant Biology 7, 277–284.CrossRefGoogle ScholarPubMed
Silverstone, AL, Ciampaglio, CN and Sun, T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. The Plant Cell 10, 155–169.CrossRefGoogle ScholarPubMed
Smith, GP (1944) Embryo culture of a tomato species hybrid. Journal of the American Society for Horticultural Science 44, 413–416.Google Scholar
Smyth, GK (2005) Limma: linear models for microarray data. In Gentleman, R, Carey, VJ, Huber, W, Irizarry, RA, Dudoit, S (eds), Bioinformatics and Computational Biology Solutions Using R and Bioconductor. New York, NY: Statistics for Biology and Health. Springer, pp. 397–420.CrossRefGoogle Scholar
Somssich, IE, Bollmann, J, Hahlbrock, K, Kombrink, E and Schulz, W (1989) Differential early activation of defense-related genes in elicitor-treated parsley cells. Plant Molecular Biology 12, 227–234.CrossRefGoogle ScholarPubMed
Stirnimann, CU, Petsalaki, E, Russell, RB and Müller, CW (2010) WD40 proteins propel cellular networks. Trends in Biochemical Sciences 35, 565–574.CrossRefGoogle ScholarPubMed
Subrahmanian, N, Remacle, C and Hamel, PP (2016) Plant mitochondrial complex i composition and assembly: a review. Biochimica et Biophysica Acta – Bioenergetics 1857, 1001–1014.CrossRefGoogle ScholarPubMed
Sun, W, Xu, X, Zhu, H, Liu, A, Liu, L, Li, J and Hua, X (2010) Comparative transcriptomic profiling of a salt-tolerant wild tomato species and a salt-sensitive tomato cultivar. Plant and Cell Physiology 51, 997–1006.CrossRefGoogle Scholar
Swidzinski, JA, Leaver, CJ and Sweetlove, LJ (2004) A proteomic analysis of plant programmed cell death. Phytochemistry 65, 1829–1838.CrossRefGoogle ScholarPubMed
Tamaoki, M, Freeman, JL and Pilon-Smits, EAH (2008) Cooperative ethylene and jasmonic acid signaling regulates selenite resistance in Arabidopsis. Plant Physiology 146, 1219–1230.CrossRefGoogle ScholarPubMed
Tao, Y, Xie, Z, Chen, W, Glazebrook, J, Chang, H-S, Han, B, Zhu, T, Zou, G and Katagiri, F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. The Plant Cell 15, 317–330.CrossRefGoogle ScholarPubMed
Tateda, C, Watanabe, K, Kusano, T and Takahashi, Y (2011) Molecular and genetic characterization of the gene family encoding the voltage-dependent anion channel in Arabidopsis. Journal of Experimental Botany 62, 4773–4785.CrossRefGoogle ScholarPubMed
Tateda, C, Yamashita, K, Takahashi, F, Kusano, T and Takahashi, Y (2009) Plant voltage-dependent anion channels are involved in host defense against Pseudomonas cichorii and in Bax-induced cell death. Plant Cell Reports 28, 41–51.CrossRefGoogle ScholarPubMed
Thompson, GA and Goggin, FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. In Journal of Experimental Botany 57, 755–766.CrossRefGoogle ScholarPubMed
Toledo-Ortiz, G, Huq, E and Rodríguez-Concepción, M (2010) Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proceedings of the National Academy of Sciences of the USA 107, 11626–11631.CrossRefGoogle ScholarPubMed
Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635–641.CrossRefGoogle Scholar
Ton, J, Flors, V and Mauch-Mani, B (2009) The multifaceted role of ABA in disease resistance. Trends in Plant Science 14, 310–317.CrossRefGoogle ScholarPubMed
Uehara, T, Sugiyama, S, Matsuura, H, Arie, T and Masuta, C (2010) Resistant and susceptible responses in tomato to cyst nematode are differentially regulated by salicylic acid. Plant and Cell Physiology 51, 1524–1536.CrossRefGoogle ScholarPubMed
Umesha, S and Kavitha, R (2011) Induction of cinnamyl alcohol dehydrogenase in bacterial spot disease resistance of tomato. Journal of Bacteriology Research 3, 16–27.Google Scholar
van den Burg, HA, Tsitsigiannis, DI, Rowland, O, Lo, J, Rallapalli, G, MacLean, D, Takken, FLW and Jones, JDG (2008) The F-Box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato. The Plant Cell Online 20, 697–719.CrossRefGoogle ScholarPubMed
Van Gijsegem, F, Somssich, IE and Scheel, D (1995) Activation of defense-related genes in parsley leaves by infection with Erwinia chrysanthemi. European Journal of Plant Pathology 101, 549–559.CrossRefGoogle Scholar
Veenman, L, Shandalov, Y and Gavish, M (2008) VDAC activation by the 18 kDa translocator protein (TSPO), implications for apoptosis. Journal of Bioenergetics and Biomembranes 40, 199–205.CrossRefGoogle Scholar
Voehringer, D, Hirschberg, D, Xiao, J, Lu, Q, Roederer, M, Lock, CB, Herzenberg, LA and Steinman, L (2000) Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proceedings of the National Academy of Sciences of the USAmerica 97, 2680–2685.CrossRefGoogle ScholarPubMed
Vogt, T and Jones, P (2000) Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends in Plant Science 5, 380–386.CrossRefGoogle ScholarPubMed
Von Lintig, J, Welsch, R, Bonk, M, Giuliano, G, Batschauer, A and Kleinig, H (1997) Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. Plant Journal 12, 625–634.CrossRefGoogle ScholarPubMed
von Saint Paul, V, Zhang, W, Kanawati, B, Geist, B, Faus-Keßler, T, Schmitt-Kopplin, P and Schäffner, AR (2011) The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. The Plant Cell 23, 4124–4145.CrossRefGoogle ScholarPubMed
Wang, H, Hao, L, Shung, C-Y, Sunter, G and Bisaro, DM (2003) Adenosine kinase Is inactivated by geminivirus AL2 and L2 proteins. The Plant Cell 15, 3020–3032.CrossRefGoogle ScholarPubMed
Wang, F, Zhu, D, Huang, X, Li, S, Gong, Y, Yao, Q, Fu, X, Fan, L-M and Deng, XW (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. The Plant Cell Online 21, 2378–2390.CrossRefGoogle ScholarPubMed
Weiß, S and Winkelmann, T (2017) Transcriptome profiling in leaves representing aboveground parts of apple replant disease affected Malus domestica ‘M26’ plants. Scientia Horticulturae 222, 111–125.CrossRefGoogle Scholar
Weretilnyk, EA, Alexander, KJ, Drebenstedt, M, Snider, JD, Summers, PS and Moffatt, BA (2001) Maintaining methylation activities during salt stress. The involvement of adenosine kinase. Plant Physiology 125, 856–865.CrossRefGoogle ScholarPubMed
Wiethölter, N, Graeßner, B, Mierau, M, Mort, AJ and Moerschbacher, BM (2003) Differences in the methyl ester distribution of homogalacturonans from near-isogenic wheat lines resistant and susceptible to the wheat stem rust fungus. Molecular Plant-Microbe Interactions 16, 945–952.CrossRefGoogle ScholarPubMed
Williamson, VM (1998) Root-knot nematode resistance genes in tomato and their potential for future use. Annual Review of Phytopathology 36, 277–293.CrossRefGoogle ScholarPubMed
Williamson, VM and Colwell, G (1991) Acid phosphatase-1 from nematode resistant tomato. Plant Physiology 97, 139–146.CrossRefGoogle ScholarPubMed
Williamson, V and Roberts, P (2009) Mechanisms and genetics of resistance. In Perry, RN, Moens, M, Starr, JL (eds), Root-knot Nematodes. Wallingford, Oxfordshire, UK: CAB International, pp. 301–325.CrossRefGoogle Scholar
Xu, Y and Huang, B (2018) Transcriptomic analysis reveals unique molecular factors for lipid hydrolysis, secondary cell-walls and oxidative protection associated with thermotolerance in perennial grass. BMC Genomics 19, 70.CrossRefGoogle ScholarPubMed
Xu, LG, Li, LY and Shu, HB (2004) TRAF7 potentiates MEKK3-induced AP1 and CHOP activation and induces apoptosis. Journal of Biological Chemistry 279, 17278–17282.CrossRefGoogle ScholarPubMed
Zhang, F, Zhu, L and He, G (2004) Differential gene expression in response to brown planthopper feeding in rice. Journal of Plant Physiology 161, 53–62.CrossRefGoogle ScholarPubMed
Zhang, Q, Shirley, N, Lahnstein, J and Fincher, GB (2005) Characterization and expression patterns of UDP-D-glucuronate decarboxylase genes in barley. Plant Physiology 138, 131–141.CrossRefGoogle ScholarPubMed
Zhou, S, Wei, S, Boone, B and Levy, S (2007) Microarray analysis of genes affected by salt stress in tomato. African Journal of Environmental Science and Technology 1, 14–26.Google Scholar