Effect of heat-shock pre-treatment on tomato plants infected by powdery mildew fungus

https://doi.org/10.17221/24/2018-PPSCitation:Nožková V., Mieslerová B., Luhová L., Piterková J., Novák O., Špundová M., Lebeda A. (2019): Effect of heat-shock pre-treatment on tomato plants infected by powdery mildew fungus. Plant Protect. Sci., 55: 31-42.
download PDF

The effect of plant heat-shock (HS) pre-treatment (40.5°C, 2 h) on Pseudoidium neolycopersici development in the susceptible and moderately resistant Solanum spp. genotypes was studied together with biochemical responses (endogenous concentrations of salicylic (SA), jasmonic (JA), abscisic acid (ABA), and peroxidase (POX) activity). In HS pre-treated S. lycopersicum, an acceleration of pathogen, chlorosis and necrosis development, strong SA, JA accumulation, and increased POX activity were detected. In S. chmielewskii, HS pre-treatment caused a slight suppression of pathogen development, increase in JA, ABA concentrations, and POX activity. HS accelerated and strengthened the development of symptoms and biochemical responses to the infection in the susceptible genotype in contrast to moderately resistant genotype with a robust defence response to an infection per se.

Achuo E. A., Audenaert K., Meziane H., Hofte M. (2004): The salicylic acid-dependent defence pathway is effective against different pathogens in tomato and tobacco. Plant Pathology, 53, 65-72 https://doi.org/10.1111/j.1365-3059.2004.00947.x
Achuo E. A., Prinsen E., Hofte M. (2006): Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathology, 55, 178-186 https://doi.org/10.1111/j.1365-3059.2006.01340.x
Adie B. A.T., Perez-Perez J., Perez-Perez M. M., Godoy M., Sanchez-Serrano J.-J., Schmelz E. A., Solano R. (2007): ABA Is an Essential Signal for Plant Resistance to Pathogens Affecting JA Biosynthesis and the Activation of Defenses in Arabidopsis. THE PLANT CELL ONLINE, 19, 1665-1681 https://doi.org/10.1105/tpc.106.048041
Almagro L., Gómez Ros L. V., Belchi-Navarro S., Bru R., Ros Barceló A., Pedreño M. A. (2009): Class III peroxidases in plant defence reactions. Journal of Experimental Botany, 60, 377-390 https://doi.org/10.1093/jxb/ern277
Almeselmani Moaed, Deshmukh P.S., Sairam R.K., Kushwaha S.R., Singh T.P. (2006): Protective role of antioxidant enzymes under high temperature stress. Plant Science, 171, 382-388 https://doi.org/10.1016/j.plantsci.2006.04.009
Angelini R., Manes F., Federico R. (1990): Spatial and functional correlation between diamine-oxidase and peroxidase activities and their dependence upon de-etiolation and wounding in chick-pea stems. Planta, 182, - https://doi.org/10.1007/BF00239989
Asselbergh Bob, De Vleesschauwer David, Höfte Monica (2008): Global Switches and Fine-Tuning—ABA Modulates Plant Pathogen Defense. Molecular Plant-Microbe Interactions, 21, 709-719 https://doi.org/10.1094/MPMI-21-6-0709
Bergougnoux Véronique, Hlaváčková Vladimíra, Plotzová Renáta, Novák Ondřej, Fellner Martin (2009): The 7B-1 mutation in tomato (Solanum lycopersicum L.) confers a blue light-specific lower sensitivity to coronatine, a toxin produced by Pseudomonas syringae pv. tomato. Journal of Experimental Botany, 60, 1219-1230 https://doi.org/10.1093/jxb/ern366
Camejo Daymi, Guzmán-Cedeño Ángel, Moreno Alexander (2016): Reactive oxygen species, essential molecules, during plant–pathogen interactions. Plant Physiology and Biochemistry, 103, 10-23 https://doi.org/10.1016/j.plaphy.2016.02.035
Cao Feng Yi, Yoshioka Keiko, Desveaux Darrell (2011): The roles of ABA in plant–pathogen interactions. Journal of Plant Research, 124, 489-499 https://doi.org/10.1007/s10265-011-0409-y
Clarke Shannon M., Cristescu Simona M., Miersch Otto, Harren Frans J. M., Wasternack Claus, Mur Luis A. J. (2009): Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytologist, 182, 175-187 https://doi.org/10.1111/j.1469-8137.2008.02735.x
Cingoz Gunce Sahin, Gurel Ekrem (2016): Effects of salicylic acid on thermotolerance and cardenolide accumulation under high temperature stress in Digitalis trojana Ivanina. Plant Physiology and Biochemistry, 105, 145-149 https://doi.org/10.1016/j.plaphy.2016.04.023
Dat James F., Lopez-Delgado Humberto, Foyer Christine H., Scott Ian M. (1998): Parallel Changes in H 2 O 2 and Catalase during Thermotolerance Induced by Salicylic Acid or Heat Acclimation in Mustard Seedlings. Plant Physiology, 116, 1351-1357 https://doi.org/10.1104/pp.116.4.1351
Dat James F., Lopez-Delgado Humberto, Foyer Christine H., Scott Ian M. (2000): Effects of Salicylic Acid on Oxidative Stress and Thermotolerance in Tobacco. Journal of Plant Physiology, 156, 659-665 https://doi.org/10.1016/S0176-1617(00)80228-X
Ellis Christine, Karafyllidis Ioannis, Turner John G. (2002): Constitutive Activation of Jasmonate Signaling in an Arabidopsis Mutant Correlates with Enhanced Resistance to Erysiphe cichoracearum , Pseudomonas syringae , and Myzus persicae. Molecular Plant-Microbe Interactions, 15, 1025-1030 https://doi.org/10.1094/MPMI.2002.15.10.1025
Halim V. A., Vess A., Scheel D., Rosahl S. (2006): The Role of Salicylic Acid and Jasmonic Acid in Pathogen Defence. Plant Biology, 8, 307-313 https://doi.org/10.1055/s-2006-924025
Hazen B.E., Bushnell W.R. (1983): Inhibition of the hypersensitive reaction in barley to powdery mildew by heat shock and cytochalasin B. Physiological Plant Pathology, 23, 421-438 https://doi.org/10.1016/0048-4059(83)90026-7
Heath M.C. (2000): Hypersensitive response-related death. Plant Molecular Biology, 44: 321–334.https://doi.org/10.1023/A:1026592509060
Hiraga Susumu, Sasaki Katsutomo, Ito Hiroyuki, Ohashi Yuko, Matsui Hirokazu (2001): A Large Family of Class III Plant Peroxidases. Plant and Cell Physiology, 42, 462-468 https://doi.org/10.1093/pcp/pce061
Hlaváčková Vladimíra, Krchňák Pavel, Nauš Jan, Novák Ondřej, Špundová Martina, Strnad Miroslav (2006): Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta, 225, 235-244 https://doi.org/10.1007/s00425-006-0325-x
Huang C., Groot T., Meijer-Dekens F., Niks R., Lindhout P. (1998): The resistance to powdery mildew (Oidium lycopersicum) in Lycopersicon species is mainly associated with hypersensitive response. European Journal of Plant Pathology, 104: 399–407.https://doi.org/10.1023/A:1008092701883
Huang C.C., Biesheuvel J., Lindhout P., Niks R.E. (2000): Host range of Oidium lycopersici occurring in the Netherlands. European Journal of Plant Pathology, 106: 465–473.https://doi.org/10.1023/A:1008706614291
Hückelhoven R., Kogel K.H. (2003): Reactive oxygen intermediates in plant-microbe interactions: Who is who in powdery mildew resistance? Planta, 216: 891–902.
Huysmans Marlies, Lema A Saul, Coll Nuria S, Nowack Moritz K (2017): Dying two deaths — programmed cell death regulation in development and disease. Current Opinion in Plant Biology, 35, 37-44 https://doi.org/10.1016/j.pbi.2016.11.005
Jin J.B., Cai B., Zhou J.M. (2017): Salicylic acid. In: Li J., Li C., Smith S.M. (eds): Hormone Metabolism and Signaling in Plants: Hormone Metabolism and Signaling in Plants. London, Academic Press: 273–289.
Kotak Sachin, Larkindale Jane, Lee Ung, von Koskull-Döring Pascal, Vierling Elizabeth, Scharf Klaus-Dieter (2007): Complexity of the heat stress response in plants. Current Opinion in Plant Biology, 10, 310-316 https://doi.org/10.1016/j.pbi.2007.04.011
Kubienová L., Sedlářová M., Vítečková-Wünschová A., Piterková J., Luhová L., Mieslerová B., Lebeda A., Navrátil M., Petřivalský M. (2013): Effect of extreme temperatures on powdery mildew development and Hsp70 induction in tomato and wild Solanum spp. . Plant Protection Science, 49, S41-S54 https://doi.org/10.17221/45/2013-PPS
Kumar Sanjeev, Kaushal Neeru, Nayyar Harsh, Gaur P. (2012): Abscisic acid induces heat tolerance in chickpea (Cicer arietinum L.) seedlings by facilitated accumulation of osmoprotectants. Acta Physiologiae Plantarum, 34, 1651-1658 https://doi.org/10.1007/s11738-012-0959-1
Larkindale Jane, Huang Bingru (2005): Effects of Abscisic Acid, Salicylic Acid, Ethylene and Hydrogen Peroxide in Thermotolerance and Recovery for Creeping Bentgrass. Plant Growth Regulation, 47, 17-28 https://doi.org/10.1007/s10725-005-1536-z
Lebeda A., Reinink K. (1994): Histological characterization of resistance in lactuca saligna to lettuce downy mildew (Bremia lactucae). Physiological and Molecular Plant Pathology, 44, 125-139 https://doi.org/10.1016/S0885-5765(05)80106-7
Lebeda A., Mieslerová B. (1999): Identification, occurrence and host range of tomato powdery mildew (Oidium lycopersici) in the Czech Republic. Acta Phytopathologica et Entomologica Hungarica, 34: 13–25.
Lebeda A., Mieslerová B. (2002): Variability in pathogenicity of Oidium neolycopersici on Lycopersicon species. Journal of Plant Disease Protection, 109: 129–141.
Lebeda A., Mieslerová B. (2010): Screening for resistance to tomato powdery mildew (Oidium neolycopersici). In: Spencer M.M., Lebeda A. (eds): Mass Screening Techniques for Selecting Crops Resistant to Disease. Vienna, International Atomic Energy Agency (IAEA): 257–265.
Lebeda Aleš, Mieslerová Barbora, Petřivalský Marek, Luhová Lenka, Špundová Martina, Sedlářová Michaela, Nožková-Hlaváčková Vladimíra, Pink David A. C. (2014): Resistance mechanisms of wild tomato germplasm to infection of Oidium neolycopersici. European Journal of Plant Pathology, 138, 569-596 https://doi.org/10.1007/s10658-013-0307-3
LI CHENGWEI, FAINO LUIGI, DONG LIN, FAN JUNMEI, KISS LEVENTE, DE GIOVANNI CLAUDIO, LEBEDA ALES, SCOTT JOHN, MATSUDA YOSHINORI, TOYODA HIDEYOSHI, LINDHOUT PIM, VISSER RICHARD G. F., BONNEMA GUUSJE, BAI YULING (2012): Characterization of polygenic resistance to powdery mildew in tomato at cytological, biochemical and gene expression level. Molecular Plant Pathology, 13, 148-159 https://doi.org/10.1111/j.1364-3703.2011.00737.x
Lindhout Pim, Pet Gerard, van der Beek Hans (1993): Screening wild Lycopersicon species for resistance to powdery mildew (Oidium lycoperiscum). Euphytica, 72, 43-49 https://doi.org/10.1007/BF00023771
López-Delgado H., Mora-Herrera M. E., Zavaleta-Mancera H. A., Cadena-Hinojosa M., Scott I. M. (2004): Salicylic acid enhances heat tolerance and potato virus X (PVX) elimination during thermotherapy of potato microplants. American Journal of Potato Research, 81, 171-176 https://doi.org/10.1007/BF02871746
Mauch-Mani Brigitte, Mauch Felix (2005): The role of abscisic acid in plant–pathogen interactions. Current Opinion in Plant Biology, 8, 409-414 https://doi.org/10.1016/j.pbi.2005.05.015
Mieslerova B., Lebeda A., Chetelat R. T. (2000): Variation in Response of Wild Lycopersicon and Solanum spp. against Tomato Powdery Mildew (Oidium lycopersici). Journal of Phytopathology, 148, 303-311 https://doi.org/10.1046/j.1439-0434.2000.00492.x
Mieslerová B., Lebeda A., Kennedy R., Novotny R. (2002): Comparative morphological studies on tomato powdery mildew (Oidium neolycopersici). Acta Phytopathologica et Entomologica Hungarica, 37, 57-74 https://doi.org/10.1556/APhyt.37.2002.1-3.7
MIESLEROVA B, LEBEDA A, KENNEDY R (2004): Variation in Oidium neolycopersici development on host and non-host plant species and their tissue defence responses. Annals of Applied Biology, 144, 237-248 https://doi.org/10.1111/j.1744-7348.2004.tb00339.x
Mlíčková Kateřina, Luhová Lenka, Lebeda Aleš, Mieslerová Barbora, Peč Pavel (2004): Reactive oxygen species generation and peroxidase activity during Oidium neolycopersici infection on Lycopersicon species. Plant Physiology and Biochemistry, 42, 753-761 https://doi.org/10.1016/j.plaphy.2004.07.007
PITERKOVÁ JANA, PETŘIVALSKÝ MAREK, LUHOVÁ LENKA, MIESLEROVÁ BARBORA, SEDLÁŘOVÁ MICHAELA, LEBEDA ALEŠ (2009): Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Molecular Plant Pathology, 10, 501-513 https://doi.org/10.1111/j.1364-3703.2009.00551.x
Piterková Jana, Luhová Lenka, Mieslerová Barbora, Lebeda Aleš, Petřivalský Marek (2013): Nitric oxide and reactive oxygen species regulate the accumulation of heat shock proteins in tomato leaves in response to heat shock and pathogen infection. Plant Science, 207, 57-65 https://doi.org/10.1016/j.plantsci.2013.02.010
Politycka Barbara (1997): Free and glucosylated phenolics, phenol β-glucosyltransferase activity and membrane permeability in cucumber roots affected by derivatives of cinnamic and benzoic acids. Acta Physiologiae Plantarum, 19, 311-317 https://doi.org/10.1007/s11738-997-0007-8
Pozo M.J., van Loon L.C., Pieterse C.M.J. (2004): Jasmonates – Signals in plant-microbe interactions. Journal of Plant Growth Regulation, 23: 211–222.
Prokopová Jitka, Mieslerová Barbora, Hlaváčková Vladimíra, Hlavinka Jan, Lebeda Aleš, Nauš Jan, Špundová Martina (2010): Changes in photosynthesis of Lycopersicon spp. plants induced by tomato powdery mildew infection in combination with heat shock pre-treatment. Physiological and Molecular Plant Pathology, 74, 205-213 https://doi.org/10.1016/j.pmpp.2010.01.001
Reddy Ramesha A., Kumar Bhumesh, Reddy Palakolanu Sudhakar, Mishra Rabi N., Mahanty Srikrishna, Kaul Tanushri, Nair Suresh, Sopory Sudhir K., Reddy Malireddy K. (2009): Molecular cloning and characterization of genes encoding Pennisetum glaucum ascorbate peroxidase and heat-shock factor: Interlinking oxidative and heat-stress responses. Journal of Plant Physiology, 166, 1646-1659 https://doi.org/10.1016/j.jplph.2009.04.007
Robert-Seilaniantz Alexandre, Grant Murray, Jones Jonathan D.G. (2011): Hormone Crosstalk in Plant Disease and Defense: More Than Just JASMONATE-SALICYLATE Antagonism. Annual Review of Phytopathology, 49, 317-343 https://doi.org/10.1146/annurev-phyto-073009-114447
Satková P., Starý T., Plešková V., Zapletalová M., Kašparovský T., Činčalová-Kubienová L., Luhová L., Mieslerová B., Mikulík J., Lochman J., Petřivalský M. (2017): Diverse responses of wild and cultivated tomato to BABA, oligandrin and Oidium neolycopersici infection. Annals of Botany, 119: 829–840.
Schweizer P., Gees R., Mosinger E. (1993): Effect of Jasmonic Acid on the Interaction of Barley (Hordeum vulgare L.) with the Powdery Mildew Erysiphe graminis f.sp. hordei. Plant Physiology, 102, 503-511 https://doi.org/10.1104/pp.102.2.503
Schweizer Patrick, Vallélian-Bindschedler Laurence, Mösinger Egon (1995): Heat-induced resistance in barley to the powdery mildew fungus Erysiphe graminis f.sp. hordei. Physiological and Molecular Plant Pathology, 47, 51-66 https://doi.org/10.1006/pmpp.1995.1042
Sharma Manvi, Laxmi Ashverya (2016): Jasmonates: Emerging Players in Controlling Temperature Stress Tolerance. Frontiers in Plant Science, 6, - https://doi.org/10.3389/fpls.2015.01129
Shigenaga A.M., Argueso C.T. (2016): No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens. Seminars in Cell & Developmental Biology, 56: 174–189.
Silva M.C., Rijo L. Jr., Rodrigues C.J., Vasconcelos M.I. (1992): Estudos histólogicos da accao de tratamentos pelo calor nas expressoes de suscepribilidade e de resistencia na interaccao Coffea arabica-Hemileia vastatrix. Turrialba, 1: 200–206.
Talieva M.N., Runkova L.V., Andreev L.N. (1999): Effect of abscisic acid and kartolin on plant resistance to powdery mildew. Izvestiya Akademii Nauk Seriya Biologicheskaya, 5: 534–538.
Tománková Kateřina, Luhová Lenka, Petřivalský Marek, Peč Pavel, Lebeda Aleš (2006): Biochemical aspects of reactive oxygen species formation in the interaction between Lycopersicon spp. and Oidium neolycopersici. Physiological and Molecular Plant Pathology, 68, 22-32 https://doi.org/10.1016/j.pmpp.2006.05.005
Vallélian-Bindschedler L, Schweizer P, Mösinger E, Métraux J-P (1998): Heat-induced resistance in barley to powdery mildew (Blumeria graminisf.sp.hordei) is associated with a burst of active oxygen species. Physiological and Molecular Plant Pathology, 52, 185-199 https://doi.org/10.1006/pmpp.1998.0140
Vlot A. Corina, Dempsey D'Maris Amick, Klessig Daniel F. (2009): Salicylic Acid, a Multifaceted Hormone to Combat Disease. Annual Review of Phytopathology, 47, 177-206 https://doi.org/10.1146/annurev.phyto.050908.135202
Walters Dale, Cowley Tracy, Mitchell Ann (2002): Methyl jasmonate alters polyamine metabolism and induces systemic protection against powdery mildew infection in barley seedlings. Journal of Experimental Botany, 53, 747-756 https://doi.org/10.1093/jexbot/53.369.747
Wasternack C. (2006): Oxylipins: biosynthesis, signal transduction and action. In: Hedden P., Thomas S.G. (eds): Plant Hormone Signalling. Annual Plant Reviews. Oxford, Blackwell Publishing: 185–229.
Whipps J. M., Budge S. P., Fenlon J. S. (1998): Characteristics and host range of tomato powdery mildew. Plant Pathology, 47, 36-48 https://doi.org/10.1046/j.1365-3059.1998.00207.x
Wiese J., Kranz T., Schubert S. (2004): Induction of Pathogen Resistance in Barley by Abiotic Stress. Plant Biology, 6, 529-536 https://doi.org/10.1055/s-2004-821176
WOJTASZEK Przemysław (1997): Oxidative burst: an early plant response to pathogen infection. Biochemical Journal, 322, 681-692 https://doi.org/10.1042/bj3220681
download PDF

© 2018 Czech Academy of Agricultural Sciences