Elevated ozone induces jasmonic acid defense of tomato plants and reduces midgut proteinase activity in Helicoverpa armigera

As a consequence of membrane lipid peroxidation, foliar defense compounds are changed by elevated ozone (O3), which in turn affects the palatability and performance of insect herbivores. The induced defense of two tomato [Solanum esculentum L. (Solanaceae)] genotypes, namely jasmonic acid (JA) pathway‐deficient mutant spr2 and its wild‐type control, was studied in response to cotton bollworm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae), as well as the digestive adaptation of these insects under elevated O3 in open‐top field chambers. Our data indicated that elevated O3 increased foliar JA and salicylic acid (SA) levels simultaneously and up‐regulated proteinase inhibitors (PIs) and lipoxidase activities in wild‐type plants, regardless of H. armigera infestation. In contrast, only the O3+H. armigera treatment increased free SA levels in spr2 plants, but did not affect JA level or PI activities. Additionally, the lower activity of midgut digestive enzymes, including active alkaline trypsin‐like enzyme and chymotrypsin‐like enzyme, was observed in the midgut of cotton bollworms after they consumed wild‐type plants treated for 2 h with elevated O3. With temporary increases at 8 h, all four digestive enzymes of interest in the insect midgut dropped when they were fed with wild‐type plants under elevated O3 treatment. Increases in atmospheric O3 are thought to increase JA signaling and consequently reduce the activities of midgut digestive enzymes in H. armigera, therefore enhancing plant resistance against insect herbivores.

[1]  Suli Huang,et al.  The Dose–Response Decrease in Heart Rate Variability: Any Association with the Metabolites of Polycyclic Aromatic Hydrocarbons in Coke Oven Workers? , 2012, PloS one.

[2]  Chuanyou Li,et al.  Elevated CO2 Reduces the Resistance and Tolerance of Tomato Plants to Helicoverpa armigera by Suppressing the JA Signaling Pathway , 2012, PloS one.

[3]  M. Xie,et al.  Volatile Emissions from the Invasive Weed Eupatorium adenophorum Induced by Aphis gossypii Feeding and Methyl Jasmonate Treatment , 2010, Weed Science.

[4]  S. Wilkinson,et al.  Drought, ozone, ABA and ethylene: new insights from cell to plant to community. , 2010, Plant, cell & environment.

[5]  P. Reymond,et al.  Insect eggs suppress plant defence against chewing herbivores. , 2010, The Plant journal : for cell and molecular biology.

[6]  R. Julkunen‐Tiitto,et al.  Do elevated atmospheric CO2 and O3 affect food quality and performance of folivorous insects on silver birch? , 2010 .

[7]  E. DeLucia,et al.  Elevated atmospheric carbon dioxide and ozone alter soybean diseases at SoyFACE , 2010 .

[8]  M. A. Martínez-Ghersa,et al.  Getting the interactions right: will higher O3 levels interfere with induced defenses to aphid feeding? , 2009 .

[9]  E. DeLucia,et al.  Elevated ozone alters soybean-virus interaction. , 2008, Molecular plant-microbe interactions : MPMI.

[10]  I. Baldwin,et al.  Digestive Duet: Midgut Digestive Proteinases of Manduca sexta Ingesting Nicotiana attenuata with Manipulated Trypsin Proteinase Inhibitor Expression , 2008, PloS one.

[11]  M. Berenbaum,et al.  Transcriptional profiling reveals elevated CO2 and elevated O3 alter resistance of soybean (Glycine max) to Japanese beetles (Popillia japonica). , 2008, Plant, cell & environment.

[12]  M. Clerici,et al.  Peripheral Blood Endothelial Progenitors as Potential Reservoirs of Kaposi's Sarcoma-Associated Herpesvirus , 2008, PloS one.

[13]  K. Zhu‐Salzman,et al.  Cowpea bruchid Callosobruchus maculatus counteracts dietary protease inhibitors by modulating propeptides of major digestive enzymes , 2007, Insect molecular biology.

[14]  B. Gimeno,et al.  Risk assessments for forest trees: the performance of the ozone flux versus the AOT concepts. , 2007, Environmental pollution.

[15]  Julia Koricheva,et al.  Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta‐analysis , 2007 .

[16]  E. Zvereva,et al.  Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a metaanalysis , 2006 .

[17]  À. Bayés,et al.  Structural basis of the resistance of an insect carboxypeptidase to plant protease inhibitors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  A. Chidthaisong,et al.  Effects of Elevated Ozone Concentrations on Thai Jasmine Rice Cultivars (Oryza Sativa L.) , 2005 .

[19]  R. Bostock Signal crosstalk and induced resistance: straddling the line between cost and benefit. , 2005, Annual review of phytopathology.

[20]  J. Kangasjärvi,et al.  Signalling and cell death in ozone‐exposed plants , 2005 .

[21]  B. Oppert,et al.  A chymotrypsin-like proteinase from the midgut of Tenebrio molitor larvae. , 2005, Biochimie.

[22]  M. Ashmore Assessing the future global impacts of ozone on vegetation , 2005 .

[23]  E. P. McDonald,et al.  CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria) , 2005 .

[24]  J. Gatehouse,et al.  Plant-insect interactions: molecular approaches to insect resistance. , 2004, Current opinion in biotechnology.

[25]  K. Gruden,et al.  Molecular basis of Colorado potato beetle adaptation to potato plant defence at the level of digestive cysteine proteinases. , 2004, Insect biochemistry and molecular biology.

[26]  L. Juliano,et al.  Coevolution of insect trypsins and inhibitors. , 2004, Archives of insect biochemistry and physiology.

[27]  I. Baldwin,et al.  Manipulation of Endogenous Trypsin Proteinase Inhibitor Production in Nicotiana attenuata Demonstrates Their Function as Antiherbivore Defenses1[w] , 2004, Plant Physiology.

[28]  M. Aono,et al.  Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression , 2003, Plant Molecular Biology.

[29]  S. Long,et al.  How does elevated ozone impact soybean? A meta‐analysis of photosynthesis, growth and yield , 2003 .

[30]  J. Kangasjärvi,et al.  Differential Effects of Elevated Ozone on Two Hybrid Aspen Genotypes Predisposed to Chronic Ozone Fumigation. Role of Ethylene and Salicylic Acid1 , 2003, Plant Physiology.

[31]  G. Thompson,et al.  Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. , 2002, Archives of insect biochemistry and physiology.

[32]  H. Porta,et al.  Plant Lipoxygenases. Physiological and Molecular Features , 2002, Plant Physiology.

[33]  S. Grün,et al.  Oxidative burst and cell death in ozone-exposed plants , 2002 .

[34]  P. Lawrence,et al.  Plant protease inhibitors in control of phytophagous insects , 2002 .

[35]  D. Inzé,et al.  Oxidative Burst and the Role of Reactive Oxygen Species in Plant-pathogen Interactions , 2001 .

[36]  K. Pihlaja,et al.  Effects of Long-Term Open-Field Ozone Exposure on Leaf Phenolics of European Silver Birch (Betula pendula Roth) , 2001, Journal of Chemical Ecology.

[37]  I. Baldwin,et al.  Ontogeny Constrains Systemic Protease Inhibitor Response in Nicotiana attenuata , 2001, Journal of Chemical Ecology.

[38]  R. Creelman,et al.  Jasmonic Acid Signaling Modulates Ozone-Induced Hypersensitive Cell Death , 2000, Plant Cell.

[39]  Ceci,et al.  Opposite effects on spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants , 1998, Plant physiology.

[40]  K. Gruden,et al.  The cysteine protease activity of Colorado potato beetle (Leptinotarsa decemlineata Say) guts, which is insensitive to potato protease inhibitors, is inhibited by thyroglobulin type-1 domain inhibitors. , 1998, Insect biochemistry and molecular biology.

[41]  I. Mitsuhara,et al.  Antagonistic Effect of Salicylic Acid and Jasmonic Acid on the Expression of Pathogenesis-Related (PR) Protein Genes in Wounded Mature Tobacco Leaves , 1998 .

[42]  M. Jongsma,et al.  The adaptation of insects to plant protease inhibitors. , 1997, Journal of insect physiology.

[43]  R. Broadway Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. , 1997, Journal of insect physiology.

[44]  R. Karban,et al.  Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field , 1996, Journal of Chemical Ecology.

[45]  P. Hasegawa,et al.  Plant Defense Genes Are Synergistically Induced by Ethylene and Methyl Jasmonate. , 1994, The Plant cell.

[46]  D. Klessig,et al.  Temperature-Dependent Induction of Salicylic Acid and Its Conjugates during the Resistance Response to Tobacco Mosaic Virus Infection. , 1992, The Plant cell.

[47]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[48]  William W. Cohen,et al.  The preparation and properties of two new chromogenic substrates of trypsin. , 1961, Archives of biochemistry and biophysics.

[49]  F. Ge,et al.  Effect of elevated O3 associated with Bt cotton on the abundance, diversity and community structure of soil Collembola , 2011 .

[50]  Xiaoke Wang,et al.  Effects of elevated ozone on growth and yield of field-grown rice in Yangtze River Delta, China. , 2008, Journal of environmental sciences.

[51]  T. Rufty,et al.  Survival and Development of Tobacco Hornworm Larvae on Tobacco Plants Grown Under Elevated Levels of Ozone , 2004, Journal of Chemical Ecology.

[52]  Y. Birk Plant Protease Inhibitors: Significance in Nutrition, Plant Protection, Cancer Prevention and Genetic Engineering , 2003 .

[53]  P. Ranjekar,et al.  Chickpea Defensive Proteinase Inhibitors Can Be Inactivated by Podborer Gut Proteinases , 1998 .

[54]  H. Sandermann,et al.  Ozone and plant health. , 1996, Annual review of phytopathology.

[55]  P. Hughes,et al.  Influence of ozone air pollution on plant-herbivore interactions. Part 2: Effects of ozone on feeding preference, growth and consumption rates of monarch butterflies (Danaus plexippus). , 1992, Environmental pollution.

[56]  S. Duffey,et al.  Plant proteinase inhibitors: Mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exiqua , 1986 .