Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Ozone triggers different defence mechanisms against powdery mildew (Blumeria graminis DC. Speer f. sp. tritici) in susceptible and resistant wheat genotypes

Sercan Pazarlar A , Nedim Cetinkaya A , Melike Bor B C and Filiz Ozdemir B
+ Author Affiliations
- Author Affiliations

A University of Ege, Faculty of Agriculture, Department of Plant Protection, 35100 Izmir, Turkey.

B University of Ege, Faculty of Science, Department of Biology, 35100 Izmir, Turkey.

C Corresponding author. Email: melike.bor@ege.edu.tr

Functional Plant Biology 44(10) 1016-1028 https://doi.org/10.1071/FP17038
Submitted: 2 February 2017  Accepted: 15 June 2017   Published: 18 July 2017

Abstract

Ozone has been proposed as a convenient elicitor against pathogens since it is known to generate different reactive oxygen species (ROS) and induce nonspecific defence by altering gene expression. The mode of action and its interaction with other defence pathways are yet to be elucidated. Besides its negative effects on plants, ozone can be used for triggering defence against environmental stresses, including pathogens, when used at appropriate concentrations. Powdery mildew, caused by the obligate biotrophic fungus Blumera graminis f.sp. tritici (Bgt), is an important plant disease that reduces crop yield and quality. We hypothesised that ozone treatment may elicit defence against Bgt by inducing ROS signalling or other routes such as the salicylic acid (SA) or jasmonic acid (JA) pathways. We conducted experiments with Bgt-susceptible (cv. Pamukova) and resistant (cv. Tahirova) wheat (Triticum aestivum L,) cultivars and treated them with different ozone concentrations before Bgt inoculation. Stress response and defence-related features such as antioxidative enzyme activity; lipid peroxidation; H2O2 and Ca+2 levels; PR1, LOX, PAL and RBOH gene expression; and disease severity were assayed. Clear discrepancies between the responses of susceptible and resistant cultivars were found, suggesting that different defence routes were activated. Here, we showed that ozone treatment was effective for diminishing Bgt invasion in the susceptible cultivar in the short term, which was probably related to defence induced via the SA pathway. Moreover, the resistant cultivar Tahirova exhibited a different mode of action against the pathogen that was triggered by ozone treatment, plausibly related to the JA pathway.

Additional keywords: fungus, jasmonic acid, pathogen, ROS signalling, salicylic acid, Triticum aestivum L.


References

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlsVGitLk%3D&md5=7defff6fc79bf274d695d8ed5adb8abcCAS |

Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276–287.
Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XjtFKhsg%3D%3D&md5=41a81f7134ea2a9b8a235b3333eaa8b0CAS |

Bergmeyer N (1970) ‘Methoden der enzymatischen analyse.’ (Akademie Verlag: Berlin)

Biagioni M, Nali C, Heimler D, Lorenzini G (1997) PAL activity and differential ozone sensitivity in tobacco, bean and poplar. Journal of Phytopathology 145, 533–539.
PAL activity and differential ozone sensitivity in tobacco, bean and poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvV2nuw%3D%3D&md5=20238419b41a8af1b8ab90e44707bf09CAS |

Bilgin DD, Aldea M, O’Neill BF, Benitez M, Li M, Clough SJ, DeLucia EH (2008) Elevated ozone alters soybean–virus interaction. Molecular Plant—Microbe Interactions 21, 1297–1308.
Elevated ozone alters soybean–virus interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFChtbzJ&md5=5fbe0f57243bef5fc4ba7702efe2502dCAS |

Biswas DK, Xu H, Li YG, Sun JZ, Wang XZ, Han XG, Jiang GM (2008) Genotypic differences in leaf biochemical, physiological and growth responses to ozone in 20 winter wheat cultivars released over the past 60 years. Global Change Biology 14, 46–59.

Bor M, Ozdemir F, Türkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Science 164, 77–84.
The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFertrw%3D&md5=eca15f72a98f3a8595629d8a647f7403CAS |

Boyd JM, Gallo GJ, Elangovan B, Houghton AB, Malstrom S, Avery BJ, Ebb RG, Subramanian T, Chittenden T, Lutz RJ (1995) Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene 11, 1921–1928.

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=2821bcfbf01a16b0f1b14eb3a73c5812CAS |

Bradley DJ, Kjellbom I, Lamb CJ (1992) Elicitor and wound induced oxidative cross-linking of a plant cell wall proline-rich protein: a novel, rapid defence response. Cell 70, 21–30.
Elicitor and wound induced oxidative cross-linking of a plant cell wall proline-rich protein: a novel, rapid defence response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlvVygtLk%3D&md5=659797b4cbf0033be1c89f9af6647ebdCAS |

Büker P, Morrissey T, Briolat A, Falk R, Simpson D, Tuovinen JP, Alonso R, Barth S, Baumgarten M, Grulke N, Karlsson PE, King J, Lagergren F, Matyssek R, Nunn A, Ogaya R, Pẽuelas J, Rhea L, Schaub M, Uddling J, Werner W, Emberson LD (2012) DO3SE modelling of soil moisture to determine ozone flux to forest trees. Atmospheric Chemistry and Physics 12, 5537–5562.
DO3SE modelling of soil moisture to determine ozone flux to forest trees.Crossref | GoogleScholarGoogle Scholar |

Daudi A, Cheng Z, O’Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP (2012) The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. The Plant Cell 24, 275–287.
The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOks78%3D&md5=83620fbb58822e21a3c842deca78c856CAS |

Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nature Reviews Genetics 11, 539–548.
Plant immunity: towards an integrated view of plant–pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovFOhtrs%3D&md5=d9fdbf42a65eeadb23de051b444ae1c6CAS |

Eckey-Kaltenbach H, Ernst D, Heller W, Sandermann JH (1994) Biochemical plant responses to ozone. Plant Physiology 104, 67–74.
Biochemical plant responses to ozone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFKit74%3D&md5=ef4a478798e2b5e872ded97d7614f8feCAS |

Ellis R, Hanway JJ, Holmgren G, Keeney DR, Bidwell OW (1973) ‘Sampling and analysis of soils, plants, waste waters, and sludge-suggested standardization and methodology. Research Publication 170.’ (Agricultural Experimental Station, Kansas State University: Manhattan, KS).

Enright S, Cipollini D (2011) Overlapping defence responses to water limitation and pathogen attack and their consequences for resistance to powdery mildew disease in garlic mustard, Alliaria petiolate. Chemoecology 21, 89–98.
Overlapping defence responses to water limitation and pathogen attack and their consequences for resistance to powdery mildew disease in garlic mustard, Alliaria petiolate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvVSrs78%3D&md5=380e79ad88f55e20169aab365a08432dCAS |

Fabro G, Rizzi YS, Alvarez ME (2016) Arabidopsis proline dehydrogenase contributes to flagellin-mediated PAMP-triggered Immunity by affecting RBOHD. Molecular Plant—Microbe Interactions 29, 620–628.
Arabidopsis proline dehydrogenase contributes to flagellin-mediated PAMP-triggered Immunity by affecting RBOHD.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhslCit7rJ&md5=59dcd9d60909bbea6c8120048180c835CAS |

Faoro F, Iriti M (2009) Plant cell death and cellular alterations induced by ozone: key studies in Mediterranean conditions. Environmental Pollution 157, 1470–1477.
Plant cell death and cellular alterations induced by ozone: key studies in Mediterranean conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktF2lu70%3D&md5=a5483fd66bd50429753ea6cef6d16431CAS |

Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linsyead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446.
Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlGgtLg%3D&md5=dc90ce6dd130e8a7fd34100cf7f77cd1CAS |

Foyer CH, Halliwell B (1976) Presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21–25.
Presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2czlsVeltA%3D%3D&md5=aa5e917cc8f2851aa0b02b36fcfdb226CAS |

Ghanta S, Chattopadhyay S (2011) Glutathione as a signalling molecule. Plant Signaling & Behavior 6, 783–788.
Glutathione as a signalling molecule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitlOit7Y%3D&md5=f310cf594b7557204e331b7b12952ff5CAS |

Gillespie C, Stabler D, Tallentire E, Goumenaki E, Barnes J (2015) Exposure to environmentally-relevant levels of ozone negatively influence pollen and fruit development. Environmental Pollution 206, 494–501.
Exposure to environmentally-relevant levels of ozone negatively influence pollen and fruit development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht12ku7nM&md5=05fdaaf5c9fb28a8c5f90fb4b7f29a45CAS |

Girotti AW (1998) Lipid hydroperoxide generation, turnover, and effector action in biological systems. Journal of Lipid Research 39, 1529–1542.

Glazebrook J (2005) Contrasting mechanisms of defence against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205–227.
Contrasting mechanisms of defence against biotrophic and necrotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOksrrN&md5=9ce42df9ede136cba96eb4855c9b1ac0CAS |

Herzog V, Fahimi H (1973) Determination of the activity of peroxidase. Analytical Biochemistry 55, 554–562.
Determination of the activity of peroxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlt1aqsLw%3D&md5=16b9ace7c8b71571a511eb178d3fc6acCAS |

Howe GA (2004) Jasmonates as signals in wound response. Journal of Plant Growth Regulation 23, 223–237.
Jasmonates as signals in wound response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislSlt78%3D&md5=1ef4948613e28e18011a830ce45c657bCAS |

Jaspers P, Kollist H, Langebartels C, Kangasjarvi J (2005) Plant responses to ozone. In ‘Antioxidants and reactive oxygen species in plants’. (Ed. N. Smirnoff.) pp. 268–292. (Blackwell: Oxford, UK.

Liu X, Sui L, Huang Y, Geng C, Yin B (2015) Physiological and visible injury responses in different growth stages of winter wheat to ozone stress and the protection of spermidine. Atmospheric Pollution Research 6, 596–604.
Physiological and visible injury responses in different growth stages of winter wheat to ozone stress and the protection of spermidine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFymsrzF&md5=89f1a21911782c3cd9a5e67705941362CAS |

Madhava Rao KV, Sresty TV (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Science 157, 113–128.
Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFCjtL4%3D&md5=522619edd9d6f4aafb0c2fa8b9d00af7CAS |

Mudd JB, Freeman BA (1977) Reaction of ozone with biological membranes. In: ‘Biochemical effects of environmental pollutants’. (Ed. SD Lee) pp. 97–133. (Ann Arbor Science Publications: Ann Arbor, MI)

Munné-Bosch S, Peñuelas J (2004) Drought induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions. Plant Science 166, 1105–1110.
Drought induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions.Crossref | GoogleScholarGoogle Scholar |

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.

Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. The Plant Cell 22, 3130–3141.
HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVKjs7vL&md5=c099c74aa5689fcad42b7f82a37d8ab7CAS |

Orton ES, Brown JMK (2016) Reduction of growth and reproduction of biothrophic fungus Blumeria graminis in the presence of a necrotrophic pathogen. Frontiers in Plant Science 7, 742–752.
Reduction of growth and reproduction of biothrophic fungus Blumeria graminis in the presence of a necrotrophic pathogen.Crossref | GoogleScholarGoogle Scholar |

Ozkur O, Ozdemir F, Bor M, Turkan I (2009) Physiological and antioxidant responses of the perennial xerophyte Capparis ovata Desf. to drought. Environmental and Experimental Botany 66, 487–492.
Physiological and antioxidant responses of the perennial xerophyte Capparis ovata Desf. to drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsV2ku7s%3D&md5=b740665095bc19c3277c1a051080c5a4CAS |

Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Current Opinion in Plant Biology 6, 320–326.
Establishing compatibility between plants and obligate biotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsValt7c%3D&md5=2ddb54873b599b6df4dd9c1353c10ebaCAS |

Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5, 308–316.
Networking by small-molecule hormones in plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks12ktL4%3D&md5=4f5ad9041169dad5e60c16181478f72cCAS |

Ramel F, Sulmon C, Bogard M, Couée I, Gouesbet G (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biology 9, 28
Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets.Crossref | GoogleScholarGoogle Scholar |

Rao MV, Koch JR, Davis KR (2000) Ozone: a tool for probing programmed cell death in plants. Plant Molecular Biology 44, 345–358.
Ozone: a tool for probing programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFajsQ%3D%3D&md5=cb09a3299bd5b1647e2d05e656672135CAS |

Rao MV, Lee H, Davis KR (2002) Ozone induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. The Plant Journal 32, 447–456.
Ozone induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1Kruro%3D&md5=59c2ceae50f07ed9d178e8256a9ebd05CAS |

Rusch H, Laurence JA (1993) Interactive effects of ozone and powdery mildew on pea seedlings. Phytopathology 83, 1258–1263.
Interactive effects of ozone and powdery mildew on pea seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFKis7Y%3D&md5=42ab51d91d1af57d3ea4f48aa95d168eCAS |

Sandermann H, Dieter Ernst J, Heller W, Langebartels C (1998) Ozone: an abiotic elicitor of plant defence reactions. Trends in Plant Science 3, 47–50.
Ozone: an abiotic elicitor of plant defence reactions.Crossref | GoogleScholarGoogle Scholar |

Sharma YK, Leon J, Raskin I, Davis KR (1996) Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defence-related transcripts and induced resistance. Proceedings of the National Academy of Sciences of the United States of America 93, 5099–5104.
Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defence-related transcripts and induced resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtVKlur0%3D&md5=e52a2220690ef8fbb0717e891c48318dCAS |

Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends in Plant Science 15, 89–97.
Proline: a multifunctional amino acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1yit7s%3D&md5=4661dc67199f253edaa35b9741678b02CAS |

Tamaoki M (2008) The role of phytohormone signaling in ozone induced cell death in plants. Plant Signaling & Behavior 3, 166–174.
The role of phytohormone signaling in ozone induced cell death in plants.Crossref | GoogleScholarGoogle Scholar |

Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8, 397–403.
Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFGgtrg%3D&md5=5bf1b968b86863965f1105f01ae15485CAS |

Tuomainen J, Pellinen R, Roy S, Kiiskinen M, Eloranta T, Karjalainen R, Kangasjärvi J (1996) Ozone affects birch (Betula pendula Roth) phenylpropanoid, polyamine and active oxygen detoxifying pathways at biochemical and gene expression levels. Journal of Plant Physiology 148, 179–188.
Ozone affects birch (Betula pendula Roth) phenylpropanoid, polyamine and active oxygen detoxifying pathways at biochemical and gene expression levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtVGhtrg%3D&md5=f51df8bb99868fb6c2f1cd636b93f340CAS |

Vechet L, Burketova L, Sindelarova M (2009) A comparative study of the efficiency of several sources of induced resistance to powdery mildew (Blumera graminis f. sp. tritici) in wheat under field conditions. Crop Protection 28, 151–154.
A comparative study of the efficiency of several sources of induced resistance to powdery mildew (Blumera graminis f. sp. tritici) in wheat under field conditions.Crossref | GoogleScholarGoogle Scholar |

Violini G (1995) Ozone and plant pathogens. Rivista di Patologia Vegetale 5, 113–130.

Walters D, Walsh D, Newton A, Lyon G (2005) Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 95, 1368–1373.
Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCjtL%2FK&md5=1bf6c05bc12976e3ec2123b7ca05b174CAS |

Wang J, Zeng Q, Zhu J, Chen C, Liu G, Tang H (2014) Apoplastic antioxidant enzyme responses to chronic free-air ozone exposure in two different ozone-sensitive wheat cultivars. Plant Physiology and Biochemistry 82, 183–193.
Apoplastic antioxidant enzyme responses to chronic free-air ozone exposure in two different ozone-sensitive wheat cultivars.Crossref | GoogleScholarGoogle Scholar |

Wang YJ, Wei XY, Jing XQ, Chang YL, Hu CH, Wang X, Chen KM (2016) The fundamental role of NOX family proteins in plant immunity and their regulation. International Journal of Molecular Sciences 17, 805
The fundamental role of NOX family proteins in plant immunity and their regulation.Crossref | GoogleScholarGoogle Scholar |

Wiese A, Elzinga N, Wobbes B, Smeekens S (2004) A conserved upstream open reading frame mediates sucrose-induced repression of translation. The Plant Cell 16, 1717–1729.
A conserved upstream open reading frame mediates sucrose-induced repression of translation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFSqt7g%3D&md5=89abd1c2c0fe9a6fed6716bff2563d70CAS |

Zhang Z, Henderson C, Perfect E, Carver TL, Thomas BJ, Skamnioti P (2005) Of genes and genomes, needles and haystacks: Blumera graminis and functionality. Molecular Plant Pathology 6, 561–575.
Of genes and genomes, needles and haystacks: Blumera graminis and functionality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVykt7jE&md5=21a347703b11f58772177f4999c9be22CAS |