Dynamic Changes in Plant Secondary Metabolites Induced by Botrytis cinerea Infection

In response to pathogen infection, some plants increase production of secondary metabolites, which not only enhance plant defense but also induce fungicide resistance, especially multidrug resistance (MDR) in the pathogen through preadaptation. To investigate the cause of MDR in Botrytis cinerea, grapes ‘Victoria’ (susceptible to B. cinerea) and ‘Shine Muscat’ (resistant to B. cinerea) were inoculated into seedling leaves with B. cinerea, followed by extraction of metabolites from the leaves on days 3, 6, and 9 after inoculation. The extract was analyzed using gas chromatography/quadrupole time-of-flight mass (GC/QTOF) combined with solid-phase microextraction (SPME) for volatile and nonvolatile metabolomic components. Nonvolatile metabolites γ-aminobutyric acid (GABA), resveratrol, piceid, and some carbohydrates or amino acids, coupled with volatile metabolites β-ocimene, α-farnesene, caryophyllene, germacrene D, β-copaene, and alkanes, accumulated at a higher level in grape leaves infected with B. cinerea compared to in noninoculated leaves. Among the established metabolic pathways, seven had greater impacts, including aminoacyl-tRNA biosynthesis, galactose metabolism, valine, leucine, and isoleucine biosynthesis. Furthermore, isoquinoline alkaloid biosynthesis; phenylpropanoid biosynthesis; monobactam biosynthesis; tropane, piperidine, and pyridine alkaloid biosynthesis; phenylalanine metabolism; and glucosinolate biosynthesis were related to antifungal activities. Based on liquid chromatography/quadrupole time-of-flight mass (LC/QTOF) detection and bioassay, B. cinerea infection induced production of plant secondary metabolites (PSMs) including eugenol, flavanone, reserpine, resveratrol, and salicylic acid, which all have inhibitory activity against B. cinerea. These compounds also promoted overexpression of ATP-binding cassette (ABC) transporter genes, which are involved in induction of MDR in B. cinerea.

[1]  Nicole R. Buan,et al.  The effects of exogenously applied antioxidants on plant growth and resilience , 2023, Phytochemistry Reviews.

[2]  Yin Zhu,et al.  Comprehensive investigation on non-volatile and volatile metabolites in four types of green teas obtained from the same tea cultivar of Longjing 43 (Camellia sinensis var. sinensis) using the widely targeted metabolomics. , 2022, Food chemistry.

[3]  I. Feussner,et al.  N-Hydroxy pipecolic acid methyl ester is involved in Arabidopsis immunity , 2022, bioRxiv.

[4]  A. Fernie,et al.  Plant metabolic gene clusters in the multi-omics era. , 2022, Trends in plant science.

[5]  G. Tzelepis,et al.  A Verticillium longisporum pleiotropic drug transporter determines tolerance to the plant host β‐pinene monoterpene , 2021, Molecular plant pathology.

[6]  O. Zabotina,et al.  Coexpression of Fungal Cell Wall-Modifying Enzymes Reveals Their Additive Impact on Arabidopsis Resistance to the Fungal Pathogen, Botrytis cinerea , 2021, Biology.

[7]  Xiping Wang,et al.  The impact of Elsinoë ampelina-infection on key metabolic properties in Vitis vinifera cv. Red Globe berries via multi-omics approaches. , 2021, Molecular plant-microbe interactions : MPMI.

[8]  R. Nauen,et al.  Comparative analysis of the detoxification gene inventory of four major Spodoptera pest species in response to xenobiotics. , 2021, Insect biochemistry and molecular biology.

[9]  Nada M. Mostafa,et al.  Metabolomic Profiles of Essential Oils from Selected Rosa Varieties and Their Antimicrobial Activities , 2021, Plants.

[10]  R. Nauen,et al.  Transcriptional regulation of xenobiotic detoxification genes in insects - An overview. , 2021, Pesticide biochemistry and physiology.

[11]  Xiaolin Li,et al.  Metabolic Mechanism of Plant Defense against Rice Blast Induced by Probenazole , 2021, Metabolites.

[12]  Zhìhóng Hú,et al.  Characterization of the Field Fludioxonil Resistance and Its Molecular Basis in Botrytis cinerea from Shanghai Province in China , 2021, Microorganisms.

[13]  Youjun Zhang,et al.  Plant flavonoids enhance the tolerance to thiamethoxam and flupyradifurone in whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). , 2020, Pesticide biochemistry and physiology.

[14]  D. Newman,et al.  Bacterial defenses against a natural antibiotic promote collateral resilience to clinical antibiotics , 2020, bioRxiv.

[15]  Yanni Yin,et al.  A fungal ABC transporter FgAtm1 regulates iron homeostasis via the transcription factor cascade FgAreA-HapX , 2019, PLoS pathogens.

[16]  D. Chagné,et al.  Genetic control of α-farnesene production in apple fruit and its role in fungal pathogenesis. , 2019, The Plant journal : for cell and molecular biology.

[17]  J. Meis,et al.  Invasive Aspergillosis by Aspergillus flavus: Epidemiology, Diagnosis, Antifungal Resistance, and Management , 2019, Journal of fungi.

[18]  Zhi-Wei Kang,et al.  Volatile β-Ocimene Can Regulate Developmental Performance of Peach Aphid Myzus persicae Through Activation of Defense Responses in Chinese Cabbage Brassica pekinensis , 2018, Front. Plant Sci..

[19]  N. Desneux,et al.  Uptake of quercetin reduces larval sensitivity to lambda-cyhalothrin in Helicoverpa armigera , 2018, Journal of Pest Science.

[20]  Zenghui Sun,et al.  Induction of systemic resistance in tomato against Botrytis cinerea by N-decanoyl-homoserine lactone via jasmonic acid signaling , 2018, Planta.

[21]  W. Xie,et al.  Identification of glutathione S‐transferases in Bemisia tabaci (Hemiptera: Aleyrodidae) and evidence that GSTd7 helps explain the difference in insecticide susceptibility between B. tabaci Middle East‐Minor Asia 1 and Mediterranean , 2018, Insect molecular biology.

[22]  Ying Liu,et al.  Elevated carboxylesterase activity contributes to the lambda-cyhalothrin insensitivity in quercetin fed Helicoverpa armigera (Hübner) , 2017, PloS one.

[23]  S. Tyerman,et al.  γ-Aminobutyric acid (GABA) signalling in plants , 2017, Cellular and Molecular Life Sciences.

[24]  W. Mu,et al.  Baseline Sensitivity of Botrytis cinerea to the Succinate Dehydrogenase Inhibitor Isopyrazam and Efficacy of this Fungicide. , 2016, Plant disease.

[25]  N. Shitan,et al.  Secondary metabolites in plants: transport and self-tolerance mechanisms , 2016, Bioscience, biotechnology, and biochemistry.

[26]  Z. Miszalski,et al.  Plastoquinone redox state modifies plant response to pathogen. , 2015, Plant physiology and biochemistry : PPB.

[27]  M. Deabes,et al.  Chemical Composition and Antifungal Activity of Ocimum basilicum L. Essential Oil , 2015, Open access Macedonian journal of medical sciences.

[28]  M. Haring,et al.  Green Leaf Volatiles: A Plant’s Multifunctional Weapon against Herbivores and Pathogens , 2013, International journal of molecular sciences.

[29]  Kathrine B. Christensen,et al.  Semi-preparative isolation of dihydroresveratrol-3-O-β-d-glucuronide and four resveratrol conjugates from human urine after oral intake of a resveratrol-containing dietary supplement. , 2013, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[30]  M. Frías,et al.  The Botrytis cinerea cerato-platanin BcSpl1 is a potent inducer of systemic acquired resistance (SAR) in tobacco and generates a wave of salicylic acid expanding from the site of application. , 2013, Molecular plant pathology.

[31]  J. Zeier,et al.  Pipecolic Acid, an Endogenous Mediator of Defense Amplification and Priming, Is a Critical Regulator of Inducible Plant Immunity[W] , 2012, Plant Cell.

[32]  G. Montenegro,et al.  ANTIFUNGAL ACTIVITY OF THREE CHILEAN PLANT EXTRACTS ON BOTRYTIS CINEREA , 2012 .

[33]  S. Fillinger,et al.  Strong resistance to the fungicide fenhexamid entails a fitness cost in Botrytis cinerea, as shown by comparisons of isogenic strains. , 2012, Pest management science.

[34]  E. M. Soylu,et al.  In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. , 2010, International journal of food microbiology.

[35]  Thomas D. Schmittgen,et al.  Analyzing real-time PCR data by the comparative CT method , 2008, Nature Protocols.

[36]  K. Matsui,et al.  Analysis of defensive responses activated by volatile allo-ocimene treatment in Arabidopsis thaliana. , 2006, Phytochemistry.

[37]  H. Schoonbeek,et al.  Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. , 2006, Pest management science.

[38]  W. Su,et al.  A rapid LC/MS/MS quantitation assay for naringin and its two metabolites in rats plasma. , 2006, Journal of pharmaceutical and biomedical analysis.

[39]  J. Glazebrook Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. , 2005, Annual review of phytopathology.

[40]  K. Matsui,et al.  Volatile C6-aldehydes and Allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. , 2005, Plant & cell physiology.

[41]  L. Elviri,et al.  Liquid chromatography-electrospray tandem mass spectrometry of cis-resveratrol and trans-resveratrol: development, validation, and application of the method to red wine, grape, and winemaking byproducts. , 2004, Journal of agricultural and food chemistry.

[42]  Bruce D. Whitaker,et al.  Cloning and functional expression of an (E,E)-α-farnesene synthase cDNA from peel tissue of apple fruit , 2004, Planta.

[43]  R. Ferreira,et al.  Osmotin and thaumatin from grape: a putative general defense mechanism against pathogenic fungi. , 2003, Phytopathology.

[44]  H. Schoonbeek,et al.  Bcmfs1, a Novel Major Facilitator Superfamily Transporter from Botrytis cinerea, Provides Tolerance towards the Natural Toxic Compounds Camptothecin and Cercosporin and towards Fungicides , 2002, Applied and Environmental Microbiology.

[45]  M. Sbaghi,et al.  Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. , 2002, Journal of agricultural and food chemistry.

[46]  H. Hamamoto,et al.  A novel ABC transporter gene, PMR5, is involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum , 2002, Molecular Genetics and Genomics.

[47]  B. Williamson,et al.  Botrydial is produced in plant tissues infected by Botrytis cinerea. , 2001, Phytochemistry.

[48]  H. Schoonbeek,et al.  The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. , 2001, Molecular plant-microbe interactions : MPMI.

[49]  L. Zwiers,et al.  Characterization of the ABC transporter genes MgAtr1 and MgAtr2 from the wheat pathogen Mycosphaerella graminicola. , 2000, Fungal genetics and biology : FG & B.

[50]  A. Osbourn,et al.  Fungal Resistance to Plant Antibiotics as a Mechanism of Pathogenesis , 1999, Microbiology and Molecular Biology Reviews.

[51]  R. Lamuela-Raventós,et al.  Piceid, the major resveratrol derivative in grape juices. , 1999, Journal of agricultural and food chemistry.

[52]  M. Wisniewski,et al.  Rapid Evaluation of Plant Extracts and Essential Oils for Antifungal Activity Against Botrytis cinerea. , 1997, Plant disease.

[53]  Fa-ching Chen,et al.  RHUSFLAVANONE, A NEW BIFLAVANONE FROM THE SEEDS OF WAX TREE , 1976 .

[54]  Layla G. Sharp,et al.  Volatile components of the aerial parts of Prunella vulgaris L. (Lamiaceae) , 2020 .

[55]  I. Ślesak,et al.  Crassulacean Acid Metabolism and Its Role in Plant Acclimatization to Abiotic Stresses and Defence Against Pathogens , 2019, Progress in Botany.

[56]  F. Carrari,et al.  Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection. , 2010, Phytochemistry.

[57]  M. Sbaghi,et al.  The Significance of Stilbene-Type Phytoalexin Degradation by Culture Filtrates of Botrytis Cinerea in the Vine- Botrytis Interaction , 1993 .

[58]  R. Miller,et al.  Development of Methods for Screening Grapevines for Resistance to Infection by Downy Mildew. II. Resveratrol Production , 1987, American Journal of Enology and Viticulture.

[59]  R. Miller,et al.  Development of Methods for Screening Grapevines for Resistance to Infection by Downy Mildew. I. Dual Culturein vitro , 1986, American Journal of Enology and Viticulture.