192 research outputs found

    Relationship between petal abscission and programmed cell death in Prunus yedoensis and Delphinium belladonna

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    Depending on the species, the end of flower life span is characterized by petal wilting or by abscission of petals that are still fully turgid. Wilting at the end of petal life is due to programmed cell death (PCD). It is not known whether the abscission of turgid petals is preceded by PCD. We studied some parameters that indicate PCD: chromatin condensation, a decrease in nuclear diameter, DNA fragmentation, and DNA content per nucleus, using Prunus yedoensis and Delphiniumbelladonna which both show abscission of turgid petals at the end of floral life. No DNA degradation, no chromatin condensation, and no change in nuclear volume was observed in P. yedoensis petals, prior to abscission. In abscising D.belladonna petals, in contrast, considerable DNA degradation was found, chromatin was condensed and the nuclear volume considerably reduced. Following abscission, the nuclear area in both species drastically increased, and the chromatin became unevenly distributed. Similar chromatin changes were observed after dehydration (24 h at 60°C) of petals severed at the time of flower opening, and in dehydrated petals of Ipomoea nil and Petunia hybrida, severed at the time of flower opening. In these flowers the petal life span is terminated by wilting rather than abscission. It is concluded that the abscission of turgid petals in D. belladonna was preceded by a number of PCD indicators, whereas no such evidence for PCD was found at the time of P. yedoensis petal abscission. Dehydration of the petal cells, after abscission, was associated with a remarkable nuclear morphology which was also found in younger petals subjected to dehydration. This nuclear morphology has apparently not been described previously, for any organism

    Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in <i>Arabidopsis</i>

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    Programmed cell death (PCD) is used by plants for development and survival to biotic and abiotic stresses. The role of caspases in PCD is well established in animal cells. Over the past 15 years, the importance of caspase-3-like enzymatic activity for plant PCD completion has been widely documented despite the absence of caspase orthologues. In particular, caspase-3 inhibitors blocked nearly all plant PCD tested. Here, we affinity-purified a plant caspase-3-like activity using a biotin-labelled caspase-3 inhibitor and identified Arabidopsis thaliana cathepsin B3 (AtCathB3) by liquid chromatography with tandem mass spectrometry (LC-MS/MS). Consistent with this, recombinant AtCathB3 was found to have caspase-3-like activity and to be inhibited by caspase-3 inhibitors. AtCathepsin B triple-mutant lines showed reduced caspase-3-like enzymatic activity and reduced labelling with activity-based caspase-3 probes. Importantly, AtCathepsin B triple mutants showed a strong reduction in the PCD induced by ultraviolet (UV), oxidative stress (H2O2, methyl viologen) or endoplasmic reticulum stress. Our observations contribute to explain why caspase-3 inhibitors inhibit plant PCD and provide new tools to further plant PCD research. The fact that cathepsin B does regulate PCD in both animal and plant cells suggests that this protease may be part of an ancestral PCD pathway pre-existing the plant/animal divergence that needs further characterisation

    SAM levels, gene expression of SAM synthetase, methionine synthase and ACC oxidase, and ethylene emission from N. suaveolens flowers

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    S′adenosyl-l-methionine (SAM) is a ubiquitous methyl donor and a precursor in the biosynthesis of ethylene, polyamines, biotin, and nicotianamine in plants. Only limited information is available regarding its synthesis (SAM cycle) and its concentrations in plant tissues. The SAM concentrations in flowers of Nicotiana suaveolens were determined during day/night cycles and found to fluctuate rhythmically between 10 and 50 nmol g−1 fresh weight. Troughs of SAM levels were measured in the evening and night, which corresponds to the time when the major floral scent compound, methyl benzoate, is synthesized by a SAM dependent methyltransferase (NsBSMT) and when this enzyme possesses its highest activity. The SAM synthetase (NsSAMS1) and methionine synthase (NsMS1) are enzymes, among others, which are involved in the synthesis and regeneration of SAM. Respective genes were isolated from a N. suaveolens petal cDNA library. Transcript accumulation patterns of both SAM regenerating enzymes matched perfectly those of the bifunctional NsBSMT; maximum mRNA accumulations of NsMS1 and NsSAMS1 were attained in the evening. Ethylene, which is synthesized from SAM, reached only low levels of 1–2 ppbv in N. suaveolens flowers. It is emitted in a burst at the end of the life span of the flowers, which correlates with the increased expression of the 1-aminocyclopropane-1-carboxylate oxidase (NsACO)

    Interaction of plant growth regulators and reactive oxygen species to regulate petal senescence in wallflowers (Erysimum linifolium)

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    Background In many species floral senescence is coordinated by ethylene. Endogenous levels rise, and exogenous application accelerates senescence. Furthermore, floral senescence is often associated with increased reactive oxygen species, and is delayed by exogenously applied cytokinin. However, how these processes are linked remains largely unresolved. Erysimum linifolium (wallflower) provides an excellent model for understanding these interactions due to its easily staged flowers and close taxonomic relationship to Arabidopsis. This has facilitated microarray analysis of gene expression during petal senescence and provided gene markers for following the effects of treatments on different regulatory pathways. Results In detached Erysimum linifolium (wallflower) flowers ethylene production peaks in open flowers. Furthermore senescence is delayed by treatments with the ethylene signalling inhibitor silver thiosulphate, and accelerated with ethylene released by 2-chloroethylphosphonic acid. Both treatments with exogenous cytokinin, or 6-methyl purine (which is an inhibitor of cytokinin oxidase), delay petal senescence. However, treatment with cytokinin also increases ethylene biosynthesis. Despite the similar effects on senescence, transcript abundance of gene markers is affected differentially by the treatments. A significant rise in transcript abundance of WLS73 (a putative aminocyclopropanecarboxylate oxidase) was abolished by cytokinin or 6-methyl purine treatments. In contrast, WFSAG12 transcript (a senescence marker) continued to accumulate significantly, albeit at a reduced rate. Silver thiosulphate suppressed the increase in transcript abundance both of WFSAG12 and WLS73. Activity of reactive oxygen species scavenging enzymes changed during senescence. Treatments that increased cytokinin levels, or inhibited ethylene action, reduced accumulation of hydrogen peroxide. Furthermore, although auxin levels rose with senescence, treatments that delayed early senescence did not affect transcript abundance of WPS46, an auxin-induced gene. Conclusions A model for the interaction between cytokinins, ethylene, reactive oxygen species and auxin in the regulation of floral senescence in wallflowers is proposed. The combined increase in ethylene and reduction in cytokinin triggers the initiation of senescence and these two plant growth regulators directly or indirectly result in increased reactive oxygen species levels. A fall in conjugated auxin and/or the total auxin pool eventually triggers abscission

    Helicobacter pylori regulates iNOS promoter by histone modifications in human gastric epithelial cells. [R. Pero* corresponding author]

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    Inducible nitric oxide synthase (iNOS) expression is altered in gastrointestinal diseases. Helicobacter pylori (Hp) infection may have a critical role in iNOS disregulation. We undertook this study to investigate possible chromatin changes occurring early during iNOS gene activation as a direct consequence of Hp???gastric cells interaction. We show that Hp infection is followed by different expression and chromatin modifications in gastric cells including (1) activation of iNOS gene expression, (2) chromatin changes at iNOS promoter including decreased H3K9 methylation and increased H3 acetylation and H3K4 methylation levels, (3) selective release of methyl-CpG-binding protein 2 from the iNOS promoter. Moreover, we show that Hp-induced activation of iNOS is delayed, but not eliminated, by the treatment with LSD1 inhibitors. Our data suggest a role for specific chromatin-based mechanisms in the control of human iNOS gene expression upon Hp exposure

    The Ustilago maydis Effector Pep1 Suppresses Plant Immunity by Inhibition of Host Peroxidase Activity

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    The corn smut Ustilago maydis establishes a biotrophic interaction with its host plant maize. This interaction requires efficient suppression of plant immune responses, which is attributed to secreted effector proteins. Previously we identified Pep1 (Protein essential during penetration-1) as a secreted effector with an essential role for U. maydis virulence. pep1 deletion mutants induce strong defense responses leading to an early block in pathogenic development of the fungus. Using cytological and functional assays we show that Pep1 functions as an inhibitor of plant peroxidases. At sites of Δpep1 mutant penetrations, H2O2 strongly accumulated in the cell walls, coinciding with a transcriptional induction of the secreted maize peroxidase POX12. Pep1 protein effectively inhibited the peroxidase driven oxidative burst and thereby suppresses the early immune responses of maize. Moreover, Pep1 directly inhibits peroxidases in vitro in a concentration-dependent manner. Using fluorescence complementation assays, we observed a direct interaction of Pep1 and the maize peroxidase POX12 in vivo. Functional relevance of this interaction was demonstrated by partial complementation of the Δpep1 mutant defect by virus induced gene silencing of maize POX12. We conclude that Pep1 acts as a potent suppressor of early plant defenses by inhibition of peroxidase activity. Thus, it represents a novel strategy for establishing a biotrophic interaction

    Expression of two barley proteinase inhibitors in tomato promotes endogenous defensive response and enhances resistance to Tuta absoluta

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    [EN] Background: For as long as 350 million years, plants and insects have coexisted and developed a set of relationships which affect both organisms at different levels. Plants have evolved various morphological and biochemical adaptations to cope with herbivores attacks. However, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) has become the major pest threatening tomato crops worldwide and without the appropriated management it can cause production losses between 80 to 100%. Results: The aim of this study was to investigate the in vivo effect of a serine proteinase inhibitor (BTI-CMe) and a cysteine proteinase inhibitor (Hv-CPI2) from barley on this insect and to examine the effect their expression has on tomato defensive response. We found that larvae fed on the double transgenic plants showed a notable reduction in weight. Moreover, only 56% of the larvae reached the adult stage. The emerged adults showed wings deformities and reduced fertility. We also investigated the effect of proteinase inhibitors ingestion on the insect digestive enzymes. Our results showed a decrease in larval trypsin activity. Transgenes expression had no harmful effect on Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae), a predator of Tuta absoluta, despite transgenic tomato plants attracted the mirid. We also found that barley cystatin expression promoted plant defense by inducing the expression of the tomato endogenous wound inducible Proteinase inhibitor 2 (Pin2) gene, increasing the production of glandular trichomes and altering the emission of volatile organic compounds. Conclusion: Our results demonstrate the usefulness of the co-expression of different proteinase inhibitors for the enhancement of plant resistance to Tuta absoluta.This work was partly supported by grants BIO2013-40747-R and AGL2014-55616-C3 from the Spanish Ministry of Economy and Competitiveness (MINECO)Hamza, R.; Pérez-Hedo, M.; Urbaneja, A.; Rambla Nebot, JL.; Granell Richart, A.; Gaddour, K.; Beltran Porter, JP.... (2018). Expression of two barley proteinase inhibitors in tomato promotes endogenous defensive response and enhances resistance to Tuta absoluta. BMC Plant Biology. 18. https://doi.org/10.1186/s12870-018-1240-6S18Oerke EC. Crop losses to pests. J Agric Sci. 2005;144(01):31.Jouanin L, Bonadé-Bottino M, Girard C, Morrot G, Giband M. Transgenic plants for insect resistance. Plant Sci. 1998;131(1):1–11.Markwick NP, Docherty LC, Phung MM, Lester MT, Murray C, Yao JL, Mitra DS, Cohen D, Beuning LL, Kutty-Amma S, et al. Transgenic tobacco and apple plants expressing biotin-binding proteins are resistant to two cosmopolitan insect pests, potato tuber moth and lightbrown apple moth, respectively. Transgenic Res. 2003;12(6):671–81.Koiwa H, Bressan RA, Hasegawa PM. Regulation of protease inhibitors and plant defense. Trends Plant Sci. 1997;2(10):379–84.Ryan CA. Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol. 1990;28(1):425–49.Abdeen A, Virgos A, Olivella E, Villanueva J, Aviles X, Gabarra R, Prat S. Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Mol Biol. 2005;57(2):189–202.Quilis J, López-García B, Meynard D, Guiderdoni E, San Segundo B. Inducible expression of a fusion gene encoding two proteinase inhibitors leads to insect and pathogen resistance in transgenic rice. Plant Biotechnol J. 2014;12(3):367–77.Smigocki AC, Ivic-Haymes S, Li H, Savic J. Pest protection conferred by a Beta vulgaris serine proteinase inhibitor gene. PLoS One. 2013;8(2):e57303.Mazumdar-Leighton S, Broadway RM. Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochem Mol Biol. 2001;31(6–7):645–57.Oppert B, Morgan TD, Hartzer K, Kramer KJ. Compensatory proteolytic responses to dietary proteinase inhibitors in the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2005;140(1):53–8.Broadway RM. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J Insect Physiol. 1997;43(9):855–74.Zhu-Salzman K, Koiwa H, Salzman R, Shade R, Ahn JE. Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol Biol. 2003;12(2):135–45.Oppert B, Morgan TD, Hartzer K, Lenarcic B, Galesa K, Brzin J, Turk V, Yoza K, Ohtsubo K, Kramer KJ. Effects of proteinase inhibitors on digestive proteinases and growth of the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Comparative biochemistry and physiology Toxicology & pharmacology : CBP. 2003;134(4):481–90.Duan X, Li X, Xue Q, Abo-El-Saad M, Xu D, Wu R. Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nat Biotechnol. 1996;14(4):494–8.Pompermayer P, Lopes AR, Terra WR, Parra JRP, Falco MC, Silva-Filho MC. Effects of soybean proteinase inhibitor on development, survival and reproductive potential of the sugarcane borer, Diatraea saccharalis. Entomologia Experimentalis et Applicata. 2001;99(1):79–85.Alfonso-Rubí J, Ortego F, Castañera P, Carbonero P, Díaz I. Transgenic expression of trypsin inhibitor CMe from barley in indica and japonica rice, confers resistance to the rice weevil Sitophilus oryzae. Transgenic Res. 2003;12(1):23–31.Altpeter F, Diaz I, Mc Auslane H, Gaddour K, Carbonero P, Vasil IK. Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Mol Breed. 1999;5(1):53–63.Martinez M, Cambra I, Carrillo L, Diaz-Mendoza M, Diaz I. Characterization of the entire cystatin gene family in barley and their target cathepsin L-like cysteine-proteases, partners in the hordein mobilization during seed germination. Plant Physiol. 2009;151(3):1531–45.FAOSTAT: Food and Organization of the United Nations, statistics division. 2017.Mueller LA, Lankhorst RK, Tanksley SD, Giovannoni JJ, White R, Vrebalov J, Fei Z, van Eck J, Buels R, Mills AA, et al. A snapshot of the emerging tomato genome sequence. The Plant Genome. 2009;2(1):78–92.Ellul P, Garcia-Sogo B, Pineda B, Rios G, Roig L, Moreno V. The ploidy level of transgenic plants in agrobacterium-mediated transformation of tomato cotyledons (Lycopersicon esculentum L. mill.) is genotype and procedure dependent. Theor Appl Genet. 2003;106(2):231–8.Pino LE, Lombardi-Crestana S, Azevedo MS, Scotton DC, Borgo L, Quecini V, Figueira A, Peres LE. The Rg1 allele as a valuable tool for genetic transformation of the tomato'Micro-Tom'model system. Plant Methods. 2010;6(1):23.Sharma MK, Solanke AU, Jani D, Singh Y, Sharma AK. A simple and efficient agrobacterium-mediated procedure for transformation of tomato. J Biosci. 2009;34(3):423–33.van Eck J, Kirk DD, Walmsley AM. Tomato (Lycopersicum esculentum). Agrobacterium Protocols. 2006:459–74.Dan Y, Yan H, Munyikwa T, Dong J, Zhang Y, Armstrong CL. MicroTom—a high-throughput model transformation system for functional genomics. Plant Cell Rep. 2006;25(5):432–41.Pearce G, Strydom D, Johnson S, Ryan CA. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science. 1991;253(5022):895–9.Farmer EE, Ryan CA. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci. 1990;87(19):7713–6.Bosch M, Wright LP, Gershenzon J, Wasternack C, Hause B, Schaller A, Stintzi A. Jasmonic acid and its precursor 12-oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in tomato. Plant Physiol. 2014;166(1):396–410.Christensen SA, Nemchenko A, Borrego E, Murray I, Sobhy IS, Bosak L, DeBlasio S, Erb M, Robert CA, Vaughn KA. The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. Plant J. 2013;74(1):59–73.Boughton AJ, Hoover K, Felton GW. Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J Chem Ecol. 2005;31(9):2211–6.Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA. The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell. 2004;16(1):126–43.Peiffer M, Tooker JF, Luthe DS, Felton GW. Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol. 2009;184(3):644–56.Bryant J, Green TR, Gurusaddaiah T, Ryan CA. Proteinase inhibitor II from potatoes: isolation and characterization of its protomer components. Biochemistry. 1976;15(16):3418–24.Johnson R, Narvaez J, An G, Ryan C. Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc Natl Acad Sci. 1989;86(24):9871–5.Klopfenstein NB, Allen KK, Avila FJ, Heuchelin SA, Martinez J, Carman RC, Hall RB, Hart ER, McNabb HS. Proteinase inhibitor II gene in transgenic poplar: chemical and biological assays. Biomass Bioenergy. 1997;12(4):299–311.Dicke M, Takabayashi J, Posthumus MA, Schütte C, Krips OE. Plant—Phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues and in responses of predatory mites. Exp Appl Acarol. 1998;22(6):311–33.Turlings T, Loughrin JH, Mccall PJ, Röse U, Lewis WJ, Tumlinson JH. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci. 1995;92(10):4169–74.Levin DA. The role of trichomes in plant defense. Q Rev Biol. 1973;48(1, Part 1):3–15.Traw BM, Dawson TE. Differential induction of trichomes by three herbivores of black mustard. Oecologia. 2002;131(4):526–32.Handley R, Ekbom B, Ågren J. Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana. Ecological Entomology. 2005;30(3):284–92.Valverde P, Fornoni J, NÚÑez-Farfán J. Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. J Evol Biol. 2001;14(3):424–32.Elle E, Hare J. Environmentally induced variation in floral traits affects the mating system in Datura wrightii. Funct Ecol. 2002;16(1):79–88.Agrawal AA. Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology. 2000;81(7):1804–13.Dalin P, Björkman C. Adult beetle grazing induces willow trichome defence against subsequent larval feeding. Oecologia. 2003;134(1):112–8.Campos MR, Biondi A, Adiga A, Guedes RN, Desneux N. From the western Palaearctic region to beyond: Tuta absoluta 10 years after invading Europe. J Pest Sci. 2017:1–10.Desneux N, Wajnberg E, Wyckhuys KA, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Ruescas DC, Tabone E, Frandon J. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci. 2010;83(3):197–215.Urbaneja A, Montón H, Mollá O. Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol. 2009;133(4):292–6.Pérez-Hedo M, Urbaneja A. Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci. 2015;88(1):65–73.Hewitt E. The composition of the nutrient solution. Sand and water culture methods used in the study of plant Nutrition. 1966:187–246.Karimi M, Inzé D, Depicker A. GATEWAY™ vectors for agrobacterium-mediated plant transformation. Trends Plant Sci. 2002;7(5):193–5.Martín-Trillo M, Grandío EG, Serra F, Marcel F, Rodríguez-Buey ML, Schmitz G, Theres K, Bendahmane A, Dopazo H, Cubas P. Role of tomato BRANCHED1-like genes in the control of shoot branching. Plant J. 2011;67(4):701–14.Vargas C. Observations on the bionomics and natural enemies of the tomato moth, Gnorimoschema absoluta (Meyrick)(Lep. Gelechiidae). Idesia. 1970;1:75–110.Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A. A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. BioControl. 2014;59(2):175–83.Abbot C. Solar variation and the weather. Science (New York, NY). 1925;62(1605):307.Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1–2):248–54.Bouagga S, Urbaneja A, Rambla JL, Granell A, Pérez-Hedo M. Orius laevigatus strengthens its role as a biological control agent by inducing plant defenses. J Pest Sci. 2017:1–10.Hilder VA, Gatehouse AM, Sheerman SE, Barker RF, Boulter D. A novel mechanism of insect resistance engineered into tobacco. Nature. 1987;330(6144):160–3.Saikia K, Kalita J, Saikia PK. Biology and life cycle generations of common crow–Euploea core core Cramer (Lepidoptera: Danainae) on Hemidesmus indica host plant. Int J NeBIO. 2010;1(3):28–37.Srinivasan A, Giri AP, Gupta VS. Structural and functional diversities in lepidopteran serine proteases. Cellular & molecular biology letters. 2006;11(1):132.Tamhane VA, Chougule NP, Giri AP, Dixit AR, Sainani MN, Gupta VS. In vivo and in vitro effect of Capsicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases. Biochimica et Biophysica Acta (BBA)-General Subjects. 2005;1722(2):156–67.Telang M, Srinivasan A, Patankar A, Harsulkar A, Joshi V, Damle A, Deshpande V, Sainani M, Ranjekar P, Gupta G. Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry. 2003;63(6):643–52.Damle MS, Giri AP, Sainani MN, Gupta VS. Higher accumulation of proteinase inhibitors in flowers than leaves and fruits as a possible basis for differential feeding preference of Helicoverpa armigera on tomato (Lycopersicon esculentum mill, cv. Dhanashree). Phytochemistry. 2005;66(22):2659–67.De Leo F, Bonadé-Bottino MA, Ceci LR, Gallerani R, Jouanin L. Opposite effects on spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiol. 1998;118(3):997–1004.Rahbé Y, Ferrasson E, Rabesona H, Quillien L. Toxicity to the pea aphid Acyrthosiphon pisum of anti-chymotrypsin isoforms and fragments of Bowman–Birk protease inhibitors from pea seeds. Insect Biochem Mol Biol. 2003;33(3):299–306.Luo M, Ding L-W, Ge Z-J, Wang Z-Y, Hu B-L, Yang X-B, Sun Q-Y, Xu Z-F. The characterization of SaPIN2b, a plant trichome-localized proteinase inhibitor from Solanum americanum. Int J Mol Sci. 2012;13(11):15162–76.Dalin P, Ågren J, Björkman C, Huttunen P, Kärkkäinen K. Leaf trichome formation and plant resistance to herbivory. In: Dordrecht SA, editor. Induced plant resistance to herbivory. Netherlands: Springer; 2008. p. 89–105.Gonzáles WL, Negritto MA, Suárez LH, Gianoli E. Induction of glandular and non-glandular trichomes by damage in leaves of Madia sativa under contrasting water regimes. Acta Oecol. 2008;33(1):128–32.Luo M, Wang Z, Li H, Xia K-F, Cai Y, Xu Z-F. Overexpression of a weed (Solanum americanum) proteinase inhibitor in transgenic tobacco results in increased glandular trichome density and enhanced resistance to Helicoverpa armigera and Spodoptera litura. Int J Mol Sci. 2009;10(4):1896–910.Björkman C, Dalin P, Ahrné K. Leaf trichome responses to herbivory in willows: induction, relaxation and costs. New Phytol. 2008;179(1):176–84.Duffey S. Plant glandular trichomes: their partial role in defence against insects. Insects and the plant surface. London: Edward Arnold; 1986. p. 151–72.James DG. Further field evaluation of synthetic herbivore-induced plan volatiles as attractants for beneficial insects. J Chem Ecol. 2005;31(3):481–95.Naselli M, Zappalà L, Gugliuzzo A, Garzia GT, Biondi A, Rapisarda C, Cincotta F, Condurso C, Verzera A, Siscaro G. Olfactory response of the zoophytophagous mirid Nesidiocoris tenuis to tomato and alternative host plants. Arthropod Plant Interact. 2017;11(2):121–31.Tholl D. Biosynthesis and biological functions of terpenoids in plants. Advances in Biochemical Engineering and Biotechnology. 2015;148:63-106.Lange BM, Rujan T, Martin W, Croteau R. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci. 2000;97(24):13172–7.Dudareva N, Klempien A, Muhlemann JK, Kaplan I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol. 2013;198(1):16–32.Razal RA, Ellis S, Singh S, Lewis NG, Towers GHN. Nitrogen recycling in phenylpropanoid metabolism. Phytochemistry. 1996;41(1):31–5.Effmert U, Große J, Röse US, Ehrig F, Kägi R, Piechulla B. Volatile composition, emission pattern, and localization of floral scent emission in Mirabilis jalapa (Nyctaginaceae). Am J Bot. 2005;92(1):2–12.Guterman I, Masci T, Chen X, Negre F, Pichersky E, Dudareva N, Weiss D, Vainstein A. Generation of phenylpropanoid pathway-derived volatiles in transgenic plants: rose alcohol acetyltransferase produces phenylethyl acetate and benzyl acetate in petunia flowers. Plant Mol Biol. 2006;60(4):555–63.Vogel JT, Tan B-C, McCarty DR, Klee HJ. The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. J Biol Chem. 2008;283(17):11364–73.Colquhoun TA, Kim JY, Wedde AE, Levin LA, Schmitt KC, Schuurink RC, Clark DG. PhMYB4 fine-tunes the floral volatile signature of petunia×hybrida through PhC4H. J Exp Bot. 2011;62(3):1133–43.Kolosova N, Gorenstein N, Kish CM, Dudareva N. Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell. 2001;13(10):2333–47.Maeda H, Shasany AK, Schnepp J, Orlova I, Taguchi G, Cooper BR, Rhodes D, Pichersky E, Dudareva N. RNAi suppression of arogenate dehydratase1 reveals that phenylalanine is synthesized predominantly via the arogenate pathway in petunia petals. Plant Cell. 2010;22(3):832–49.Lerdau M, Gray D. Ecology and evolution of light-dependent and light-independent phytogenic volatile organic carbon. New Phytol. 2003;157(2):199–211.Martin DM, Gershenzon J, Bohlmann J. Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol. 2003;132(3):1586–99.van Doorn WG, Woltering EJ. Physiology and molecular biology of petal senescence. J Exp Bot. 2008;59(3):453–80
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