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Biological roles of monoterpene volatiles derived from rough lemon (Citrus jambhiri Lush) in citrus defense

  • Fungal Diseases
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Abstract

Volatile compounds of plants, including monoterpenes, are a possible source of signal molecules that induce defense systems to protect plants from tissue damage. Volatile compounds from rough lemon leaves were trapped by solid-phase microextraction fibers in sealed vials, and subsequent gas chromatography–mass spectrometry and gas chromatography analyses identified the profile of the major components, mainly various monoterpenes. Among several monoterpenes examined, citral, citronellal, and linalool significantly inhibited the spore germination and hyphal growth of Alternaria alternata. The effect of linalool was fungistatic, while the effects of citral and citronellal were partially fungicidal. Wounding of rough lemon leaves induced a significant increase in release of monoterpenes. The release of linalool was the most abundant and was 14.5 times that of unwounded rough lemon leaves. Unlike the wounding treatment, microbe attack did not significantly change monoterpene releases, and there was statistically no difference found in the peak areas from microbe-treated and untreated leaves. Linalool, limonene, and β-pinene also had insect-repellant effects on wild-type Drosophila melanogaster. Expression patterns of defense-related genes in rough lemon and rice significantly changed after treatment with vapors of monoterpene volatiles. Taking these results together, monoterpene volatiles are likely to play roles in the defense of rough lemon against microbe and insect pathogens.

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References

  • Akimitsu K, Kohmoto K, Otani H, Nishimura S (1989) Host–specific effect of toxin from the rough lemon pathotype of Alternaria alternata on mitochondria. Plant Physiol 89:925–931

    Article  PubMed  CAS  Google Scholar 

  • Akimitsu K, Tsukuda S, Suzuki N, Ichii M, Tajima S (2005) An elicitor effect of d-Psicose for induction of plant defense gene transcriptions. In: Tajima S, Asada Y (eds) Rare sugars: creating a novel bio-world with rare sugars. International Society of Rare Sugars, Kagawa, pp 163–168

    Google Scholar 

  • Alpendurada MF (2000) Solid-phase microextraction: a promising technique for sample preparation in environmental analysis. J Chromatogr A 889:3–14

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515

    Article  PubMed  CAS  Google Scholar 

  • Bickers D, Calow P, Greim H, Hanifin JM, Rogers AE, Saurat JH, Sipes IG, Smith RL, Tagami H (2003) A toxicologic and dermatologic assessment of linalool and related esters when used as fragrance ingredients. Food Chem Toxicol 41:919–942

    Article  PubMed  CAS  Google Scholar 

  • Birkett MA, Campbell CA, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Pettersson J, Pickett JA, Poppy GM, Pow EM, Pye BJ, Smart LE, Wadhams GH, Wadhams LJ, Woodcock CM (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc Natl Acad Sci USA 97:9329–9334

    Article  PubMed  CAS  Google Scholar 

  • Blee E (1998) Phytooxylipins and plant defense reactions. Prog Lipid Res 37:33–72

    Article  PubMed  CAS  Google Scholar 

  • Bolter CJ, Dicke M, Van Loon JJ, Visser JH, Posthumus MA (1997) Attraction of Colorado potato beetle to herbivore-damaged plants during herbivory and after its termination. J Chem Ecol 23:1003–1023

    Article  CAS  Google Scholar 

  • Choi HS, Sawamura M (2001) Volatile flavor components of ripe and overripe ki-mikans (Citrus flaviculpus Hort. ex Tanaka) in comparison with Hyuganatsu (Citrus tamurana Hort. ex Tanaka). Biosci Biotechnol Biochem 65:48–55

    Article  PubMed  CAS  Google Scholar 

  • Cox SD, Gustafson JE, Mann CM, Markham JL, Liew YC, Hartland RP, Bell HC, Warmington JR, Wyllie SG (1998) Tea tree oil causes K+ leakage and inhibits respiration in Escherichia coli. Lett Appl Microbiol 26:355–358

    Article  PubMed  CAS  Google Scholar 

  • De Moraes CM, Lewis SP, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • Debi RB, Taketa S, Ichii M (2005) Cytokinin inhibits lateral root initiation but stimulates lateral root elongation in rice (Oryza sativa). J Plant Physiol 162:507–515

    Article  CAS  Google Scholar 

  • Dorman HJ, Deans SG (2000) Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J Appl Microbiol 88:308–316

    Article  PubMed  CAS  Google Scholar 

  • Gancel AL, Ollitrault P, Froelicher Y, Tomi F, Jacquemond C, Luro F, Brillouet JM (2005) Leaf volatile compounds of six citrus somatic allotetraploid hybrids originating from various combinations of lime, lemon, citron, sweet orange, and grapefruit. J Agric Food Chem 53:2224–2230

    Article  PubMed  CAS  Google Scholar 

  • Gomi K, Ito N, Yamamato H, Akimitsu K (2002a) Characterization and functional analysis of class I and class II acidic chitinase cDNA from rough lemon. J Gen Plant Pathol 68:191–199

    Article  CAS  Google Scholar 

  • Gomi K, Yamamato H, Akimitsu K (2002b) Characterization of a lipoxygenase gene in rough lemon induced by Alternaria alternata. J Gen Plant Pathol 68:191–199

    Article  CAS  Google Scholar 

  • Gomi K, Yamamato H, Akimitsu K (2003a) Epoxide hydrolase: a mRNA induced by the fungal pathogen Alternaria alternata on rough lemon (Citrus jambhiri Lush). Plant Mol Biol 53:189–199

    Article  PubMed  CAS  Google Scholar 

  • Gomi K, Yamasaki Y, Ymamoto H, Akimitsu K (2003b) Characterization of a hydroperoxide lyase gene and effect of C6-volatiles on expression of genes of the oxylipin metabolism in citrus. J Plant Physiol 160:1219–1231

    Article  PubMed  CAS  Google Scholar 

  • Griffin SG, Wyllie SG, Markham JL, Leach DN (1999) The role of structure and molecular properties of terpenoids in determining their antimicrobial activity. Flavour Fragr J 14:322–332

    Article  CAS  Google Scholar 

  • Hamilton-Kemp TR, McCracken CT Jr, Loughrin JH, Andersen RA, Hildebrand DF (1992) Effects of some natural volatile compounds on the pathogenic fungi Alternaria alternata and Botrytis cinerea. J Chem Ecol 18:1083–1091

    Article  CAS  Google Scholar 

  • Hatanaka A, Kajiwara T, Sekiya J (1987) Biosynthetic pathway for C6-aldehydes formation from linolenic acid in green leaves. Chem Phys Lipids 44:341–361

    Article  CAS  Google Scholar 

  • Kim IS, Grosch W (1981) Partial purification and properties of a hydroperoxide lyase from fruits of pear. J Agric Food Chem 29:1220–1225

    Article  CAS  Google Scholar 

  • Kohmoto K, Akimitsu K, Otani H (1991) Correlation of resistance and susceptibility of citrus to Alternaria alternata with sensitivity to host-specific toxins. Phytopathology 81:719–722

    Google Scholar 

  • Kohmoto K, Itoh Y, Shimomura N, Kondoh Y, Otani H, Kodama M, Nishimura S, Nakatsuka S (1993) Isolation and biological activities of two host-specific toxins from the tangerine pathotype of Alternaria alternata. Phytopathology 83:495–502

    Article  CAS  Google Scholar 

  • Kurita N, Miyaji M, Kurane R, Takahara Y, Ichimura K (1979) Antifungal activity and molecular orbital energies of aldehyde compounds from oils of higher plants. Agri Biol Chem 43:2365–2371

    CAS  Google Scholar 

  • Kurita N, Miyaji M, Kurane R, Takahara Y, Ichimura K (1981) Antifungal activity of components of essential oils. Agri Biol Chem 45:945–952

    CAS  Google Scholar 

  • Lewinsohn E, Gijzen M, Savage TJ, Croteau R (1991) Defense mechanisms of conifers: relationship of monoterpene cyclase activity to anatomical specialization and oleoresin monoterpene content. Plant Physiol 96:38–43

    PubMed  CAS  Google Scholar 

  • Lota M, de Rocca Serra D, Tomi F, Casanova J (2001) Chemical variability of peel and leaf essential oils of 15 species of mandarins. Biochem Syst Ecol 29:77–104

    Article  PubMed  CAS  Google Scholar 

  • Lota ML, de Rocca Serra D, Tomi F, Jacquemond C, Casanova J (2002) Volatile components of peel and leaf oils of lemon and lime species. J Agric Food Chem 50:796–805

    Article  PubMed  CAS  Google Scholar 

  • Lou Y, Baldwin IT (2003) Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proc Natl Acad Sci USA 100 (Suppl 2):14581–14586

    Article  PubMed  CAS  Google Scholar 

  • Lücker J, Schwab W, van Hautum B, Blaas J, van der Plas LH, Bouwmeester HJ, Verhoeven HA (2004) Increased and altered fragrance of tobacco plants after metabolic engineering using three monoterpene synthases from lemon. Plant Physiol 134:510–519

    Article  PubMed  CAS  Google Scholar 

  • Luo M, Jiang LK, Huang YX, Xiao M, Li B, Zou GL (2004) Effects of citral on Aspergillus flavus spores by quasi-elastic light scattering and multiplex microanalysis techniques. Acta Biochim Biophys Sin (Shanghai) 36:277–283

    Article  CAS  Google Scholar 

  • Mur LA, Kenton P, Draper J (1997) Something in the air: volatile signals in plant defence. Trends Microbiol 5:297–300

    Article  PubMed  CAS  Google Scholar 

  • Nakashita H, Yoshioka K, Takayama M, Kuga R, Midoh N, Usami R, Horikoshi K, Yoneyama K, Yamaguchi I (2001) Characterization of PBZ1, a probenazole-inducible gene, in suspension-cultured rice cells. Biosci Biotechnol Biochem 65:205–208

    Article  PubMed  CAS  Google Scholar 

  • Nishizawa Y, Kawakami A, Hibi T, He DY, Shibuya N, Minami E (1999a) Regulation of the chitinase gene expression in suspension-cultured rice cells by N-acetylchitooligosaccharides: differences in the signal transduction pathways leading to the activation of elicitor-responsive genes. Plant Mol Biol 39:907–914

    Article  PubMed  CAS  Google Scholar 

  • Nishizawa Y, Nishio Z, Nakazono K, Soma M, Nakajima E, Ugaki M, Hibi T (1999b) Enhanced resistance to blast (Magnaporthe grisea) in transgenic Japonica rice by constitutive expression of rice chitinase. Theor Appl Genet 99:383–390

    Article  CAS  Google Scholar 

  • Peana AT, Marzocco S, Popolo A, Pinto A (2006a) (−)-Linalool inhibits in vitro NO formation: probable involvement in the antinociceptive activity of this monoterpene compound. Life Sci 78:719–723

    Article  PubMed  CAS  Google Scholar 

  • Peana AT, Rubattu P, Piga GG, Fumagalli S, Boatto G, Pippia P, De Montis MG (2006b) Involvement of adenosine A1 and A2A receptors in (−)-linalool-induced antinociception. Life Sci 78:2471–2474

    Article  PubMed  CAS  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    Article  PubMed  CAS  Google Scholar 

  • Sawamura M, Thi Minh Tu N, Onishi Y, Ogawa E, Choi HS (2004) Characteristic odor components of Citrus reticulata Blanco (ponkan) cold-pressed oil. Biosci Biotechnol Biochem 68:1690–1697

    Article  PubMed  CAS  Google Scholar 

  • Shiojiri K, Takabayashi J, Yano S, Takafuji A (2000) Flight response of parasitoids toward plant–herbivore complexes: a comparative study of two parasitoid–herbivore systems on cabbage plants. Appl Entomol Zool 35:87–92

    Article  Google Scholar 

  • Stelinski LL, Miller JR, Ressa NE, Gut LJ (2003) Increased EAG responses of tortricid moths after prolonged exposure to plant volatiles: evidence for octopamine-mediated sensitization. J Insect Physiol 49:845–856

    Article  PubMed  CAS  Google Scholar 

  • Takabayashi J, Dicke M, Posthumus MA (1994) Volatile herbivore-induced terpenoids in plant–mite interactions: variation caused by biotic and abiotic factors. J Chem Ecol 20:1329–1354

    Article  CAS  Google Scholar 

  • Thomson WW, Platt-Aloia KA, Endress AG (1976) Ultrastructure of oil gland development in the leaf of Citrus sinensis. L Bot Gaz 137:330–340

    Article  Google Scholar 

  • Tsukuda S, Gomi K, Yamamoto H, Akimitsu K (2006) Characterization of cDNAs encoding two distinct miraculin-like proteins and stress-related modulation of the corresponding mRNAs in Citrus jambhiri lush. Plant Mol Biol 60:125–136

    Article  PubMed  CAS  Google Scholar 

  • Weiss EA (1997) Essential oil crops. CAB International, Wallingford

    Google Scholar 

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Acknowledgments

We gratefully acknowledge Dr. H. Tamura, Kagawa University, for various suggestions and guidance in GC and GC–MS analyses. Young trees and seeds of rough lemon (Citrus jambhiri Lush) were provided by Dr. H. Siotani, National Institute of Fruit Tree Science, Kuchinotsu Citrus Research Station, Japan; A. alternata isolate O-94 was provided by the Laboratory of Plant Pathology, Tottori University. This study was supported in part by grants for priority area (A) from the Ministry of Education, Culture, Sports, Science and Technology of Japan; the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN) and Precursory Research for Embryonic Science and Technology, Japan Science and Technology Corporation.

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Authors and Affiliations

  1. Laboratory of Plant Pathology, United Graduate School and Faculty of Agriculture, Kagawa University, Miki, Kagawa, 761-0795, Japan

    Yumiko Yamasaki, Hiroyuki Yamamoto & Kazuya Akimitsu

  2. Institute of Biological Process Research, Akatsuka Orchid Co. Ltd, Tsu, Mie, 514-2293, Japan

    Hitoshi Kunoh

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  1. Yumiko Yamasaki
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  2. Hitoshi Kunoh
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  4. Kazuya Akimitsu
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Correspondence to Kazuya Akimitsu.

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Yamasaki, Y., Kunoh, H., Yamamoto, H. et al. Biological roles of monoterpene volatiles derived from rough lemon (Citrus jambhiri Lush) in citrus defense. J Gen Plant Pathol 73, 168–179 (2007). https://doi.org/10.1007/s10327-007-0013-0

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