Common gas phase molecules from fungi affect seed germination and plant health in Arabidopsis thaliana
© Hung et al.; licensee Springer 2014
Received: 21 May 2014
Accepted: 5 June 2014
Published: 15 July 2014
Fungal volatile organic compounds (VOCs) play important ecophysiological roles in mediating inter-kingdom signaling with arthropods but less is known about their interactions with plants. In this study, Arabidopsis thaliana was used as a model in order to test the physiological effects of 23 common vapor-phase fungal VOCs that included alcohols, aldehydes, ketones, and other chemical classes. After exposure to a shared atmosphere with the 23 individual VOCs for 72 hrs, seeds were assayed for rate of germination and seedling formation; vegetative plants were assayed for fresh weight and chlorophyll concentration. All but five of the VOCs tested (1-decene, 2-n-heptylfuran, nonanal, geosmin and -limonene) had a significant effect in inhibiting either germination, seedling formation or both. Seedling formation was entirely inhibited by exposure to 1-octen-3-one, 2-ethylhexanal, 3-methylbutanal, and butanal. As assayed by a combination of fresh weight and chlorophyll concentration, 2-ethylhexanal had a negative impact on two-week-old vegetative plants. Three other compounds (1-octen-3-ol, 2-ethylhexanal, and 2-heptylfuran) decreased fresh weight alone. Most of the VOCs tested did not change the fresh weight or chlorophyll concentration of vegetative plants. In summary, when tested as single compounds, fungal VOCs affected A. thaliana in positive, negative or neutral ways.
KeywordsVolatile organic compound Arabidopsis thaliana Fungi Seed germination Chlorophyll concentration Gas chromatography Mass spectroscopy
Volatiles organic compounds (VOCs) are low molecular mass compounds with high vapor pressure and low to medium water solubility that exist in the gaseous state at room temperature (Herrmann ). Approximately 250 VOCs have been identified from fungi (Chiron and Michelot ) as the products of both primary and secondary metabolism (Turner and Aldridge ; Korpi et al. ). These gas phase molecules are emitted in complex mixtures that vary quantitatively and qualitatively depending not only on the age and genetic profiles of the producing species but also on extrinsic variables such as substrate, temperature, moisture level and pH (Sunesson et al. ; Claeson et al. ; Matysik et al. ). Fungal volatiles have distinctive odorant properties and they have been studied extensively for their positive and negative sensory properties. They impart unique aromas and flavors to mold-ripened cheeses, Japanese koji and other mold-fermented food products (Steinkraus ; Kinderlerer ), and are responsible for the bouquet of gourmet mushrooms such as boletes, chanterelles and truffles (Cho et al. ; Fraatz and Zorn ). On the negative side, when foods are contaminated by molds, they produce off flavors. VOCs have been used as an indirect indicator of fungal spoilage in agricultural products (Borjesson et al. ; Jelen and Wasowicz ; Schnürer et al. ) and of mold contamination in water-damaged buildings (Kuske et al. ; Sahlberg et al. ). Finally, because VOCs can diffuse through the atmosphere and the soil, they are well adapted for signaling between species that share a common ecological niche. Both bacterial and fungal VOCs play competitive roles in chemical interactions between microorganisms (Beattie and Torrey ; Morath et al. ). Many plant and microbial volatile molecules function as semiochemicals, otherwise known as “infochemicals”, and there is a large literature on the ability of fungal VOCs to mediate arthropod behavior, where they have properties as synomones, allomones, and kairomones (Rohlfs et al. ; Mburu et al. ; Davis et al. ). The fungal VOC commonly called “mushroom alcohol” (1-octen-3-ol) is responsible for much of the musty odor associated with mold contamination and is an important insect semiochemical. It attracts many insect species, including the malaria mosquito (Takken and Knols ; Thakeow et al. ).
In contrast, the interactions between fungal VOCs and plants have not received much scientific attention (Bitas et al. ). Based on the observation that there is very little vegetation in areas known to have truffles (subterranean gourmet fungi), it has been hypothesized that these fungi may have the ability to suppress plant growth through their volatiles (Splivallo et al. ). Kishimoto et al. () have shown that 1-octen-3-ol enhances resistance of mature plants of Arabidopsis thaliana to Botrytis cinerea and activates some of the same defense genes turned on by ethylene and jasmonic acid signaling, important plant hormones involved in plant defense.
We hypothesized that we could distinguish between bioactive and inactive fungal vapors by using chemical standards of individual VOCs and then exposing plants to controlled concentrations in a model habitat. We selected A. thaliana as our test species due to the many benefits associated with the use of a well recognized model system including but not limited to: small size, short life cycle, genetic tractability, and comprehensively researched background. Preliminary studies have also shown that tomato plants exposed to VOCs are affected in a similar fashion to A. thaliana exposed to the same VOCs indicating that A. thaliana is a good model organism for study. Similarly, the effects of fungal VOCs on plant development have been demonstrated in several plants in Brassicaceae family including radish, cabbage, rape, and broccoli (Ogura et al. ). The aim of our study was to evaluate the effect of individual fungal VOCs on seed germination, vegetative plant growth and chlorophyll concentration in a controlled environment. In this report, our specific objectives have been to create standardized model exposure habitats in order to compare the possible stimulatory and inhibitory effects of fungal VOCs from different chemical classes (e.g., alcohols, aldehydes, ketones, and so forth) and to conduct exposure studies using A. thaliana seeds and two-week-old vegetative plants.
Materials and methods
Plant material and seed preparation
All volatile exposure tests were done with Arabidopsis thaliana ecotype Columbia 7. Surface-sterilization of seeds and seedling formation studies were conducted as described previously with slight modifications (Hung et al. ). Surface sterilized seeds were sown on Murashige and Skoog (MS) media with vitamins, 3% sucrose, and 0.3% Gellan Gum Powder (G 434 PhytoTechnology Laboratories, Shawnee Mission, KS). In germination-seedling formation studies, seeds were sown on Petri dishes (20 seeds per plate) with 20 ml MS media and placed at 4°C in the dark for three days to stratify the seeds. Seeds used to grow plants for exposure assays of two–week old plants were sown individually in test tubes with 10 ml of MS, covered with plant tissue culture caps and then stratified as described above. After three days, the stratified seeds in their individual test tubes were placed in a growth chamber at 21°C ± 2°C with a 16 hour photoperiod for two weeks prior to exposure to VOCs.
Chemicals and exposure conditions
Authentic standards of these high purity chemicals were purchased in liquid form from Sigma-Aldrich (St. Louis, Missouri). The criteria for the selection of these compounds were: 1) the volatiles should represent different chemical classes, 2) they had been isolated from a range of fungal species including both mushrooms and molds, and 3) that they included several VOCs commonly found in soils.
The germination and vegetative exposure to VOCs were determined using the methods described previously (Hung et al. ; Lee et al. ). Seeds (in Petri plates) or two-week-old plants (in individual test tubes) were exposed in one liter culture vessels (see Additional file 1). All tests were done at a low concentration similar to the concentration of VOCs analyzed previously: one part per million (1 ppm = 1 μl/l). The desired concentration of 1 ppm in the test container was obtained by depositing a drop of the chemical standard (VOC) in liquid form onto the inside of the glass vessel. The compounds, due to their chemical properties will quickly volatilize into the gas phase in the test conditions. Before sealing the lids, a 10 × 10 cm piece of Dura Seal Cling Sealing Film (Diversified Biotech) was placed over the top of each culture vessel so as to prevent VOC leakage through the polypropylene closure. The culture vessels containing either seeds in Petri plates or two-week-old plants in test tubes were arranged randomly in the growth chamber and then placed on a one inch throw rotator at 40 rpm in order to volatilize and evenly distribute the compounds. The control plants were placed in identical conditions without any VOCs.
Scoring germination stages
The seeds were exposed to the individual VOCs for 72 hours and then examined under a binocular microscope where they were scored into three categories: no germination, germination (emergence of the radical [embryonic root]), and seedling formation (presence of the radicle, the hypocotyls and the cotyledons) (see Additional file 2). Seeds scored as “no germination” included seeds with a ruptured testa (seed coat) but without the presence of the radicle.
Plant mass and chlorophyll concentration
After exposure to the vapors of the individual VOCs, plants were removed from the test conditions, the shoot and leaves were cut away from the roots, and fresh weight of the shoots and leaves was obtained. The chlorophyll was extracted using the method of Jing et al. () with some modifications. The plants were soaked overnight in 80% acetone at 4˚C in darkness prior to obtaining photometric readings at 663 and 645 nm with a spectrophotometer (DU800, Beckman Coulter, Brea, CA). Total chlorophyll = 20.2 (A645) + 8.02 (A663)(V/1,000 * w) where V = total volume of the sample, w = weight of the sample, A663 = absorbance at 663 nm, A645 = absorbance at 645 nm (Palta ). Each solvent extract contained one plant per treatment.
The data were analyzed and plotted using Excel software (Microsoft, Redmond, WA) and SigmaPlot (SPSS Science Inc., IL). To test the significance of the exposure studies, one-way analysis of variance (ANOVA) and Student’s t-tests were performed with the aggregated data. The Student’s t-tests determine if there are significant differences between two sets of data: the control and VOC exposed plants. For germination exposures, two replicate plates with 20 seeds per plate were tested for each compound, with two independent experiments, for a total of 80 seeds. For vegetative plant exposure, four plants were placed in the exposure vessel and three jars were used for each experiment. There were three independent experiments for each compound, for a total of 36 plants.
Seedling formation tests
Vegetative plants tests
In Figure 3, we have expressed the chlorophyll concentration data as mg/gm of fresh weight of shoots and leaves. Five compounds (−2-methyl-1-butanol, 1-octen-3-ol, dec-1-ene, heptan-2-one, and isothiocyanatocyclohexane) yielded statistically significant increases in chlorophyll concentration showing, respectively, 0.02 mg/g, 0.2 mg/g, 0.18 mg/g, 0.02 mg/g, and 0.4 mg/g greater amounts than controls. Three compounds, geosmin, 2-ethylhexanal, and 1-octen-3-one caused a statistically significant decrease in chlorophyll concentration of, respectively, 0.15 mg/g, 0.35 mg/g, and 0.42 mg/g less than controls. While geosmin did not adversely affect fresh weight, it did cause a significant decrease in chlorophyll concentration as indicated above. The compound 2-ethyl-hexanal decreased both fresh weight and chlorophyll concentration. The nonracemic form of −2-methyl-1-butanol showed a small but significantly different increase in both parameters.
In conclusion, all but five of the VOCs tested had a significant effect in inhibiting either germination, seedling formation or both. Three of the compounds (2-ethyl-hexanal, 1-octen-3-one, and 3-methylbutanal) showed more than 50% inhibition of seed germination, while 12 of the compounds (2-methylpropan-1-ol, 2-methylpropanal, heptan-2-one, octan-2-one, isothiocyanatocyclohexane, pentan-2-one, octan-3-ol, 1-octen-3-ol, 2-ethylhexanal, 1-octen-3-one, 3-methylbutanal, and butanal) were associated with more than a 50% retardation in seedling formation. Butanal was unusual in that 83% of seeds germinated (i.e. formed a radicle) but none of these germinated seeds progressed to seedling formation. In general, the most bioactive of the VOCs we tested were aldehydes and ketones. The single, most inhibitory VOC against germination and seedling formation was oct-1-en-3-one, an eight carbon ketone that has been isolated from both molds and mushrooms (Jelen and Wasowicz ). Nevertheless, in all cases, VOC exposed seeds were able to resume germination and progress to seedling stage when removed from the shared atmosphere with the VOC. We conclude that the fungal VOCs we tested have a phytostatic (inhibitory), not a phytocidal (lethal) effect on seeds.
In order to study the influence of individual fungal VOCs on plant health, we used A. thaliana as our test organism and developed standardized protocols for exposing seeds and young vegetative plants. We investigated a representative sample of common fungal VOCs encompassing seven alcohols, two alkenes, five aldehydes, four ketones, and a single representative isothiocyanate, carboxylic acid, and furan. In addition, we tested both isomers of the terpene 1-methyl-4-(1-methyetenyl)-cyclohexene, commonly known as limonene. We used a 72 hour exposure period, and exposed either seeds or young vegetative plants to 1 ppm of chemical standards of the 23 fungal VOCs in a contained chamber.
Seed germination assays with lettuce, cucumber and other economically important species have been widely employed as low-cost, ethically acceptable toxicity tests to screen for dangerous levels of industrial contamination in water and soils (Banks and Schultz ; Wang et al. ). Almost all of these assay studies have involved aqueous phase compounds, although there have been a few scattered reports describing inhibitory effect of plant volatiles on the germination of seeds from crop and weed species (Holm ; Bradow and Connick ). The physiological basis for this inhibitory action has not been elucidated. A. thaliana, though not agriculturally important, offers a number of experimental advantages for studying basic aspects of plant biology, including seed germination, because of its many genetic resources (Koornneef et al. ). Our development of an A. thaliana exposure system for studying VOC effects under controlled conditions offers the promise of being able to use this species to dissect the germination inhibition response at the molecular level.
In contrast to seed germination studies, which all report inhibition of germination by VOCs (Holm ; French et al. ; Bradow and Connick ). To date, published studies of the effects of VOCs on vegetative plants report VOC--associated growth stimulation by mixtures of VOCs emitted by growing bacteria or fungi (Ryu et al. ; Minerdi et al. ; Hung et al. ; Paul and Park ). Many soil dwelling microbes emit VOCs that mediate various chemical “conversations” between the rhizosphere and plants (Wenke et al. , ). For example, plant growth promoting rhizobacteria (PGPR) produce mixtures of VOCs that enhance growth in a wide variety of species (Farag et al. ; Vespermann et al. ; Lugtenberg and Kamilova ). In some cases, microbial VOCs induce systemic resistance (Van Loon et al. ; Ryu et al. ) or inhibit the growth of plant pathogens (Minerdi et al. , ). Volatiles of Cladosporium cladosporioides enhance growth of tobacco plants (Paul and Park ) and our laboratory has shown that vegetative plants of A. thaliana seedlings grown in a shared atmosphere with volatiles emitted by living cultures of the biocontrol fungus Trichoderma viride, displayed increased size and vigor (Hung et al. ). Fungal VOCs may contribute to the ability of certain species to outcompete neighboring plants. For example, the VOCs produced by Muscodor yucantanensis were toxic to the roots, and inhibited seed germination, of amaranth, tomato and barnyard grass (Macias-Rubalcava et al.). In all of these cases, the growth-enhancing effects were mediated by mixtures of naturally emitted VOCs that change with both growth phase and extrinsic environmental parameters.
In our studies, we used a controlled system and exposed plants to low concentrations of individual VOCs. In this controlled habitat, the VOCs tested either had neutral or negative effects on vegetative plant growth, suggesting that the known growth enhancing effects of bacterial and fungal VOCs maybe by synergistic mixtures working in concert. A parallel example is provided by the antibiotic effects of volatiles produced by Muscodor albus. This species produces a mixture of VOCs that inhibit and kill a wide range of plant pathogenic fungi and bacteria (Strobel et al. ). Nevertheless, when Muscodor VOCs were tested individually, the inhibitory effects were not observed, suggesting that the antifungal activity required a suite of VOCs working in concert (Strobel et al. ).
It should be recognized that studies on transkingdom signalling mediated by fungal VOCs are technically difficult to conduct. Biogenic VOCs exhibit enormous heterogeneity chemically, spatially, and temporally; are found in low concentrations; and by definition have innate evaporative properties that make it difficult to investigate their impact on plant growth and development in natural settings. Our exploratory research shows that by using controlled concentrations of pure synthetic compounds in model habitats, individual VOCs can be studied one by one, thereby isolating their distinct growth-promoting, growth-inhibiting and other physiological effects. The genetic and genomic resources available for A. thaliana make this organism well suited for future research on the mechanistic basis of VOC mediated interactions and for analysis of the consequent biological responses. In summary, the study of gas phase fungal metabolites offers many interesting prospects for enlarging our understanding of the way in which fungi interact with plants in nature and may have potential for commercial application of VOCs in greenhouse agriculture.
We thank Barbra Zilinskas, Chee-kok Chin, and Prakash Masurekar for their guidance and perspective. We also thank Elvira de Lange for helpful comments on an earlier draft of the manuscript. This research was supported by funds from Rutgers, The State University of New Jersey and National Science Foundation Graduate Research Fellowship under Grant No. 0937373 to SL.
- Banks MK, Schultz KE: Comparison of plants for germination toxicity tests in petroleum-contaminated soils. Water Air Soil Pollut 2005, 167: 211–219.View ArticleGoogle Scholar
- Beattie SE, Torrey GS: Toxicity of methanethiol produced by Brevibacterium linens toward Penicillium expansum . J Agr Food Sci 1986, 34: 102–104.View ArticleGoogle Scholar
- Bitas V, Kim H-S, Bennett J, Kang S: Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol Plant Microbe Interact 2013, 26: 835–843.View ArticlePubMedGoogle Scholar
- Borjesson T, Stollman U, Schnurer J: Volatile metabolites produced by six fungal species compared with other indicators of fungal growth on stored cereals. Appl Environ Microbiol 1992, 58: 2599–2605.PubMed CentralPubMedGoogle Scholar
- Bradow JM, Connick WJ: Volatile seed germination inhibitors from plant residues. J Chem Ecol 1990, 16: 645–666.View ArticlePubMedGoogle Scholar
- Chiron N, Michelot D: Odeurs de champignons: chimie et rôle dans les interactions biotiques- une revue. Cryptogam Mycol 2005, 26: 299–364.Google Scholar
- Cho IH, Namgung H-J, Choi H-K, Kim YS: Volatiles and key odorants in the pileus and stipe of pine-mushroom ( Tricholoma matsutake Sing). Food Chem 2008, 106: 71–76.View ArticleGoogle Scholar
- Claeson AS, Levin JO, Blomquist G, Sunesson AL: Volatile metabolites from microorganisms grown on humid building materials and synthetic media. J Environ Monit 2002, 4: 667–672.View ArticlePubMedGoogle Scholar
- Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK: Microbial volatile emissions as insect semiochemicals. J Chem Ecol 2013, 39: 840–859.View ArticlePubMedGoogle Scholar
- Farag MA, Ryu CM, Sumner LW, Paré PA: GC-MS SPME profiling or rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 2006, 67: 2262–2268.View ArticlePubMedGoogle Scholar
- Fraatz MA, Zorn H: Fungal Flavours. In The Mycota X: Industial Applications. 2nd edition. Edited by: Hofrichter M. Springer-Verlag, Berlin; 2010:249–264.Google Scholar
- French RC, Gale AW, Graham CL, Latterell FM, Schmitt CG, Marchetti MA, Rines HW: Differences in germination response of spores of several species of rust and smut fungi to nonanal, 6-methyl-5-hepten-2-one, and related compounds. J Agric Food Chem 1975, 23: 766–770.View ArticlePubMedGoogle Scholar
- Herrmann A: The chemistry and biology of volatiles. Wiley, Chichester; 2010.View ArticleGoogle Scholar
- Holm RE: Volatile metabolites controlling germination in buried weed seeds. Plant Physiol 1972, 30: 293–297.View ArticleGoogle Scholar
- Hung R, Lee S, Bennett JW: The effect of low concentrations of the semiochemical 1-octen-3-ol on Arabidopsis thaliana . Fungal Ecol 2013, 6: 19–26.View ArticleGoogle Scholar
- Hung R, Lee S, Bennett JW: The effects of low concentrations of the enantiomers of mushroom alcohol (1-octen-3-ol) on Arabidopsis thaliana . Mycology: Int J Fungal Biol 2014, 5: 73–80.View ArticleGoogle Scholar
- Jelen HH, Wasowicz E: Volatile fungal metabolites and their relation to the spoilage of agricultural commodities. Food Rev Int 1998, 14: 391–426.View ArticleGoogle Scholar
- Jing H, Sturre MJG, Hille J, Dijkwel PP: Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J 2002, 32: 51–63.View ArticlePubMedGoogle Scholar
- Kinderlerer J: Volatile metabolites of filamentous fungi and their role in food flavor. J Appl Bacteriol Symp Suppl 1989, 67: 133S-144S.View ArticleGoogle Scholar
- Kishimoto K, Matsui K, Ozawa R, Takabayashi J: Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana . J Gen Plant Pathol 2007, 73: 35–37.View ArticleGoogle Scholar
- Koornneef M, Bentsink L, Hilhorst H: Seed dormancy and germination. Curr Opin Plant Biol 2002, 5: 33–36.View ArticlePubMedGoogle Scholar
- Korpi A, Jarnberg J, Pasanen A-L: Microbial volatile organic compounds. Crit Rev Toxicol 2009, 39: 139–193.View ArticlePubMedGoogle Scholar
- Kuske M, Romain A-C, Nicolas J: Microbial volatile organic compounds as indicators of fungi. Can an electronic nose detect fungi in indoor environments? Build Environ 2005, 40: 824–831.View ArticleGoogle Scholar
- Lee S, Hung R, Schink A, Mauro J, Bennett JW: Phytotoxicity of volatile organic compound. Plant Grow Reg 2014.Google Scholar
- Lugtenberg B, Kamilova F: Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 2009, 63: 541–556.View ArticlePubMedGoogle Scholar
- Macias-Rubalcava ML, Hernandez-Bautista BE, Oropeza F, Duarte G, Gonzalez MC, Glenn AE, Hanlin RT, Anaya AL: Allelochemical effects of volatile compounds and organic extracts from Muscodor yucatanensis , a tropical endophytic fungus from Bursera simaruba . J Chem Ecol 2010, 36: 1122–1131.View ArticlePubMedGoogle Scholar
- Matysik S, Herbarth O, Mueller A: Determination of volatile metabolites originating from mould growth on wall paper and synthetic media. J Microbiol Methods 2008, 75: 182–187.View ArticlePubMedGoogle Scholar
- Mburu DM, Ndung’u MW, Maniania NK, Hassanali A: Comparison of volatile blends and gene sequences of two isolates of Metarhizium anisopliae of different virulence and repellency toward the termite Macrotermes michaelseni . J Exp Biol 2011, 214: 956–962.View ArticlePubMedGoogle Scholar
- Minerdi D, Bossi S, Gullino ML, Garibaldi A: Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol 2009, 11: 844–854.View ArticlePubMedGoogle Scholar
- Minerdi D, Bossi S, Maffei ME, Gullino ML, Garibaldi A: Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS Microbiol Ecol 2011, 76: 342–351.View ArticlePubMedGoogle Scholar
- Morath SU, Hung R, Bennett JW: Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 2012, 26: 73–83.View ArticleGoogle Scholar
- Ogura T, Sunairi M, Nakajima M: 2-Methylisoborneol and geosmin, the main sources of soil odor, inhibit the germination of Brassicaceae seeds. Soil Sci 2000, 46: 217–227.Google Scholar
- Palta JP: Leaf chlorophyll content. Remote Sens Rev 1990, 5: 207–213.View ArticleGoogle Scholar
- Paul D, Park KS: Identification of volatiles produced by Cladosporium cladosporioides CL-1, a fungal biocontrol agent that promotes plant growth. Sensors 2013, 13: 13969–13977.PubMed CentralView ArticlePubMedGoogle Scholar
- Rohlfs M, Obmann BR, Petersen R: Competition with filamentous fungi and its implication for a gregarious lifestyle in insects living on ephemeral resources. Ecol Entomol 2005, 30: 556–563.View ArticleGoogle Scholar
- Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, Kloepper JW: Bacterial volatiles promote growth in Arabidopsis . Proc Natl Acad Sci U S A 2003, 100: 4927–4932.PubMed CentralView ArticlePubMedGoogle Scholar
- Sahlberg B, Gunnbjörnsdottir M, Soonc A, Jogi R, Gislason T, Wieslander G, Janson C, Norback D: Airborne molds and bacteria, microbial volatile organic compounds (MVOC), plasticizers and formaldehyde in dwellings in three North European cities in relation to sick building syndrome (SBS). Sci Total Environ 2013, 444: 433–440.View ArticlePubMedGoogle Scholar
- Schnürer J, Olsson J, Borjesson T: Fungal volatiles as indicators of food and feeds spoilage. Fungal Genet Biol 1999, 27: 209–217.View ArticlePubMedGoogle Scholar
- Splivallo R, Novero M, Bertea CM, Bossi S, Bonfante P: Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana . New Phytol 2007, 175: 17–24.View ArticleGoogle Scholar
- Steinkraus KH: Industrial Applications of Oriental Fungal Fermentations. In The Filamentous Fungi Vol. 4 Fungal Technology. Edited by: Smith JE, Berry DR, Kristiansesn B. Edward Arnold, London; 1983:171–189.Google Scholar
- Strobel GA, Dirkse E, Sears J, Markworth C: Volatile antimicrobials from Muscodor albus , a novel endophytic fungus. Microbiology 2001, 147: 2943–2950.View ArticlePubMedGoogle Scholar
- Sunesson A-L, Vaes WHJ, Nilsson C-A, Blomquist GR, Andersson B, Carlson R: Identification of volatile metabolites from five fungal species cultivated on two media. Appl Environ Microbiol 1995, 61: 2911–2918.PubMed CentralPubMedGoogle Scholar
- Takken W, Knols BG: Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 1999, 44: 131–157.View ArticlePubMedGoogle Scholar
- Thakeow P, Angeli S, Weißbecker B, Schütz S: Antennal and behavioral responses of Cis boleti to fungal odor of Trametes gibbosa . Chem Senses 2008, 33: 379–387.View ArticlePubMedGoogle Scholar
- Turner WB, Aldridge DC: Fungal Metabolites II. Academic Press, London; 1983.Google Scholar
- Van Loon LC, Bakker PAHM, Pieterse CMJ: Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 1998, 36: 453–483.View ArticlePubMedGoogle Scholar
- Vespermann A, Kai M, Piechulla B: Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana . Appl Environ Microbiol 2007, 73: 5639–5641.PubMed CentralView ArticlePubMedGoogle Scholar
- Wang X, Sun C, Gao S, Wang L, Shuokui H: Validation of germination rate and root elongation as indicator to assess phytotoxicity with Cucumis sativus . Chemosphere 2001, 44: 1711–1721.View ArticlePubMedGoogle Scholar
- Wenke K, Kai M, Piechulla B: Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 2010, 231: 499–506.View ArticlePubMedGoogle Scholar
- Wenke K, Weise T, Warnke R, Valverde C, Wanke D, Kai M, Piechulla B: Bacterial Volatiles Mediating Information Between Bacteria and Plants. In Biocommunication of Plants. Edited by: Witzany G, Baluska F. Springer-Verlag, Berlin; 2012:327–347.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.