Barley (Hordeum distichon L.) roots synthesise volatile aldehydes with a strong age-dependent pattern and release (E)- non-2-enal and (E,Z)-nona-2,6-dienal after mechanical injury
Delory, Benjamin M.; Delaplace, Pierre; du Jardin, Patricket al.
[en] In the context of chemical ecology, the analysis of the temporal production pattern of volatile organic compounds (VOCs) in root tissues and the emission rate measurement of root-emitted VOCs are of major importance for setting up experiments to study the implication of these compounds in biotic interactions. Such analyses, however, remain challenging because of the belowground location of plant root systems. In this context, this study describes the evolution of the root VOC production pattern of barley (Hordeum distichon L.) at five developmental stages from germination to the end of tillering and evaluates the emission of the identified VOCs in an artificial soil. VOCs produced by crushed root tissues and released by
unexcavated root systems were analysed using dynamic sampling devices coupled to a gas chromatography-mass spectrometry methodology (synchronous SCAN/SIM). The results showed that, at each analysed developmental stage, crushed barley roots produced mainly four volatile aldehydes: hexanal; (E)-hex-2-enal; (E)-non-2-enal; and (E,Z)-nona-2,6-dienal. Higher total and individual VOC concentrations were measured in 3-day-old seminal roots compared with older phenological stages. For each developmental stage, the lipoxygenase (LOX) activity was greater for linoleic acid than α-linolenic acid and the greatest LOX activities using linoleic and α- linolenic acids as substrates were measured in 7- and 3-day-old roots, respectively. The analysis of VOCs released by barley roots into the soil showed that (E)-non-2- enal and (E,Z)-nona-2,6-dienal were the only VOCs emitted in quantifiable amounts by mechanically injured roots.
Delaplace, Pierre ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Biologie végétale
du Jardin, Patrick ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Biologie végétale
Fauconnier, Marie-Laure ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie générale et organique
Language :
English
Title :
Barley (Hordeum distichon L.) roots synthesise volatile aldehydes with a strong age-dependent pattern and release (E)- non-2-enal and (E,Z)-nona-2,6-dienal after mechanical injury
Ali J.G., Alborn H.T., Stelinski L.L. Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J. Ecol. 2011, 99:26-35. 10.1111/j.1365-2745.2010.01758.x.
Ali J.G., Alborn H.T., Stelinski L.L. Subterranean herbivore-induced volatiles released by Citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. J. Chem. Ecol. 2010, 36:361-368. 10.1007/s10886-010-9773-7.
Azam M., Jiang Q., Zhang B., Xu C., Chen K. Citrus leaf volatiles as affected by developmental stage and genetic type. Int. J. Mol. Sci. 2013, 14:17744-17766. 10.3390/ijms140917744.
Barton K.E., Koricheva J. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am. Nat. 2010, 175:481-493. 10.1086/650722.
Batten J.H., Stutte G.W., Wheeler R.M. Effect of crop development on biogenic emissions from plant populations grown in closed plant growth chambers. Phytochemistry 1995, 39:1351-1357.
Boege K., Marquis R.J. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 2005, 20:441-448. 10.1016/j.tree.2005.05.001.
Boff M.I.C., van Tol R., Smits P.H. Behavioural response of Heterorhabditis megidis towards plant roots and insect larvae. Biocontrol 2002, 47:67-83.
Boué S.M., Shih B.Y., Carter-Wientjes C.H., Cleveland T.E. Identification of volatile compounds in soybean at various developmental stages using solid phase microextraction. J. Agric. Food Chem. 2003, 51:4873-4876. 10.1021/jf030051q.
Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254. 10.1016/0003-2697(76)90527-3.
Crespo E., Hordijk C.A., de Graaf R.M., Samudrala D., Cristescu S.M., Harren F.J.M., van Dam N.M. On-line detection of root-induced volatiles in Brassica nigra plants infested with Delia radicum L. root fly larvae. Phytochemistry 2012, 84:68-77. 10.1016/j.phytochem.2012.08.013.
Croteau R., Felton M., Karp F., Kjonaas R. Relationship of camphor biosynthesis to leaf development in sage (Salvia officinalis). Plant Physiol. 1981, 67:820-824.
Danner H., Brown P., Cator E.A., Harren F.J.M., van Dam N.M., Cristescu S.M. Aboveground and belowground herbivores synergistically induce volatile organic sulfur compound emissions from shoots but not from roots. J. Chem. Ecol. 2015, 10.1007/s10886-015-0601-y.
Delory B.M., Delaplace P., Fauconnier M.-L., du Jardin P. Root-emitted volatile organic compounds: can they mediate belowground plant-plant interactions?. Plant Soil 2016, 10.1007/s11104-016-2823-3.
Dudareva N., Klempien A., Muhlemann K., Kaplan I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol. 2013, 198:16-32.
Eilers E.J., Pauls G., Rillig M.C., Hansson B.S., Hilker M., Reinecke A. Novel set-up for low-disturbance sampling of volatile and non-volatile compounds from plant roots. J. Chem. Ecol. 2015, 41:253-266. 10.1007/s10886-015-0559-9.
Elger A., Lemoine D.G., Fenner M., Hanley M.E. Plant ontogeny and chemical defence: older seedlings are better defended. Oikos 2009, 118:767-773. 10.1111/j.1600-0706.2009.17206.x.
Erb M., Balmer D., De Lange E.S., Von Merey G., Planchamp C., Robert C.A.M., Röder G., Sobhy I., Zwahlen C., Mauch-Mani B., Turlings T.C.J. Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots. Plant. Cell Environ. 2011, 34:1088-1103. 10.1111/j.1365-3040.2011.02307.x.
Erb M., Ton J., Degenhardt J., Turlings T.C. Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol. 2008, 146:867-874. 10.1104/pp.107.112169.
Farnier K., Bengtsson M., Becher P.G., Witzell J., Witzgall P., Manduríc S. Novel bioassay demonstrates attraction of the white potato cyst nematode Globodera pallida (Stone) to non-volatile and volatile host plant cues. J. Chem. Ecol. 2012, 38:795-801. 10.1007/s10886-012-0105-y.
Feng X.-L., He Y., Liang Y.-Z., Wang Y.-L., Huang L.-F., Xie J.-W. Comparative analysis of the volatile components of Agrimonia eupatoria from leaves and roots by gas chromatography-mass spectrometry and multivariate curve resolution. J. Anal. Methods Chem. 2013, Article ID 246986. 10.1155/2013/246986.
Ferreira V., Aznar M., López R., Cacho J. Quantitative gas chromatography-olfactometry carried out at different dilutions of an extract. Key differences in the odor profiles of four high-quality spanish aged red wines. J. Agric. Food Chem. 2001, 49:4818-4824.
Ferry A., Dugravot S., Delattre T., Christides J.-P., Auger J., Bagnères A.-G., Poinsot D., Cortesero A.-M. Identification of a widespread monomolecular odor differentially attractive to several Delia radicum ground-dwelling predators in the field. J. Chem. Ecol. 2007, 33:2064-2077. 10.1007/s10886-007-9373-3.
Fiers M., Lognay G., Fauconnier M.-L., Jijakli M.H. Volatile compound-mediated interactions between barley and pathogenic fungi in the soil. PLoS One 2013, 8:e66805. 10.1371/journal.pone.0066805.
Gershenzon J., McConkey M.E., Croteau R.B. Regulation of monoterpene accumulation in leaves of peppermint. Plant Physiol. 2000, 122:205-213.
Gfeller A., Laloux M., Barsics F., Kati D.E., Haubruge E., du Jardin P., Verheggen F.J., Lognay G., Wathelet J.-P., Fauconnier M.-L. Characterization of volatile organic compounds emitted by barley (Hordeum vulgare L.) roots and their attractiveness to wireworms. J. Chem. Ecol. 2013, 39:1129-1139. 10.1007/s10886-013-0302-3.
Gigot C., Ongena M., Fauconnier M.-L., Wathelet J.-P., du Jardin P., Thonart P. The lipoxygenase metabolic pathway in plants: potential for industrial production of natural green leaf volatiles. Biotechnol. Agron. Société Environ. 2010, 14:451-460.
Gouinguené S.P., Turlings T.C.J. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol. 2002, 129:1296-1307. 10.1104/pp.001941.1296.
Grechkin A.N., Hamberg M. The "heterolytic hydroperoxide lyase" is an isomerase producing a short-lived fatty acid hemiacetal. Biochim. Biophys. Acta 2004, 1636:47-58. 10.1016/j.bbalip.2003.12.003.
Guerin P.M., Ryan M.F. Relationship between root volatiles of some carrot cultivars and their resistance to the carrot fly, Psila rosae. Entomol. Exp. Appl. 1984, 36:217-224.
Hare J.D. Ontogeny and season constrain the production of herbivore-inducible plant volatiles in the field. J. Chem. Ecol. 2010, 36:1363-1374. 10.1007/s10886-010-9878-z.
Hare J.D., Sun J.J. Production of herbivore-induced plant volatiles is constrained seasonally in the field but predation on herbivores is not. J. Chem. Ecol. 2011, 37:430-442. 10.1007/s10886-011-9944-1.
Hiltpold I., Bernklau E., Bjostad L.B., Alvarez N., Miller-Struttmann N.E., Lundgren J.G., Hibbard B.E. Nature, evolution and characterisation of rhizospheric chemical exudates affecting root herbivores. Adv. Insect Physiology 2013, 10.1016/B978-0-12-417165-7.00003-9.
Hiltpold I., Erb M., Robert C.A.M., Turlings T.C.J. Systemic root signalling in a belowground, volatile-mediated tritrophic interaction. Plant Cell Environ. 2011, 34:1267-1275.
Hiltpold I., Turlings T.C.J. Belowground chemical signaling in maize: when simplicity rhymes with efficiency. J. Chem. Ecol. 2008, 34:628-635. 10.1007/s10886-008-9467-6.
Holopainen J.K., Gershenzon J. Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 2010, 15:176-184. 10.1016/j.tplants.2010.01.006.
Holtman W.L., van Duijn G., Sedee N.J.A., Douma A.C. Differential expression of lipoxygenase isoenzymes in embryos of germinating barley. Plant Physiol. 1996, 111:569-576.
Jassbi A.R., Zamanizadehnajari S., Baldwin I.T. Phytotoxic volatiles in the roots and shoots of Artemisia tridentata as detected by headspace solid-phase microextraction and gas chromatographic-mass spectrometry analysis. J. Chem. Ecol. 2010, 36:1398-1407. 10.1007/s10886-010-9885-0.
Jennings W., Shibamoto T. Qualitative Analysis of Flavor and Fragrance Volatiles by Glass Capillary Gas Chromatography 1980, Academic Press, Inc., New-York.
Kegge W., Ninkovic V., Glinwood R., Welschen R.A.M., Voesenek L.A.C.J., Pierik R. Red:far-red light conditions affect the emission of volatile organic compounds from barley (Hordeum vulgare), leading to altered biomass allocation in neighbouring plants. Ann. Bot. 2015, 10.1093/aob/mcv036.
Köllner T.G., Schnee C., Gershenzon J., Degenhardt J. The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distributions. Phytochemistry 2004, 65:1895-1902. 10.1016/j.phytochem.2004.05.021.
Kuhn U., Rottenberger S., Biesenthal T., Wolf A., Schebeske G., Ciccioli P., Kesselmeier J. Strong correlation between isoprene emission and gross photosynthetic capacity during leaf phenology of the tropical tree species Hymenaea courbaril with fundamental changes in volatile organic compounds emission composition during early leaf development. Plant Cell Environ. 2004, 27:1469-1485. 10.1111/j.1365-3040.2004.01252.x.
Lawo N.C., Weingart G.J.F., Schuhmacher R., Forneck A. The volatile metabolome of grapevine roots: first insights into the metabolic response upon phylloxera attack. Plant Physiol. Biochem. 2011, 49:1059-1063. 10.1016/j.plaphy.2011.06.008.
Laznik Ž., Košir I.J., Rozman L., Kač M., Trdan S. Preliminary results of variability in mechanical-induced volatile root-emissions of different maize cultivars. Maydica 2011, 56:343-350.
Maffei M.E. Sites of synthesis, biochemistry and functional role of plant volatiles. South Afr. J. Bot. 2010, 76:612-631. 10.1016/j.sajb.2010.03.003.
Matsui K. Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr. Opin. Plant Biol. 2006, 9:274-280.
Matsui K., Minami A., Hornung E., Shibata H., Kishimoto K., Ahnert V., Kindl H., Kajiwara T., Feussner I. Biosynthesis of fatty acid derived aldehydes is induced upon mechanical wounding and its products show fungicidal activities in cucumber. Phytochemistry 2006, 67:649-657. 10.1016/j.phytochem.2006.01.006.
Min D.B., Callison A.L., Lee H.O. Singlet oxygen oxidation for 2-pentylfuran and 2-pentenylfuran formation in soybean oil. J. Food Sci. 2003, 68:1175-1178.
Neveu N., Grandgirard J., Nenon J.P., Cortesero A.M. Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L. J. Chem. Ecol. 2002, 28:1717-1732.
Palma R., Mutis A., Manosalva L., Ceballos R., Quiroz A. Behavioral and electrophysiological responses of Hylastinus obscurus to volatiles released from the roots of Trifolium pratense L. J. Soil Sci. Plant Nutr. 2012, 12:183-193.
Peñuelas J., Asensio D., Tholl D., Wenke K., Rosenkranz M., Piechulla B., Schnitzler J.P. Biogenic volatile emissions from the soil. Plant. Cell Environ. 2014, 37:1866-1891. 10.1111/pce.12340.
Piesik D., Lyszczarz A., Tabaka P., Lamparski R., Bocianowski J., Delaney K.J. Volatile induction of three cereals: influence of mechanical injury and insect herbivory on injured plants and neighbouring uninjured plants. Ann. Appl. Biol. 2010, 157:425-434. 10.1111/j.1744-7348.2010.00432.x.
Piesik D., Panka D., Delaney K.J., Skoczek A., Lamparski R., Weaver D.K. Cereal crop volatile organic compound induction after mechanical injury, beetle herbivory (Oulema spp.), or fungal infection (Fusarium spp.). J. Plant Physiol. 2011, 168:878-886.
Quintero C., Barton K.E., Boege K. The ontogeny of plant indirect defenses. Perspect. Plant Ecol. Evol. Syst. 2013, 15:245-254. 10.1016/j.ppees.2013.08.003.
R Core Team R: a Language and Environment for Statistical Computing 2015, R Foundation for Statistical Computing, Vienna, Austria, URL. http://www.r-project.org/.
Radhika V., Kost C., Bartram S., Heil M., Boland W. Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds. Planta 2008, 228:449-457. 10.1007/s00425-008-0749-6.
Rasmann S., Hiltpold I., Ali J. The role of root-produced volatile secondary metabolites in mediating soil interactions. Advances in Selected Plant Physiology Aspects 2012, 269-290. InTech, Rijeka. G. Montanaro, D. Bartolomeo (Eds.).
Rasmann S., Köllner T.G., Degenhardt J., Hiltpold I., Toepfer S., Kuhlmann U., Gershenzon J., Turlings T.C.J. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 2005, 434:732-737. 10.1038/nature03451.
Robert C.A.M., Erb M., Duployer M., Zwahlen C., Doyen G.R., Turlings T.C.J. Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytol. 2012, 194:1061-1069. 10.1111/j.1469-8137.2012.04127.x.
Rostás M., Cripps M.G., Silcock P. Aboveground endophyte affects root volatile emission and host plant selection of a belowground insect. Oecologia 2015, 177:487-497. 10.1007/s00442-014-3104-6.
Rostás M., Eggert K. Ontogenetic and spatio-temporal patterns of induced volatiles in Glycine max in the light of the optimal defence hypothesis. Chemoecology 2008, 18:29-38. 10.1007/s00049-007-0390-z.
Shiojiri K., Karban R. Plant age, communication, and resistance to herbivores: young sagebrush plants are better emitters and receivers. Oecologia 2006, 149:214-220. 10.1007/s00442-006-0441-0.
Shiojiri K., Karban R., Ishizaki S. Plant age, seasonality, and plant communication in sagebrush. J. Plant Interact. 2011, 6:85-88. 10.1080/17429145.2010.545959.
Silva-Navas J., Moreno-Risueno M.A., Manzano C., Pallero-Baena M., Navarro-Neila S., Téllez-Robledo B., Garcia-Mina J.M., Baigorri R., Gallego F.J., del Pozo J.C. D-Root: a system for cultivating plants with the roots in darkness or under different light conditions. Plant J. 2015, 84:244-255. 10.1111/tpj.12998.
Steeghs M., Bais H.P., de Gouw J., Goldan P., Kuster W., Northway M., Fall R., Vivanco J.M. Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis. Plant Physiol. 2004, 135:47-58. 10.1104/pp.104.038703.
Stewart D.W., Dwyer L.M. Analysis of phenological observations on barley (Hordeum vulgare) using the feekes scale. Agric. For. Meteorol. 1987, 39:37-48.
Surrey K. Spectrophotometric method for determination of lipoxidase activity. Plant Physiol. 1964, 39:65-70.
Sutherland O.R., Hillier J. Olfactory response of Costelytra zealandica (Coleoptera: Melolonthinae) to the roots of several pasture plants. New Zeal. J. Zool. 1974, 1:365-369.
Tapia T., Perich F., Pardo F., Palma G., Quiroz A. Identification of volatiles from differently aged red clover (Trifolium pratense) root extracts and behavioural responses of clover root borer (Hylastinus obscurus) (Marsham) (Coleoptera: Scolytidae) to them. Biochem. Syst. Ecol. 2007, 35:61-67. 10.1016/j.bse.2006.05.020.
Turlings T.C.J., Hiltpold I., Rasmann S. The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 2012, 358:51-60. 10.1007/s11104-012-1295-3.
van Dam N.M., Samudrala D., Harren F.J.M., Cristescu S.M. Real-time analysis of sulfur-containing volatiles in Brassica plants infested with root-feeding Delia radicum larvae using proton-transfer reaction mass spectrometry. AoB Plants 2012 2012, pls021. 10.1093/aobpla/pls021.
van Tol R., van der Sommen A.T.C., Boff M.I.C., van Bezooijen J., Sabelis M.W., Smits P.H. Plants protect their roots by alerting the enemies of grubs. Ecol. Lett. 2001, 4:292-294.
Weissteiner S., Huetteroth W., Kollmann M., Weißbecker B., Romani R., Schachtner J., Schütz S. Cockchafer larvae smell host root scents in soil. PLoS One 2012, 7:e45827. 10.1371/journal.pone.0045827.
Wenke K., Kai M., Piechulla B. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 2010, 231:499-506. 10.1007/s00425-009-1076-2.
Yokawa K., Kagenishi T., Kawano T., Mancuso S., Baluška F. Illumination of Arabidopsis roots induces immediate burst of ROS production. Plant Signal. Behav. 2011, 6:1460-1464. 10.4161/psb.6.10.18165.
Zadoks J.C., Chang T.T., Konzak C.F. A decimal code for the growth stages of cereals. Weed Res. 1974, 14:415-421.
Zhang P.-Y., Chen K.-S., He P.-Q., Liu S.-H., Jiang W.-F. Effects of crop development on the emission of volatiles in leaves of Lycopersicon esculentum and its inhibitory activity to Botrytis cinerea and Fusarium oxysporum. J. Integr. Plant Biol. 2008, 50:84-91. 10.1111/j.1744-7909.2007.00597.x.
Zhu J., Park K.-C. Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J. Chem. Ecol. 2005, 31:1733-1746. 10.1007/s10886-005-5923-8.
Zhuang H., Hamilton-Kemp T.R., Andersen R.A., Hildebrand D.F. Developmental change in C6-aldehyde formation by soybean leaves. Plant Physiol. 1992, 100:80-87.