Abstract
The Masson pine (Pinus massoniana Lamb.) has a relatively strong tolerance to stressors such as acid rain, drought, and phosphorus deficiency. Previous studies have mainly focused on morphological, physiological, and metabolic responses in the needles of the Masson pine. However, there has been little study of the effects of drought stress on root tip structure or the composition of volatile organic compounds (VOCs) in the root tip. Therefore, this work aimed to evaluate the VOCs and anatomical growth responses of Masson pine root tips to drought stress. The results showed that (1) drought stress inhibited increases in root biomass, root growth, and lateral root number, and damaged and significantly deformed the root apical structure; (2) the relative contents of monoterpenes decreased with the intensity of drought stress, but the relative content of sesquiterpenes increased. (3) The ratio of sesquiterpenes to monoterpenes in the root tip was approximately 1:2 in the absence of stress, and became 3:1 under severe drought stress. The results indicate changes of secondary metabolism in the root tip of the Masson pine in response to drought stress.
References
Achotegui-Castells A, Llusià J, Hódar JA, Peuelas J (2013) Needle terpene concentrations and emissions of two coexisting subspecies of Scots pine attacked by the pine processionary moth (Thaumetopoea pityocampa). Acta Physiol Plant 35:3047–3058. doi:10.1007/s11738-013-1337-3
Adler LS, Wink M, Distl M, Lentz AJ (2006) Leaf herbivory and nutrients increase nectar alkaloids. Ecol Lett 9:960–967. doi:10.1111/j.1461-0248.2006.00944.x
Ahmed R, Hoque ATM, Hossain MK (2008) Allelopathic effects of leaf litters of Eucalyptus camaldulensis on some forest and agricultural crops. J For Res 19:19–24. doi:10.1007/s11676-008-0003-x
Bais HP, Loyola Vargas VM, Flores HE, Vivanco JM (2001) Root specific metabolism: the biology and biochemistry of underground organs. In vitro Cell Dev Biol Plant 37:730–741. doi:10.1007/s11627-001-0122-y
Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant–plant interactions: “talking trees” in the genomics era. Science 311:812–815. doi:10.1126/science.1118446
Blanch JS, Peñuelas J, Sardans J, Llusiá J (2009) Drought, warming and soil fertilization effects on leaf volatile terpene concentrations in Pinus halepensis and Quercus ilex. Acta Physiol Plant 31:207–218. doi:10.1007/s11738-008-0221-z
Blanch JS, Sampedro L, Llusia J, Moreira X, Zas R, Penuelas J (2012) Effects of phosphorus availability and genetic variation of leaf terpene content and emission rate in Pinus pinaster seedlings susceptible and resistant to the pine weevil, Hylobius abietis. Plant Biol 14:66–72. doi:10.1111/j.1438-8677.2011.00492.x
Chiatante D, Iorio AD, Maiuro L, Scippa SG (1999) Effect of water stress on root meristems in woody and herbaceous plants during the first stage of development. Plant Soil 217:159–172. doi:10.1023/A:1004691705048
Delfine S, Loreto F, Pinelli P, Tognetti R, Alvino A (2005) Isoprenoids content and photosynthetic limitations in rosemary and spearmint plants under water stress. Agric Ecosyst Environ 106:243–252. doi:10.1016/j.agee.2004.10.012
Dicke M, Loreto F (2010) Induced plant volatiles: from genes to climate change. Trends Plant Sci 15:115–117. doi:10.1016/j.tplants.2010.01.007
Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847. doi:10.1038/35081178
Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902. doi:10.1104/pp.104.049981
Eyles A, Bonello P, Ganley R, Mohammed C (2010) Induced resistance to pests and pathogens in trees. New Phytol 185:893–908. doi:10.1111/j.1469-8137.2009.03127.x
Fan FH, Ding GJ, Wen XP (2016) Proteomic analyses provide new insights into the responses of Pinus massoniana seedlings to phosphorus deficiency. Proteomics 16:504–515. doi:10.1002/pmic.201500140
Fantaye CA, Köpke D, Gershenzon J, Degenhardt J (2015) Restoring (E)-β-caryophyllene production in a non-producing maize line compromises its resistance against the fungus Colletotrichum graminicola. J Chem Ecol 41:213–223. doi:10.1007/s10886-015-0556-z
Fernandez C, Lelong B, Vila B, Mévy JP, Robles C, Greff S, Dupouyet S, Bousquet-Mélou A (2006) Potential allelopathic effect of Pinus halepensis, in the secondary succession: an experimental approach. Chemoecology 16:97–105. doi:10.1007/s00049-006-0334-z
Filella I, Penuelas J, Seco R (2009) Short-chained oxygenated VOC emissions in Pinus halepensis in response to changes in water availability. Acta Physiol Plant 31:311–318. doi:10.1007/s11738-008-0235-6
Gargallo-Garriga A, Sardans J, Pérez-Trujillo M, Rivas-Ubach A, Oravec M, Vecerova K, Urban O, Jentsch A, Kreyling J, Beierkuhnlein C, Parella T, Peñuelas J (2014) Opposite metabolic responses of shoots and roots to drought. Sci Rep 4:6829. doi:10.1038/srep06829
Gniazdowska A, Bogatek R (2005) Allelopathic interactions between plants. Multi site action of allelochemicals. Acta Physiol Plant 27:395–407. doi:10.1007/s11738-005-0017-3
Hanover JW (1992) Applications of terpene analysis in forest genetics. New For 6:159–178. doi:10.1007/BF00120643
Hiltpold I, Toepfer S, Kuhlmann U, Turlings TCJ (2010) How maize root volatiles affect the efficacy of entomopathogenic nematodes in controlling the western corn rootworm? Chemoecology 20:155–162. doi:10.1007/s00049-009-0034-6
Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184. doi:10.1016/j.tplants.2010.01.006
Hu WJ, Chen J, Liu TW, Martin S, Wang WH, Chen J, Wu FH, Liu X, Shen ZJ, Zheng HL (2014) Proteome and calcium-related gene expression in Pinus massoniana needles in response to acid rain under different calcium levels. Plant Soil 380:285–303. doi:10.1007/s11104-014-2086-9
Incerti G, Romano A, Termolino P, Lanzotti V (2013) Metabolomic fingerprinting using nuclear magnetic resonance and multivariate data analysis as a tool for biodiversity informatics: a case study on the classification of Rosa damascena. Plant Biosyst 147:947–954. doi:10.1080/11263504.2013.781072
Ioannou E, Koutsaviti A, Tzakou O, Roussis V (2014) The genus Pinus: a comparative study on the needle essential oil composition of 46 pine species. Phytochem Rev 13:741–768. doi:10.1007/s11101-014-9338-4
Jeon JH, Lee HS (2013) Volatile components of essential oils extracted from Pinus species. J Essent Oil Bear Plants 15:750–754. doi:10.1080/0972060X.2012.10644115
Kato-Noguchi H, Fushimi Y, Shigemori H (2009) An allelopathic substance in red pine needles (Pinus densiflora). J Plant Physiol 166:442–446. doi:10.1016/j.jplph.2008.06.012
Kim H, Lee B, Yun KW (2013) Comparison of chemical composition and antimicrobial activity of essential oils from three Pinus species. Ind Crop Prod 44:323–329. doi:10.1016/j.indcrop.2012.10.026
Kimura F, Sato M, Kato-Noguchi H (2015) Allelopathy of pine litter: delivery of allelopathic substances into forest floor. J Plant Biol 58:61–67. doi:10.1007/s12374-014-0322-8
Kleist E, Mentel TF, Andres S, Bohne A, Folkers A, Kiendler-Scharr A, Rudich Y, Springer M, Tillmann R, Wildt J (2012) Irreversible impacts of heat on the emissions of monoterpenes, sesquiterpenes, phenolic BVOC and green leaf volatiles from several tree species. Biogeosciences 9:5111–5123. doi:10.5194/bg-9-5111-2012
Laothawornkitkul J, Paul ND, Vickers CE, Possell M, Taylor JE, Mullineaux PM, Hewitt CN (2008) Isoprene emissions influence herbivore feeding decisions. Plant Cell Environ 31:1410–1415. doi:10.1111/j.1365-3040.2008.01849.x
Lieutier F, Yart A, Salle A (2009) Stimulation of tree defenses by ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann For Sci 66:801. doi:10.1051/forest/2009066
Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166. doi:10.1016/j.tplants.2009.12.006
Lundborg L, Nordlander G, Björklund N, Nordenhem H, Borg-Karlson AK (2016) Methyl jasmonate-induced monoterpenes in Scots pine and Norway spruce tissues affect pine weevil orientation. J Chem Ecol 42:1237–1246. doi:10.1007/s10886-016-0790-z
Meiners SJ, Kong CH, Ladwig LM, Pisula NL, Lang KA (2012) Developing an ecological context for allelopathy. Plant Ecol 213:1221–1227. doi:10.1007/s11258-012-0078-5
Napierala-Filipiak A, Werner A, Mardarowicz M, Gawdzik J (2002) Concentrations of terpenes in mycorrhizal roots of Scots pine (Pinus sylvestris L.) seedlings grown in vitro. Acta Physiol Plant 24:137–143. doi:10.1007/s11738-002-0003-y
Niinemets Ü (2010) Mild versus severe stress and BVOCs: thresholds, priming and consequences. Trends Plant Sci 15:145–153. doi:10.1016/j.tplants.2009.11.008
Niinemets Ü (2016) Uncovering the hidden facets of drought stress: secondary metabolites make the difference. Tree Physiol 36:129–132. doi:10.1093/treephys/tpv128
Niinemets Ü, Kännaste A, Copolovici L (2013) Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Front Plant Sci 4:1–15. doi:10.3389/fpls.2013.00262
Ormeño E, Mevy JP, Vila B, Bousquet-Melou A, Greff S, Bonin G, Fernandez C (2007) Water deficit stress induces different monoterpene and sesquiterpene emission changes in Mediterranean species. Relationship between terpene emissions and plant water potential. Chemosphere 67:276–284. doi:10.1016/j.chemosphere.2006.10.029
Pala PJ, Brophy JJ, Goldsack RJ, Fontaniella B (2004) Analysis of the volatile components of Lavandula canariensis (L.) Mill., a canary islands endemic species, growing in Australia. Biochem Syst Ecol 32:55–62. doi:10.1016/S0305-1978(03)00177-7
Patakas A, Nikolaou N, Zioziou E, Radoglou K, Noitsakis B (2002) The role of organic solute and ion accumulation in osmotic adjustment in drought-stressed grapevines. Plant Sci 163:361–367. doi:10.1016/S0168-9452(02)00140-1
Pham T, Chen H, Yu J, Dai L, Zhang R, Quynh T, Vu T (2014) The differential effects of the blue-stain fungus Leptographium qinlingensis on monoterpenes and sesquiterpenes in the stem of chinese white pine (Pinus armandi) saplings. Forests 5:2730–2749. doi:10.3390/f5112730
Pichersky E, Noel J, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811. doi:10.1126/science.1118510
Pichler P, Oberhuber W (2007) Radial growth response of coniferous forest trees in an inner Alpine environment to heat-wave in 2003. For Ecol Manag 242:688–699. doi:10.1016/j.foreco.2007.02.007
Rajabi-Memari H, Pazouki L, Niinemets Ü (2013) The biochemistry and molecular biology of volatile messengers in trees. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5. Tree physiology. Springer, Berlin, pp 47–93
Rice EL (1979) Allelopathy—an update. Bot Rev 45:15–109. doi:10.1007/BF02869951
Rice KJ, Gordon DR, Hardison JL, Welker JM (1993) Phenotypic variation in seedlings of a keystone tree species (Quercus douglasii) the interactive effects of acorn source and competitive environment. Oecologia 96:537–547. doi:10.1007/BF00320511
Rivoal A, Fernandez C, Greff S, Montes N, Vila B (2011) Does competition stress decrease allelopathic potential? Biochem Syst Ecol 39:401–407. doi:10.1016/j.bse.2011.05.017
Robert C, Erb M, Hiltpold I, Hibbard B, Gaillard M, Bilat J, Degenhardt J, Cambet-Petit-Jean X, Turlings T, Zwahlen C (2013) Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnol J 11:628–639. doi:10.1111/pbi.12053
Rosenkranz M, Schnitzler JP (2013) Genetic engineering of BVOC emissions from trees. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5. Tree physiology. Springer, Berlin, pp 95–118
Sampedro L, Moreira X, Zas R (2011) Resistance and response of Pinus pinaster seedlings to Hylobius abietis after induction with methyl jasmonate. Plant Ecol 212:397–401. doi:10.1007/s11258-010-9830-x
Schade GW, Goldstein AH (2001) Fluxes of oxygenated volatile organic compounds from a ponderosa pine plantation. J Geophys Res 106:3111–3124. doi:10.1029/2000JD900592
Simpraga M, Verbeeck H, Demarcke M, Joo E, Pokorska O, Amelynck C, Schoon N, Dewulf J, Van Langenhove H, Heinesch B, Aubinet M, Laffineur Q, Muller JF, Steppe K (2011) Clear link between drought stress, photosynthesis and biogenic volatile organic compounds in Fagus sylvatica L. Atmos Environ 45:5254–5525. doi:10.1016/j.atmosenv.2011.06.075
Soukup A, Čížková H (2002) Development of anatomical structure of roots of Phragmites australis. New Phytol 153:277–287. doi:10.1046/j.0028-646X.2001.00317.x
Su JW, Zeng JP, Qin XW, Ge F (2009) Effect of needle damage on the release rate of Masson pine (Pinus massoniana Lamb.) volatiles. J Plant Res 122:193–200. doi:10.1007/s10265-008-0203-7
Taveira M, Fernandes F, Guedes de Pinho P, Andrade PB, Pereira JA, Valentão P (2009) Evolution of Brassica rapa var. rapa L. volatile composition by HS-SPME and GC/ITMS. Microchem J 93:140–146. doi:10.1016/j.microc.2009.05.011
Theis N, Lerdau M (2003) The evolution of function in plant secondary metabolites. Int J Plant Sci 164:93–102. doi:10.1086/374190
Theis N, Kesler K, Adler LS (2009) Leaf herbivory increases floral fragrance in male but not female Cucurbita pepo subsp. texana (Cucurbitaceae) flowers. Am J Bot 96:897–903. doi:10.3732/ajb.0800300
Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:1–10. doi:10.1007/s11104-012-1295-3
Vacchiano G, Garbarino M, Borgogno Mondino E, Motta R (2012) Evidences of drought stress as a predisposing factor to Scots pine decline in Valle d’Aosta (Italy). Eur J For Res 131:989–1000. doi:10.1007/s10342-011-0570-9
Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51. doi:10.1104/pp.102.019661
Wang X, Liu Z, Niu L, Fu B (2013) Long-term effects of simulated acid rain stress on a staple forest plant Pinus massoniana Lamb: a proteomic analysis. Trees 27:297–309. doi:10.1007/s00468-012-0799-z
Wei G, Tian P, Zhang F, Qin H, Miao H, Chen Q, Hu Z, Cao L, Wang M, Gu X, Huang S, Chen M, Wang G (2016) Integrative analyses of non-targeted volatile profiling and transcriptome data provide molecular insight into VOC diversity in cucumber plants (Cucumis sativus L.). Plant Physiol 172:603–618. doi:10.1104/pp.16.01051
Werner A, Napierala-Filipiak AM, Gawdzik J (2004) The effects of heavy metals, content of nutrients and inoculation with mycorrhizal fungi on the level of terpenoids in roots of Pinus sylvestris seedlings. Acta Physiol Plant 26:187–196. doi:10.1007/s11738-004-0008-9
Xiang ZM, Cai K, Liang GL, Zhou SP, Ge YH, Zhang J, Geng ZL (2014) Analysis of volatile flavour components in flue-cured tobacco by headspace solid-phase microextraction combined with GC × GC–TOFMS. Anal Methods 6:3300–3308. doi:10.1039/c3ay41956h
Yoder-Williams MP, Parker VT (2011) Allelopathic interference in the seedbed of Pinus jeffreyi in the Sierra Nevada, California. Can J For Res 17:991–994. doi:10.1139/x87-153
Zhang DJ, Jian Z, Yang WQ, Wu FZ (2010) Potential allelopathic effect of eucalyptus, grandis across a range of plantation ages. Ecol Res 25:13–23. doi:10.1007/s11284-009-0627-0
Acknowledgements
The authors thank Prof. Z.N. Yang (Guizhou Normal University, Guiyang, P. R. China), for the critical reading of the manuscript. This work was supported by the National Natural Science Foundation of China (NSFC, nos. 31260183, 31660200), National Science & Technology support Program during the 12th Five-Year Plan Period (no. 2015BAD09B01) and the National High-Tech R&D Program (863 Program) (no. 2011AA10020301).
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Quan, W., Ding, G. Root tip structure and volatile organic compound responses to drought stress in Masson pine (Pinus massoniana Lamb.). Acta Physiol Plant 39, 258 (2017). https://doi.org/10.1007/s11738-017-2558-7
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DOI: https://doi.org/10.1007/s11738-017-2558-7