Green Leaf Volatiles: A New Player in the Protection against Abiotic Stresses?
Abstract
:1. Introduction
2. Green Leaf Volatiles and Abiotic Stress
2.1. The Biosynthesis of Green Leaf Volatiles
2.2. Green Leaf Volatiles in the Atmosphere
2.3. Green Leaf Volatiles and Cold Stress
2.4. Green Leaf Volatiles and Drought Stress
2.5. Green Leaf Volatiles and Photosynthesis
3. Future Perspectives
4. Summary and Conclusions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Ameye, M.; Allmann, S.; Verwaeren, J.; Smagghe, G.; Haesaert, G.; Schuurink, R.C.; Audenaert, K. Green leaf volatile production by plants: A meta-analysis. New Phytol. 2018, 220, 666–683. [Google Scholar] [CrossRef] [PubMed]
- Matsui, K.; Engelberth, J. Green leaf volatiles-the forefront of plant responses against biotic attack. Plant Cell Physiol. 2022, 63, 1378–1390. [Google Scholar] [CrossRef] [PubMed]
- Scala, A.; Allmann, S.; Mirabella, R.; Haring, M.A.; Schuurink, R.C. Green leaf volatiles: A plant’s multifunctional weapon against herbivores and pathogens. Int. J. Mol. Sci. 2013, 14, 17781–17811. [Google Scholar] [CrossRef]
- Westman, S.M.; Kloth, K.J.; Hanson, J.; Kloth, K.J.; Hanson, J.; Ohlsson, A.B.; Albrectsen, B.R. Defence priming in Arabidopsis—A Meta-Analysis. Sci. Rep. 2019, 9, 13309. [Google Scholar] [CrossRef]
- Hatanaka, A. The biogeneration of green odour by green leaves. Phytochemistry 1993, 34, 1201–1218. [Google Scholar] [CrossRef]
- Matsui, K. Green leaf volatiles: Hydroperoxide lyase pathway of oxylipin metabolism. Curr. Opin. Plant Biol. 2006, 9, 274–280. [Google Scholar] [CrossRef]
- Zimmerman, D.C.; Coudron, C.A. Identification of traumatin, a wound hormone, as 12-oxo-trans-10-dodecenoic acid. Plant Physiol. 1979, 63, 536–541. [Google Scholar] [CrossRef]
- Kunishima, M.; Yamauchi, Y.; Mizutani, M.; Kuse, M.; Takikawa, H.; Sugimoto, Y. Identification of (Z)-3:(E)-2-hexenal isomerases essential to the production of the leaf aldehyde in plants. J. Biol. Chem. 2016, 291, 14023–14033. [Google Scholar] [CrossRef]
- Spyropoulou, E.A.; Dekker, H.L.; Steemers, L.; van Maarseveen, J.H.; de Koster, C.G.; Haring, M.A.; Schuurink, R.C.; Allmann, S. Identification and characterization of (3Z):(2E)-hexenal isomerases from cucumber. Front. Plant Sci. 2017, 8, 1342. [Google Scholar] [CrossRef]
- Matsui, K.; Sugimoto, K.; Mano, J.; Ozawa, R.; Takabayashi, J. Differential metabolism of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLoS ONE 2012, 7, e36433. [Google Scholar] [CrossRef] [PubMed]
- Engelberth, J.; Engelberth, M. Variability in the capacity to produce damage-induced aldehyde green leaf volatiles among different plant species provides novel insights into biosynthetic diversity. Plants 2020, 9, 213. [Google Scholar] [CrossRef] [PubMed]
- Engelberth, M.; Selman, S.M.; Engelberth, J. In-cold exposure to Z-3-hexenal provides protection against ongoing cold stress in Zea mays. Plants 2019, 8, 165. [Google Scholar] [CrossRef] [PubMed]
- Zebelo, S.A.; Matsui, K.; Ozawa, R.; Maffei, M.E. Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Sci. 2012, 196, 93–100. [Google Scholar] [CrossRef]
- Aratani, Y.; Uemura, T.; Hagihara, T.; Matsui, K.; Toyota, M. Green leaf volatile sensory calcium transduction in Arabidopsis. Nat. Commun. 2023, 14, 6236. [Google Scholar] [CrossRef]
- Cofer, T.M.; Erb, M.; Tumlinson, J.H. The Arabidopsis thaliana carboxylesterase AtCXE12 converts volatile (Z)-3-hexenyl acetate to (Z)-3-hexenol. bioRxiv 2023. [Google Scholar] [CrossRef]
- Tanarsuwongkul, S.; Fisher, K.W.; Mullis, B.T.; Negi, H.; Roberts, J.; Tomlin, F.; Wang, Q.; Stratmann, J.W. Green leaf volatiles co-opt proteins involved in molecular pattern signalling in plant cells. Plant Cell Environ. 2024, 47, 928–946. [Google Scholar] [CrossRef]
- Engelberth, J.; Contreras, C.F.; Dalvi, C.; Li, T.; Engelberth, M. Early Transcriptome Analyses of Z-3-Hexenol-Treated Zea mays Revealed Distinct Transcriptional Networks and Anti-Herbivore Defense Potential of Green Leaf Volatiles. PLoS ONE 2012, 8, e77465. [Google Scholar] [CrossRef]
- Röse, U.S.R.; Tumlinson, J.H. Systemic induction of volatile release in cotton: How specific is the signal to herbivory? Planta 2005, 222, 327–335. [Google Scholar] [CrossRef]
- Engelberth, J.; Alborn, H.T.; Schmelz, E.A.; Tumlinson, J.H. Airborne signals prime plants against herbivore attack. Proc. Natl. Acad. Sci. USA 2004, 101, 1781–1785. [Google Scholar] [CrossRef]
- Kessler, A.; Halitschke, R.; Diezel, C.; Baldwin, I.T. Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 2006, 148, 280–292. [Google Scholar] [CrossRef]
- Heil, M.; Bueno, J.C. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. USA 2007, 104, 5467–5472. [Google Scholar] [CrossRef]
- Frost, C.J.; Mescher, M.C.; Dervinis, C.; Davis, J.M.; Carlson, J.E.; De Moraes, C.M. Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol. 2008, 180, 722–734. [Google Scholar] [CrossRef]
- Laothawornkitkul, J.; Taylor, J.E.; Paul, N.D.; Hewitt, C.N. Biogenic volatiles organic compounds in the earth system. New Phytol. 2009, 183, 27–51. [Google Scholar] [CrossRef] [PubMed]
- Sarang, K.; Rudziński, K.J.; Szmigielski, R. Green Leaf Volatiles in the Atmosphere—Properties, Transformation, and Significance. Atmosphere 2021, 12, 1655. [Google Scholar] [CrossRef]
- Karl, T.; Fall, R.; Crutzent, P.J.; Jordan, A.; Lindinger, W. High concentrations of reactive biogenic VOCs at a high altitude in late autumn. Geophys. Res. Lett. 2001, 28, 507–510. [Google Scholar] [CrossRef]
- Jardine, K.J.; Chambers, J.Q.; Holm, J.; Jardine, A.B.; Fontes, C.G.; Zorzanelli, R.F.; Meyers, K.T.; Fernandez de Souza, V.; Garcia, S.; Giminez, B.O.; et al. Green leaf volatile emissions during high temperature and drought stress in a Central Amazon rainforest. Plants 2015, 4, 678–690. [Google Scholar] [CrossRef]
- Turan, S.; Kask, K.; Kanagendran, A.; Li, S.; Anni, R.; Talts, E.; Rasulov, B.; Kannaste, A.; Niinements, U. Lethal heat stress-dependent volatile emissions from tobacco leaves: What happens beyond the thermal edge? J. Exp. Bot. 2019, 70, 5017–5030. [Google Scholar] [CrossRef] [PubMed]
- Theocharis, A.; Clement, C.; Barka, E.A. Physiological and molecular changes in plant growth at low temperatures. Planta 2012, 235, 1091–1105. [Google Scholar] [CrossRef] [PubMed]
- Copolovici, L.; Kannaste, A.; Pazouki, L.; Niinemets, U. Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J. Plant Physiol. 2012, 169, 664–672. [Google Scholar] [CrossRef] [PubMed]
- Bray, E.A.; Bailey-Serres, J.; Weretilnyk, E. Response to abiotic stresses. In Biochemistry and Molecular Biology of Plants; Gruissem, W., Buchanan, B.B., Jones, R., Eds.; American Society of Plant Physiologists: Rockville, MA, USA, 2000; pp. 1158–1249. [Google Scholar]
- Cofer, T.M.; Engelberth, M.J.; Engelberth, J. Green leaf volatiles protect maize (Zea mays) seedlings against damage from cold stress. Plant Cell Environ. 2018, 41, 1673–1682. [Google Scholar] [CrossRef]
- Zhu, J.-K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 2002, 53, 247–273. [Google Scholar] [CrossRef]
- Cao, H.; Ding, R.; Kang, S.; Du, T.; Tong, L.; Zhang, Y.; Chen, J.; Shukla, M.K. Chapter 3—Drought, salt, and combined stresses in plants: Effects, tolerance mechanisms, and strategies. Adv. Agron. 2023, 178, 107–163. [Google Scholar]
- Catola, S.; Marino, G.; Emiliani, G.; Huseynova, T.; Musayev, M.; Akparov, Z.; Maserti, B.E. Physiological and metabolomic analysis of Punica granatum (L.) under drought stress. Planta 2016, 243, 441–449. [Google Scholar] [CrossRef] [PubMed]
- Yamauchi, Y.; Kunishima, M.; Mizutani, M.; Sugimotot, Y. Reactive short-chain leaf volatiles act as powerful inducers of abiotic stress-related gene expression. Sci. Rep. 2015, 5, 8030. [Google Scholar] [CrossRef]
- Tian, S.; Guo, R.; Zou, X.; Zhang, X.; Yu, X.; Zhan, Y.; Ci, D.; Wang, M.; Wang, Y.; Si, T. Priming with the green leaf volatile (Z)-3-hexeny-1-yl acetate enhances salinity stress tolerance in peanut (Arachis hypogaea L.) seedlings. Front. Plant Sci. 2019, 10, 785. [Google Scholar] [CrossRef] [PubMed]
- Hu, S.; Chen, Q.; Guo, F.; Wang, M.; Zhao, H.; Wang, Y.; Ni, D.; Wang, P. (Z)-3-hexen-1-ol accumulation enhances hyperosmotic stress tolerance in Camellia sinensis. Plant Mol. Biol. 2020, 103, 287–302. [Google Scholar] [CrossRef] [PubMed]
- Chen, K.; Li, G.-J.; Bressan, R.A.; Song, C.-P.; Zhu, J.-K.; Zhao, Y. Abscisic acid dynamics, signaling, and functions in plants. J. Int. Plant Biol. 2020, 62, 25–54. [Google Scholar] [CrossRef] [PubMed]
- Hayat, S.; Hayat, Q.; Alyemeni, M.N.; Wani, A.S.; Pichtel, J.; Ahmad, A. Role of proline under changing environments. Plant Signal. Behav. 2012, 7, 1456–1466. [Google Scholar] [CrossRef]
- Jin, J.; Zhao, M.; Jing, T.; Wang, J.; Lu, M.; Pan, Y.; Du, W.; Zhao, C.; Bao, Z.; Zhao, W.; et al. (Z)-3-hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants. Plant Physiol. 2023, 193, 1491–1507. [Google Scholar] [CrossRef]
- Charron, C.S.; Cantliffe, D.J.; Wheeler, R.M.; Manukian, A.; Heath, R.R. Photosynthetic photon flux, photoperiod, and temperature effects on emissions of (Z)-3-hexenal, (Z)-3-hexenol, and (Z)-3-hexenyl acetate from lettuce. J. Am. Soc. Hortic. Sci. 1996, 121, 488–494. [Google Scholar] [CrossRef]
- Mimuro, M.; Nishimura, Y.; Yamazaki, I.; Kobayashi, M.; Wang, Z.Y.; Nozawa, T.; Shimada, K.; Matsuura, K. Excitation energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus: A specific effect of 1-hexenol on the optical properties of baseplate and energy transfer processes. Photosynth. Res. 1996, 48, 263–270. [Google Scholar] [CrossRef] [PubMed]
- Tanaka, T.; Ikeda, A.; Shiojiri, K.; Ozawa, R.; Shiki, K.; Nagai-Kunihiro, N.; Fujita, K.; Sugimoto, K.; Yamato, K.T.; Dohra, H.; et al. Identification of a hexenal reductase that modulates the composition of green leaf volatiles. Plant Physiol. 2018, 178, 552–564. [Google Scholar] [CrossRef]
- Savchenko, T.; Yanykin, D.; Khorobrykh, A.; Terentyev, V.; Klimov, V.; Dehesh, K. The hydroperoxide lyase branch of the oxylipin pathway protects against photoinhibition of photosynthesis. Planta 2017, 245, 1179–1192. [Google Scholar] [CrossRef]
- Wang, M.H.; Rodriguez-Saona, C.; Lavoir, A.-V.; Ninkovic, V.; Shiojiri, K.; Takabayashi, J.; Han, P. Leveraging air-borne VOC-mediated plant defense priming to optimize Integrated Pest Management. J. Pest. Sci. 2024. [Google Scholar] [CrossRef]
- Hou, S.; Tsuda, K. Salicylic acid and jasmonic acid crosstalk in plants. Essays Biochem. 2022, 66, 647–656. [Google Scholar] [PubMed]
- Chamberlain, K.; Khan, Z.R.; Pickett, J.A.; Toshova, T.; Wadhams, L.J. Diel periodicity in the production of green leaf volatiles by wild and cultivated host plants of stemborer moths, Chilo partellus and Busseola fusca. J. Chem. Ecol. 2006, 32, 565–577. [Google Scholar] [CrossRef]
- Jardine, K.; Barron-Gafford, G.A.; Norman, J.P.; Abrell, L.; Monson, R.K.; Meyers, K.T.; Pavao-Zuckerman, M.; Dontsova, K.; Kleist, E.; Werner, C.; et al. Green leaf volatiles and oxygenated metabolite emission bursts from mesquite branches following light-dark transitions. Photosynth. Res. 2012, 113, 321–333. [Google Scholar] [CrossRef]
- Maurya, A.K.; Pazouki, L.; Frost, C.J. Primed seeds with indole and (Z)-3-hexenyl acetate enhances resistance against herbivores and stimulates growth. J. Chem. Ecol. 2022, 48, 441–454. [Google Scholar] [CrossRef]
- Engelberth, J.; Engelberth, M. The costs of green leaf volatile-induced defense priming: Temporal diversity in growth response to mechanical wounding and insect herbivory. Plants 2019, 8, 23. [Google Scholar] [CrossRef]
- Engelberth, J. Primed to growth: A new role for green leaf volatiles in plant stress responses. Plant Signal. Behav. 2020, 15, 1701240. [Google Scholar] [CrossRef]
Stress | Organism | Active Compound | Responses | Citation |
---|---|---|---|---|
Cold stress | Zea mays | Z-3-hexenal Z-3-hexenol | Abiotic stress genes Reduced ion leakage Reduced damage | [12,31] |
Drought | Arabidopsis thaliana | E-2-hexenal | Abiotic stress genes | [35] |
Arachis hypogaea | Z-3-hexenyl acetate | Photosynthesis Increased water content Growth Antioxidant proteins | [36] | |
Camellia sinensis | Z-3-hexenol | Stomatal conductance Reduced lipid peroxidation ABA accumulation Proline accumulation Stress gene expression | [37] | |
Camellia sinensis | Z-3-hexenol | ABA glycosyl transferase ABA storage | [40] | |
Photosynthesis | Chloroflexus auratiacus | 1-hexanal | Reduced energy flux | [42] |
Arabidopsis thaliana | E-2-hexenal Z-3-hexenal E-2-hexenol | Reduction in photosynthetic activity | [10,43] | |
Arabidopsis thaliana | E-2-hexenal Z-3-hexenal Z-3-hexenyl acetate | Protection of PSII Recovery Reduced protein degradation | [44] |
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Engelberth, J. Green Leaf Volatiles: A New Player in the Protection against Abiotic Stresses? Int. J. Mol. Sci. 2024, 25, 9471. https://doi.org/10.3390/ijms25179471
Engelberth J. Green Leaf Volatiles: A New Player in the Protection against Abiotic Stresses? International Journal of Molecular Sciences. 2024; 25(17):9471. https://doi.org/10.3390/ijms25179471
Chicago/Turabian StyleEngelberth, Jurgen. 2024. "Green Leaf Volatiles: A New Player in the Protection against Abiotic Stresses?" International Journal of Molecular Sciences 25, no. 17: 9471. https://doi.org/10.3390/ijms25179471