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ISSN : 1598-5504(Print)
ISSN : 2383-8272(Online)
Journal of Agriculture & Life Science Vol.53 No.3 pp.17-26
DOI : https://doi.org/10.14397/jals.2019.53.3.17

Resistance of Terpenoids to Various Abiotic Stresses in Chamaecyparis obtusa

JJi Yun Min1, Dong Jin Park3, Seong Hyeon Yong1, Woo Hyeong Yang1, Yuwon Seol1, Eunji Choi1, Hak Gon Kim4, Myung Suk Choi1,2*
1Division of Environmental Forest Science, Gyeongsang National University, Jinju, 52828, Korea
2Institute of Agriculture of Life Science, Gyeongsang National University, Jinju, 52828, Korea
3Department of Seed and Seedling Management, National Forest Seed and Variety Center, Chungju, 27495, Korea
4Forest Research Department, Gyeongsangnam-do Forest Environment Research Institute, Jinju, 52615, Korea
Corresponding author: Myung Suk Choi Tel: +82-55-772-1856 Fax: +82-55-772-1859 E-mail: mschoi@gnu.ac.kr
January 18, 2019 March 4, 2019 March 20, 2019

Abstract


Chamaecyparis obtusa is one of the economical conifers planted in Korea due to its good quality timber and wood characteristics. Individuals of C. obtusa containing high terpenes (HT) and low terpenes (LT) were selected for by colorimetric method. The HT of C. obtusa was delayed in wilting against various abiotic stresses compared to the LT plants. The HT group exposed to UV did not significant influence the chlorophyll content, and the chlorophyll value was higher in the HT group than the LT group. Also, chilling treatment (5°C) did not significant influence on the chlorophyll content. However treatment at -4°C showed relatively low chlorophyll content in the LT group than the HT group. Plants exposure to high temperature was not a difference between the HT and the LT group. However, treatment at 38°C influenced the chlorophyll content that was increased exposure time-dependently. In salt treatments, chlorophyll in the HT group was lower at high concentrations (300 and 500 mM) of NaCl. However, chlorophyll content increased to slightly in treatment time-dependently, which is 6.7% to 40%. H2O2 treatment has been a negative effect on the chlorophyll content in the HT group. All concentration of H2O2 decreased the chlorophyll content of 5% to 35%. Plants containing high terpenoids were resisted against some abiotic stress such as salt and H2O2. Our results implied that terpenoids could cause various abiotic stress resistance. These results could be utilized for efficient management and biomass production during forest silvicultures.



초록


    National Research Foundation of Korea
    2017R1D1A1B04036320

    Introduction

    Chamaecyparis obtusa that naturally distributed in Japan is planted in the southern and coastal islands of Korea. It is an evergreen coniferous tree that can reach 45 m in height and 2 m in diameter at breast height. It was introduced in Korea in 1924 and has been planted as a major planting species in Jeonnam and Gyeongsangnam-do regions and has been cultivated as a windbreak forest in Jeju Island (Kim, 2002). It is a popular decorative tree in Japan's parks and gardens and other areas of temperate climates, including Western Europe and North America. Dwarf, yellow and bumpy leaves have been selected varieties. In Korea, it is one of the economical conifers to produce excellent trait timber (Maruyama et al., 2005).

    Abiotic and biological stresses cause significant loss of biomass productivity worldwide. Plant stress responses are regulated by multiple signaling pathways (Knighy & Knighy, 2001) and are superimposed on gene expression patterns induced in response to different stresses (Singh et al., 2002). The main component of C. obtusa is terpenoid. Terpene metabolites are involved in a variety of ecological and physiological functions based on the differential expression profile of the terpene synthase gene observed through response to plant development and biological and abiotic environmental factors.

    Biological and abiotic environmental factors have a particularly large impact on volatiles emitted from plant parts of plants. Non-biotic stressers are caused by the concentration of too many other metabolites in which can affect volatile compounds. As a generalization, stress increases the release of volatile compounds (Holopainen & Gershenzon, 2010). Abiotic stress affects primary and secondary metabolism in a variety of ways. Stress generally inhibits photosynthesis by reducing CO2 uptake and diffusion within the leaf to the fixation site to carbon dioxide, or by altering the photochemical or biochemical reaction of photosynthesis cycles (Flexas et al., 2004).

    Emissions are biosynthetically controlled by nonbiological factors such as light and/or temperature, atmospheric carbon dioxide concentration or nutrition (Holopainen & Gershenzon, 2010). Climate change is evidenced by changes in forest policy and species. Planting of C. obtusa is rapidly increasing in Korea. However, despite the rapid increase in the cultivation area of C. obtusa, there is no data on the physiological changes of C. obtusa. The aim of this study was to select terpenoid high and low C. obtusa plants, evaluate the chlorophyll content between these two groups and evaluate their resistance to various abiotic stresses (UV, temperature, salt and hydrogen peroxide).

    Materials and Methods

    1 Plant material

    In order to determine resistance against various abiotic stress, about 300 seedlings of 1-year-old C. obtusa were obtained from a tree nursery located at, Geumsan-myeon, Jinju, Korea. Seedlings were planted in a pot (diameter: 16 cm, bottom diameter: 11 cm, height: 17 cm), and the soil used was peat moss: pearlite: vermiculite (1 : 1 : 1, v / v). The plants were not fertilized until the experiment and were irrigated every 3 days. For the experiment, the seedlings were used for the experiment after 2 months in the growth room of 25°C in 16 hours light and 8 hours dark.

    2 Establishment of colorimetric method

    The colorimetric method of essential oil was performed by Plant Drug analysis (Blandt et al., 1984). Terpinyl acetate, Limonene, Decene, Bornyl acetate, ρ-Cymene, and 2-Carene were mixed at 1 mM each in order to observe the difference in color intensity according to the concentration of terpene.

    The terpene standard compounds were again mixed with the VS solution (Blandt et al., 1984) and allowed to react for 5 minutes at room temperature. The mixture was then dried at 80℃ for 3 minutes immediately after dropping on the TLC plate. To rapidly screen for terpenoid high contiaining tree, 1-year-old C. obtusa leaves (1 g) were homogenized and extracted with 3 mL of acetic acid for 5 minutes. Add 10 μL of VS Solution I (5% Ethanolic Sulfuric Acid) and dry at 110℃ for 5 minutes. Finally, 10 μL of VS Solution II (1% ethanol vanillin) was added and the extract was filtered (filter paper, 2 times, Advantec). 2 μL l of the filtrate was dropped on the TLC plate and dried at 80℃ for 3 minutes for visual observation. Chemicals were purchased pure grade from Sigma Aldrich Co. (USA).

    3 Selection of terpene high and low containing individuals

    Approximately 1 year old 300 seedings were selected using the colorimetric method described above. Based on the degree of colorimetric response, terpene high and low - containing individuals were classified and used for various stress tests.

    4 Treatment of various abiotic stress

    Abiotic stress treated as UV, cold, heat, salt and hydrogen peroxide, respectively. A mercury lamp (HPQ 125W, Philips, Eindhoven, Netherlands) with characteristic emission in the range of 320 nm was used as a UV-B radiation source to illuminate the response of plants by UV irradiation. The HT and LT group seedlings were treated for 2 days under HPQ lamps for 5 days. The distance between the lamp and the plant was 25cm. For the UV-B irradiation treatment, a cellulose acetate filter (φ13 mm) was used to block radiation below 280 nm. The response of plants to UV stress was examined through chlorophyll content measurements.

    Plant response was investigated by chilling treatment. HT group and LT group seedlings were grown for 24 hours at 25℃, 5℃ and -4℃, respectively. Chlorophyll contents of leaves located 2 cm below the top of the plant exposed to low temperature were examined at 6 hrs intervals.

    Individual response against heat stress was investigated through measurements of chlorophyll content. The HT and LT groups did expose to temperature with 25℃ (control), 38℃ and 45℃ for 8 hr, and the chlorophyll of leaf investigated at 2 hr interval. In this experiment, leaves of C. obtusa were dried and broken after 8 hr of heat treatment.

    To investigate the response of plants to salt, we used various concentrations of sodium chloride (0, 60, 120 and 240 mM). The HT and LT plant pots were irrigated at 3 days intervals with filtered water for up to 6 weeks. Homogeneous plants were divided into four groups and treated with 0, 100, 300 and 500 mM NaCl treatment irrigated 3 days interval by the addition of sodium chloride to water (250 ml/day). To prevent the increase of osmotic pressure due to the accumulation of salt due to the continuation of the irrigation process, each pot was flushed with 500 ml of filtrate before irrigation with saline for 1 week. Chlorophyll was examined at intervals of 2 days for 7 days.

    To investigate the response of plants to oxidative stress, HT and LT plants were grown in a growth chamber under a cool fluorescent white (Philips, 20W) light of 52 μmol m-2 s-1 (PAR). Two months later, the primary leaves of the plants were placed in various concentrations of H2O2 (0, 50, 100, 300 and 500 ppm) and incubated in the dark for 6 hours at 25℃. The primary leaves were then washed three times twice with H2O and used for chlorophyll analysis. Chlorophyll was detected at intervals of 2 days for 7 days.

    5 Determination of chlorophyll content

    To determine the tolerance of various abiotic stresses, chlorophyll content was measured from leaf samples collected at each treatment time from plants grown under light. Chlorophyll content was measured using portable SPAD-502 plus (Konica Minolta, Japan). The average of three readings obtained from the SPAD was obtained from each leaf.

    6 Statistical analysis

    Data The experiments were repeated for a minimum of three times. Data was subjected to statistical analysis by using SAS for Windows Version (Ver. 6.12, SAS Institute Inc., Cary, NC, USA).

    Results and Discussion

    1 Selection of individual for high and low terpene content

    Terpenes form dark colored complexes when treated with color reagents. C. obtusa leaf extract reacted with VS solution and appeared brown. There was a difference in intensity of color depending on each individual. The intensity of color of the terpene standard and VS solution reactants increased in proportion to the concentration of terpene (Fig. 1, 2). HT and LT were screened according to the colorimetric method as the primary selection method (Fig. 2). The results showed that the color intensity from the VS solution was variable. Therefore, it was divided into HT and LT groups according to the intensity of color.

    2 Response against UV stress

    UV treatment affected the chlorophyll content of the C. obtusa trees (Fig. 3). The contents of chlorophyll in ultraviolet treated leaves were slightly different in terpene high and low-containing plant leaves. Chlorophyll content was slightly higher in HT group than in LT group. However, chlorophyll content in HT group did not show any significant difference with time. Kaewsuksaeng et al. (2011) reported that the chlorophyll content of citrus treated with UV-B was higher than that of the control (no ultraviolet light) for 30 days at 25℃or not treated with UV-B.

    In natural conditions plants are continuously exposed to environmental stresses, one such inevitable stress factor is the exposure to UV-B (280-320 nm) radiation (Dolzhenko et al., 2010). The impact of UV-B radiation on terpenes seems to indicate a stimulation of their biosynthesis and emission. A more recent study again showed increased isoprene emission rate of subarctic peatlands when irradiated with increasing levels of UV-B radiation and explained the rising emission as a consequence of oxidative damage to membranes and to the induction of the terpene defensive antioxidant pathway. UV damage to cellular structure may also induce emission of other volatile compounds (Loreto & Velikova, 2001;Tiiva et al., 2007).

    3 Response against cold stress

    The effect of low temperature stress on the chlorophyll content of C. obtusa leaves is shown in Fig. 4. As a result, the chlorophyll content was not changed in the HT plant group at low temperature treatments time and time, but the LT plant group affected. Mean chlorophyll content was higher in the HT group than the LT group. These results indicate that HT trees showed stronger resistance to temperatures than LT trees. In previous studies, plants exposed at 4℃ did not affect the chlorophyll content of pea plants (Georgieva & Lichtenthaler, 1999). Low temperatures are one of the major environmental factors that affect plant growth and development and greatly limit the spatial distribution of plants and agricultural productivity (Feng et al., 2009). Many plant species are susceptible to sequential adaptation mechanisms due to low temperature exposure and may increase cold tolerance. Adherence to low temperatures is accompanied by biochemical, structural, and physiological changes (Thomashow, 2002). Low temperature treatment further increases volatile emissions from green leaves, presumably leading to widespread destruction of the sesquiterpene containing structures at low temperatures (Copolovici et al., 2012). Cold adaptation of plants requires regulation of many other genes, particularly genes that ultimately contribute to the increased stability of the plasma membrane during cold stress (Breton et al., 2000).

    4 Response against heat stress

    The chlorophyll content was investigated by high temperature treatment (Fig. 5). It is shown that there were no significant differences between HT and LT group exposed to high temperature. The chlorophyll content of the HT plant group varied with the treatment temperature, but there was no change with time. On the other hand, the chlorophyll content in the LT plant group was different according to the treatment temperature and treatment time (Fig. 5). However, there was no significant difference in mean chlorophyll value between HT and LT groups. Temperature affects the evaporation and release of volatile compounds that leach out of the impermeable cell layer (Kesselmeier & Staudt, 1999). In another study, temperature treatment at 35°C did not change chlorophyll fluorescence parameters and reported a slight increase in chlorophyll content in pea plants (Georgieva & Lichtenthaler, 1999).

    High temperatures are generally associated with drought stress and therefore affect plant growth. Plants are an important mechanism to dissociate latent heat through the evaporation of water and to separate temperature and leaf temperatures (Loreto & Schnitzler, 2010). Temperature has a powerful and immediate effect on the activity of enzymes that catalyze the synthesis of many volatile compounds. Thus, the main effect of temperature rise is a direct increase in terpene formed through the enzymatic reaction. There is no study on the relationship between heat and terpene biosynthesis.

    When heat stress occurs (around 40-45°C for enzymes in the MEP pathway), then is observed a very rapid inhibition of terpene emission (Loreto et al., 2006). Copolovici et al. (2012) reported that even a moderate heat shock at 37℃ strongly reduced assimilation rate. Heat shock treatment of the cotton plants resulted in polyamine accumulation in leaves and a transient acceleration of ethylene evolution (Kuznetsov et al., 1991). Kumar-Tewari & Charan- Tripathy (1998) showed that chlorophyll biosynthesis of cucumber seedlings was inhibited by 90% and 60%, respectively, under low temperature and heat stress, and inhibition of chlorophyll biosynthesis was higher at lower temperatures. Previous studies have demonstrated that monoterpenes enhance plant heat stress resistance (Copolovici et al., 2005;Llusiá et al., 2005), and heat exposure has shown to enhance terpene emissions (Vickers et al., 2009).

    5 Response against salt stress

    The chlorophyll content of the leaves of C. obtusa was examined by salt treatment (Fig. 6). In the HT group, the rophyll content was not significantly different from salt treatments but in the LT group, plants that treated with NaCl showed a large change in the chlorophyll content. In the LT group, 100 mM salt treatment reduced the chlorophyll content by 28.5%. The average content of chlorophyll was higher in the HT group than in the LT group.

    Salt stress induced a reduction of the number of chloroplasts (Marchner & Possingham, 1975). In conclusion, the present investigation shows that the induced decrease of chlorophyll content in severely NaCl stressed leaves, and therefore limitations of chlorophyll synthesis.

    Sunflower exposure to salt stress has been reported to be more severe necrotic syndrome than osmotic stress exposure, due to salt toxicity (Andrade & Santos, 2003). However, there was no definite study of the independent involvement of salt stress in chlorophyll metabolism (Santos, 2004). The release of volatile compounds such as terpene has a great impact on drought and salt. These abiotic stresses directly affect stomatal conductance and cause diffusion and biochemical restriction of photosynthesis (Fall et al., 1999). Reduction of photosynthesis and pore closure are expected to have a negative impact on the release of volatile compounds by altering the carbon supply to the MEP pathway and by increasing their resistance to release (Loreto & Schnitzler, 2010).

    6 Response against hydrogen peroxide induced oxidative stress

    The effect of hydrogen peroxide treatment on chlorophyll content was investigated (Fig. 6). HT plant group was not affected by concentration and time of hydrogen peroxide treatment. However, the chlorophyll content of LT plant group decreased with increasing treatment time. However, treatment of H2O2 in the LT group was not significantly different between the treated concentrations Fig. 7

    Plants require oxygen for energy generation and survival. However, during redox processes such and photosynthesis in chloroplasts or oxidation-phosphorylation in mitochondria, Reactive oxygen species (ROS) including superoxide anion radical (O2), hydrogen peroxide (H2O2), and hydroxyl radical (OH) are frequently generated (Bolwell & Wojtaszek, 1997). Also, oxidative stress is a common physiological stress that often challenges plants. (ROS) are major factors in oxidative stress that significantly affect plant cell growth and secondary metabolism (Zhao et al., 2005).

    Plants produce a variety of responses such as antioxidant system activation, hypersensitive cell death, and defense gene activation against oxidative stress (Lavine et al., 1994;Vranová et al., 2002). The relationship between ROS and secondary metabolites has been studied for a long time because plant secondary metabolites are usually orientation related substances. Zhao & Sakai (2003) suggested that H2O2- mediated activation of Jasmonic acid-biosynthesis enzymes and increased production of β-thujaplicin could be achieved. However, further investigation is needed to determine whether H2O2 affects biosynthesis of chlorophyll.

    In conclusion, plant responses to various stress treatments did not show any differences between The HT and LT groups. However, the HT group resisted abiotic stresses such as salt and heat shocks. These results showed that terpene stress resistance in plants. Although the physiological and biochemical basis for resistance induced by abiotic stress is not clearly understood, it is believed that terpene containing plants, including plants, provide a variety of stress tolerance. Further research is needed to reveal physiological and biochemical mechanisms by which terpenes induce tolerance to a variety of other environmental stresses. In addition, research is needed to reveal protein and gene related stress resistance. These results could be used for effective management and biomass production in deforestation.

    Acknowledgements

    This work was supported by the Basic Science and Engineering Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry if education (2017R1D1A1B04036320).

    Figure

    JALS-53-3-17_F1.gif

    Quantitative Correlation by the colorimetric reaction of the terepene standard and VS solution reactants.

    JALS-53-3-17_F2.gif

    Selection of high and low terpenes containing group by colorimetric method.

    JALS-53-3-17_F3.gif

    Changes in the chlorophyll content of C. obtusa after UV treatment. A: High-terpenes containing group (HT) and B: Low-terpenes containing group (LT).

    JALS-53-3-17_F4.gif

    SPAD chlorophyll contents of C. obtusa leaves by cold stress treatement. A: High-terpenes containing group (HT), B: Low-terpenes containing group (LT).

    JALS-53-3-17_F5.gif

    SPAD chlorophyll contents of C. obtusa leaves by heat stress treatement. A: High- terpenes containing group (HT), B: Low-terpenes containing group (LT).

    JALS-53-3-17_F6.gif

    SPAD chlorophyll contents of C. obtusa leaves by salt (NaCl) stress treatement. A: High-terpenes containing group (HT), B: Low-terpenes containing group (LT).

    JALS-53-3-17_F7.gif

    SPAD chlorophyll contents of C. obtusa leaves by hydrogen peroxide (H2O2) stress treatment. A: Highterpenes containing group (HT), B: Low-terpenes containing group (LT).

    Table

    Reference

    1. Andrade S and Santos C. 2003. The effects of salt and osmotic stresses on carbohydrate metabolism. I. Symposium on insular ecosystems. Book of Abstracts. Porto Santo, Portugal.
    2. Blandt S , Wagner H and Zgainski EM. 1984. Plant Drug Analysis: A Thin Layer Chromatography Atlas. pp.384. Eds. Springer. NY. USA.
    3. Bolwell GP and Wojtaszek P. 1997. Mechanism for the generation of reactive oxygen species in plant defence - a broad perspective. Physiol. Mol. Plant Pathol. 51: 347-366.
    4. Breton G , Danyluk J , Ouellet F and Sarhan F. 2000. Biotechnological applications of plant freezing associated proteins. Biotechnol Annu Rev. 6: 59-101.
    5. Copolovici L , Kännaste A , Pazouki L and Niinemets U. 2012. 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. 169: 664-672.
    6. Copolovici LO , Filella I , Llusiá J , Niinemets U and Peñuelas J. 2005. The capacity for thermal protection of photosynthetic electron transport varies for different monoterpenes in Quercus ilex. Plant Physiol. 139: 485-496.
    7. Dolzhenko Y , Bertea CM , Occhipinti A , Bossi S and Maftei ME. 2010. UV-B modulates the interplay between terpenoids and flavonoids in peppermint (Mentha x piperita L.). J. Photochem. Photobiol. B. Biol. 100: 67-75.
    8. Fall R , Karl T , Hansel A , Jordan A and Lindinger W. 1999. Volatile organic compounds emitted after leaf wounding: On-line analysis by proton-transferreaction mass spectrometry. J. Geophys. Res. Atmos. 104: 15963-15974.
    9. Feng DR , Liu B , Li WY , He YM , Qi KB , Wang HB and Wang JF. 2009. Over-expression of coldinduced plasma membrane protein gene (MpRCI) from plantain enhances low temperature-resistance in transgenic tobacco. Environ. Exp. Bot. 65: 395-402.
    10. Flexas J , Bota J , Loreto F , Cornic G and Sharkey TD. 2004. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol (Stuttg). 6: 269-279.
    11. Georgieva K and Lichtenthaler HK. 1999. Photosynthetic activity and acclimation ability of pea plants to low and high temperature treatment as studied by means of chlorophyll fluorescence. J. Plant Physiol. 155: 416-423.
    12. Holopainen JK and Gershenzon J. 2010. Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 15: 176-184.
    13. Koewsuksaeng S , Vrano Y , Aiamla-or S , Shigyo M and Yamauchi N. 2011. Ettect of UV-B irradiation on Chlorophyll-degrading enzyme activities and postharvest quality in stored lime (Citrus latitalia Tan.) trait. Postharrest Biol. Technol. 61: 124-130.
    14. Kesselmeier J and Staudt M. 1999. Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J. Atmos. Chem. 33: 23-88.
    15. Kim TU. 2002. The woody plants of Korea. pp.38. eds. Kyo-Hak Publishing Co. JJ. KOR.
    16. Knighy H and Knight MR. 2001. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci. 6: 262-267.
    17. Kumar-Tewari A and Charan-Tripathy B. 1998. Temperature-stress-induced impairment of chlorophyll biosynthetic reaction in cucumber and wheat. Plant Physiol. 117: 851-858.
    18. Kuznetsov VV , Khydyrov BT , Shevyakova NI and Rakitin VY. 1991. Heat shock induction by of salt tolerance in cotton - involvement of polyamines, ethylene, and proline. Soviet Plant Physiol. 38: 1203-1210.
    19. Lavine A , Tenhaken R , Dixon R and Lamb C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 79: 583-593.
    20. Llusiá J , Peñuelas J , Asensio D and Munné-Bosch S. 2005. Airborne limonene confers limited thermotolerance to Quercus ilex. Physiol. Plant. 123: 40-48.
    21. Loreto F and Schnitzler JP. 2010. Abiotic stress and induced BVOCs. Trends Plant Sci. 15: 154-166.
    22. Loreto F and Velikova V. 2001. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol. 127: 1781-1787.
    23. Loreto F , Barta C , Brilli F and Nogues I. 2006. On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant Cell Environ. 29: 1820-1828.
    24. Marchner H and Possingham JV. 1975. Effects of K and Na on the growth of leaf discs of sugar beet and spinach. Z. Pflanzenphysiol. 75: 6-16.
    25. Maruyama E , Ishii K and Hosoi Y. 2005. Efficient plant regeneration of Hinoki cypress (Chamaecyparis obtusa) via somatic embryogenesis. J. For. Res. 10: 73-77.
    26. Santos CV. 2004. Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci. Hortic. 103: 93-99.
    27. Singh K , Foley RC and Oñate-Sánchez L. 2002. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 5: 430-436.
    28. Thomashow MF. 2002. So what’s new in the field of plant cold acclimation? Lots! Plant Physiol. 125: 89-93.
    29. Tiiva P , Rinnan R , Faubert P , Räsänen J , Holopainen T , Kyrö E and Holopainen JK. 2007. Isoprene emission from a subarctic peatland under enhanced UV-B radiation. New Phytol. 176: 346-355.
    30. Vickers CE , Gershenzon J , Lerdau MT and Loreto F. 2009. A unified mechanism of action for volatile isoprenoids in plant atiotic stress. Nat. Chem. Biol. 5: 283-291.
    31. Vranová E , Inzé D and Van Breusegem F. 2002. Signal transduction during oxidative stress. J. Exp. Bot. 53: 1227-1236.
    32. Zhao J and Sakai K. 2003. Multiple signalling pathways mediate fungal elicitor-induced betathujaplicin biosynthesis in Cupressus lusitanica cell cultures. J. Exp. Bot. 54: 647-656.
    33. Zhao J , Fujita K and Sakai K. 2005. Oxidative stress in plant cell culture: a role in production of β-thujaplicin by Cupressus lusitanica suspension culture. Biotechnol. Bioeng. 90: 621-631.
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