Differential Anthocyanin Concentrations and Expression of Anthocyanin Biosynthesis Genes in Strawberry ‘Sachinoka’ during Fruit Ripening under High-temperature Stress

We investigated anthocyanin concentration and the expression of anthocyanin biosynthesis related genes in strawberry ‘Sachinoka’ (Fragaria×ananassa Duch.) grown at control regime (20/15°C, 14/10 h, day/night) or high temperature regime (30/15°C, 14/10 h). In Experiment 1, fruits were harvested at di...

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Published inEnvironment control in biology Vol. 56; no. 1; pp. 1 - 6
Main Authors OKUTSU, Keisuke, IKEDA, Takashi, MATSUSHITA, Kohei
Format Journal Article
LanguageEnglish
Published Fukuoka Japanese Society of Agricultural, Biological and Environmental Engineers and Scientists 2018
Japan Science and Technology Agency
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Online AccessGet full text
ISSN1880-554X
1883-0986
DOI10.2525/ecb.56.1

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Abstract We investigated anthocyanin concentration and the expression of anthocyanin biosynthesis related genes in strawberry ‘Sachinoka’ (Fragaria×ananassa Duch.) grown at control regime (20/15°C, 14/10 h, day/night) or high temperature regime (30/15°C, 14/10 h). In Experiment 1, fruits were harvested at different color stages. In the control treatment, the anthocyanin concentration increased as fruit ripened, and was highest at the fully ripe stage. In the high-temperature treatment, however, it was significantly lower at the fully ripe stage. These results were relevant with the peak value of expression of anthocyanin biosynthesis genes which was inhibited in fruits grow at high temperature regime. In Experiment 2, we applied high temperature at different fruit color stages to test the effect of the timing of high temperature stress on coloring. When exposed fruit to high temperature after half ripe stage, the anthocyanin concentration and gene expression in fully ripe fruit were not significantly different from the control. But in fruit exposed before half ripe stage, the anthocyanin concentration and gene expression significantly reduced. These results indicate that the level of gene expression of anthocyanin biosynthesis is affected by the timing of exposure fruit to high temperature stress.
AbstractList We investigated anthocyanin concentration and the expression of anthocyanin biosynthesis related genes in strawberry ‘Sachinoka’ (Fragaria×ananassa Duch.) grown at control regime (20/15°C, 14/10 h, day/night) or high temperature regime (30/15°C, 14/10 h). In Experiment 1, fruits were harvested at different color stages. In the control treatment, the anthocyanin concentration increased as fruit ripened, and was highest at the fully ripe stage. In the high-temperature treatment, however, it was significantly lower at the fully ripe stage. These results were relevant with the peak value of expression of anthocyanin biosynthesis genes which was inhibited in fruits grow at high temperature regime. In Experiment 2, we applied high temperature at different fruit color stages to test the effect of the timing of high temperature stress on coloring. When exposed fruit to high temperature after half ripe stage, the anthocyanin concentration and gene expression in fully ripe fruit were not significantly different from the control. But in fruit exposed before half ripe stage, the anthocyanin concentration and gene expression significantly reduced. These results indicate that the level of gene expression of anthocyanin biosynthesis is affected by the timing of exposure fruit to high temperature stress.
Author OKUTSU, Keisuke
IKEDA, Takashi
MATSUSHITA, Kohei
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Cites_doi 10.1016/j.abb.2007.04.040
10.1007/s10535-015-0548-4
10.1016/S0168-9452(02)00417-X
10.1111/j.1365-3040.2011.02316.x
10.1186/1471-2229-6-27
10.1111/nph.12017
10.1016/j.plantsci.2011.04.012
10.1046/j.1365-313X.2001.01154.x
10.1038/nprot.2008.73
10.1016/j.plantsci.2004.03.021
10.1007/s00425-012-1650-x
10.2525/ecb.49.209
10.2525/ecb.54.101
10.1093/jxb/erm055
10.5344/ajev.2006.57.1.54
10.1007/BF00019111
10.1007/s00425-007-0598-8
10.2525/ecb1963.42.21
10.1093/jxb/ert377
10.1016/0304-4238(90)90082-P
10.2503/jjshs1.78.387
10.1007/s00425-014-2228-6
10.1016/j.tplants.2013.06.003
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Kadomura-Ishikawa, Y., Miyawaki, K., Takahashi, A., Masuda, T., Noji, S. 2015b. RNAi-mediated silencing and overexpression of the FaMYB1 gene and its effect on anthocyanin accumulation in strawberry fruit. Biol. Plantarum 59: 677–685.
Dela, G., Or, E., Ovadia, R., Nissim-Levi, A., Weiss, D., Oren-Shamir, M. 2003. Changes in anthocyanin concentration and composition in ‘Jaguar’ rose flowers due to transient high air temperature conditions. Plant Sci. 164: 333–340.
Matsushita, K., Sakayori, T., Ikeda, T. 2016. The effect of high air temperature on anthocyanin concentration and the expressions of its biosynthetic genes in strawberry ‘Sachinoka’. Environ. Control Biol. 54: 101–107.
Jaakola, L. 2013. New insights into the regulation of anthocyanin biosynthesis in fruits. Trends. Plant Sci. 18: 477–483.
Mori, K., Sugaya, S., Gemma, H. 2004. Regulatory mechanism of anthocyanin biosynthesis in ‘Kyoho’ grape berries grown under different temperature conditions. Environ. Control Biol. 42: 21–30.
Medina-Puche, L., Cumplido-Laso, G., Amil-Ruiz, F., Hoffmann, T., Ring, L., Rodríguez-Franco, A., Caballero, J. L., Schwab, W., Muñoz-Blanco, J., Blanco-Portales, R. 2014. MYB10 plays a major role in the regulation of flavonoid/ phenylpropanoid metabolism during ripening of Fragaria× ananassa fruits. J. Exp. Bot. 65: 401–417.
Yamane, T., Jeong, S. T., Goto-Yamamoto, N., Koshita, Y., Kobayashi, S. 2006. Effect of temperature on anthocyanin biosynthesis in grape berry skins. Am. J. Enol. Vitic. 57: 54–59.
Schaart, J. G., Dubos, C., De La Fuente, I. R., Van Houwelingen, A. M. M. L., de Vos, R. C. H., Jonker, H. H., Xu, W., Routaboul, J. M., Lepiniec, L., Bovy, A. G. 2013. Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria×ananassa) fruits. New. Phytol. 197: 454–467.
Azuma, A., Yakushiji, H., Koshita, Y., Kobayashi, S. 2012. Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 236: 1067–1080.
Jeong, S. T., Goto-Yamamoto, N., Kobayashi, S., Esaka, M. 2004. Effects of plant hormones and shading on the accumulation anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Sci. 167: 247–252.
Saure, M. C. 1990. External control of anthocyanin formation in apple. Sci. Hortic. 42: 181–218.
Pombo, M. A., Martínez, G. A., Civello, P. M. 2011. Cloning of FaPAL6 gene from strawberry fruit and characterization of its expression and enzymatic activity in two cultivars with different anthocyanin accumulation. Plant Sci. 181: 111–118.
Lin-Wang, K., Micheletti, D., Palmer, J., Volz, R., Lozano, L., Espley, R., Hellens, R. P., Chagne, D., Rowan, D. D., Troggio, M., Iglesias, I., Allan, A. C. 2011. High air temperature reduces apple fruit color via modulation of the anthocyanin regulatory complex. Plant Cell Environ. 34: 1176–1190.
Castellarin, S. D., Matthews, M. A., Di Gaspero, G., Gambetta, G. A. 2007. Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 227: 101–112.
Ikeda, T., Matsushita, K., Oyaizu, Y., Okutsu, K. 2016. Different expressions of anthocyanin biosynthetic genes for strawberry ‘Sachinoka’ fruits under water and high temperature stresses. 8th International Strawberry Symposium 2016, Quebec City, Canada. Book of Abstracts: 144.
Kobayashi, S. 2009. Regulation of anthocyanin biosynthesis in grapes. J. Jpn. Soc. Hortic. Sci. 78: 387–393.
Reid, K. E., Olsson, N., Schlosser, J., Peng, F., Lund, S. T. 2006. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol. 6: 27.
Kadomura-Ishikawa, Y., Miyawaki, K., Takahashi, A., Masuda, T., Noji, S. 2015a. Light and abscisic acid independently regulated FaMYB10 in Fragaria×ananassa fruit. Planta 241: 953–965.
Almeida, J. R. M., D’Amico, E., Preuss, A., Carbone, F., De Vos, R. C. H., Deiml, B., Mourgues, F., Perrotta, G., Fischer, T. C., Bovy, A. G., Martens, S., Rosati, C. 2007. Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria×ananassa). Arch. Biochem. Biophys. 465: 61–71.
Boss, P. K., Davies, C., Robinson, S. P. 1996. Expression of anthocyanin biosynthesis pathway genes in red and white grapes. Plant Mol. Biol. 32: 565–569.
Mori, K., Goto-Yamamoto, N., Kitayama, M., Hashizume, K. 2007. Loss of anthocyanins in red-wine grape under high air temperature. J. Exp. Bot. 58: 1935–1945.
Schmittgen, T. D., Livak, K. J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3: 1101–1108.
Ikeda, T., Suzuki, N., Nakayama, M., Kawakami, Y. 2011. The effects of high air temperature and water stress on fruit growth and anthocyanin concentration of pot-grown strawberry (Fragaria×ananassa Duch. cv. ‘Sachinoka’) plants. Environ. Control Biol. 49: 209–215.
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References_xml – reference: Castellarin, S. D., Matthews, M. A., Di Gaspero, G., Gambetta, G. A. 2007. Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 227: 101–112.
– reference: Kadomura-Ishikawa, Y., Miyawaki, K., Takahashi, A., Masuda, T., Noji, S. 2015b. RNAi-mediated silencing and overexpression of the FaMYB1 gene and its effect on anthocyanin accumulation in strawberry fruit. Biol. Plantarum 59: 677–685.
– reference: Lin-Wang, K., Micheletti, D., Palmer, J., Volz, R., Lozano, L., Espley, R., Hellens, R. P., Chagne, D., Rowan, D. D., Troggio, M., Iglesias, I., Allan, A. C. 2011. High air temperature reduces apple fruit color via modulation of the anthocyanin regulatory complex. Plant Cell Environ. 34: 1176–1190.
– reference: Dela, G., Or, E., Ovadia, R., Nissim-Levi, A., Weiss, D., Oren-Shamir, M. 2003. Changes in anthocyanin concentration and composition in ‘Jaguar’ rose flowers due to transient high air temperature conditions. Plant Sci. 164: 333–340.
– reference: Schaart, J. G., Dubos, C., De La Fuente, I. R., Van Houwelingen, A. M. M. L., de Vos, R. C. H., Jonker, H. H., Xu, W., Routaboul, J. M., Lepiniec, L., Bovy, A. G. 2013. Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria×ananassa) fruits. New. Phytol. 197: 454–467.
– reference: Ikeda, T., Matsushita, K., Oyaizu, Y., Okutsu, K. 2016. Different expressions of anthocyanin biosynthetic genes for strawberry ‘Sachinoka’ fruits under water and high temperature stresses. 8th International Strawberry Symposium 2016, Quebec City, Canada. Book of Abstracts: 144.
– reference: Yamane, T., Jeong, S. T., Goto-Yamamoto, N., Koshita, Y., Kobayashi, S. 2006. Effect of temperature on anthocyanin biosynthesis in grape berry skins. Am. J. Enol. Vitic. 57: 54–59.
– reference: Medina-Puche, L., Cumplido-Laso, G., Amil-Ruiz, F., Hoffmann, T., Ring, L., Rodríguez-Franco, A., Caballero, J. L., Schwab, W., Muñoz-Blanco, J., Blanco-Portales, R. 2014. MYB10 plays a major role in the regulation of flavonoid/ phenylpropanoid metabolism during ripening of Fragaria× ananassa fruits. J. Exp. Bot. 65: 401–417.
– reference: Kadomura-Ishikawa, Y., Miyawaki, K., Takahashi, A., Masuda, T., Noji, S. 2015a. Light and abscisic acid independently regulated FaMYB10 in Fragaria×ananassa fruit. Planta 241: 953–965.
– reference: Reid, K. E., Olsson, N., Schlosser, J., Peng, F., Lund, S. T. 2006. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol. 6: 27.
– reference: Mori, K., Goto-Yamamoto, N., Kitayama, M., Hashizume, K. 2007. Loss of anthocyanins in red-wine grape under high air temperature. J. Exp. Bot. 58: 1935–1945.
– reference: Pombo, M. A., Martínez, G. A., Civello, P. M. 2011. Cloning of FaPAL6 gene from strawberry fruit and characterization of its expression and enzymatic activity in two cultivars with different anthocyanin accumulation. Plant Sci. 181: 111–118.
– reference: Almeida, J. R. M., D’Amico, E., Preuss, A., Carbone, F., De Vos, R. C. H., Deiml, B., Mourgues, F., Perrotta, G., Fischer, T. C., Bovy, A. G., Martens, S., Rosati, C. 2007. Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria×ananassa). Arch. Biochem. Biophys. 465: 61–71.
– reference: Jeong, S. T., Goto-Yamamoto, N., Kobayashi, S., Esaka, M. 2004. Effects of plant hormones and shading on the accumulation anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Sci. 167: 247–252.
– reference: Saure, M. C. 1990. External control of anthocyanin formation in apple. Sci. Hortic. 42: 181–218.
– reference: Boss, P. K., Davies, C., Robinson, S. P. 1996. Expression of anthocyanin biosynthesis pathway genes in red and white grapes. Plant Mol. Biol. 32: 565–569.
– reference: Ikeda, T., Suzuki, N., Nakayama, M., Kawakami, Y. 2011. The effects of high air temperature and water stress on fruit growth and anthocyanin concentration of pot-grown strawberry (Fragaria×ananassa Duch. cv. ‘Sachinoka’) plants. Environ. Control Biol. 49: 209–215.
– reference: Azuma, A., Yakushiji, H., Koshita, Y., Kobayashi, S. 2012. Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 236: 1067–1080.
– reference: Aharoni, A., De Vos, R. C. H., Wein, M., Sun, Z., Greco, R., Kroon, A., Mol, J. N. M., O’Connell, A. P. 2001. The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J. 28: 319–332.
– reference: Jaakola, L. 2013. New insights into the regulation of anthocyanin biosynthesis in fruits. Trends. Plant Sci. 18: 477–483.
– reference: Matsushita, K., Sakayori, T., Ikeda, T. 2016. The effect of high air temperature on anthocyanin concentration and the expressions of its biosynthetic genes in strawberry ‘Sachinoka’. Environ. Control Biol. 54: 101–107.
– reference: Schmittgen, T. D., Livak, K. J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3: 1101–1108.
– reference: Kobayashi, S. 2009. Regulation of anthocyanin biosynthesis in grapes. J. Jpn. Soc. Hortic. Sci. 78: 387–393.
– reference: Mori, K., Sugaya, S., Gemma, H. 2004. Regulatory mechanism of anthocyanin biosynthesis in ‘Kyoho’ grape berries grown under different temperature conditions. Environ. Control Biol. 42: 21–30.
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– ident: 24
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Snippet We investigated anthocyanin concentration and the expression of anthocyanin biosynthesis related genes in strawberry ‘Sachinoka’ (Fragaria×ananassa Duch.)...
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SubjectTerms Biosynthesis
Color
Coloring
Colour
Control
Exposure
Fragaria ananassa
fruit coloring stage
Fruits
Gene expression
Genes
High temperature
Ripening
Stress concentration
Temperature
Temperature effects
timing of stress
Title Differential Anthocyanin Concentrations and Expression of Anthocyanin Biosynthesis Genes in Strawberry ‘Sachinoka’ during Fruit Ripening under High-temperature Stress
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