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  Eur.J.Hortic.Sci. 82 (5) 232-238 | DOI: 10.17660/eJHS.2017/82.5.2
ISSN 1611-4426 print and 1611-4434 online | © ISHS 2017 | European Journal of Horticultural Science | Original article

Night temperatures affect fruit coloration and expressions of anthocyanin biosynthetic genes in 'Hongro' apple fruit skins

Suhyun Ryu1, Hyun-Hee Han1, Jae Hoon Jeong1, YongHee Kwon1, Jeom Hwa Han1, Gyung Ran Do1, In-Myung Choi1 and Hee Jae Lee2,3
1 Fruit Research Division, National Institute of Horticultural and Herbal Science, Wanju, Korea
2 Department of Plant Science, Seoul National University, Seoul, Korea
3 Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, Korea

We analyzed the fruit skin coloration and expressions of anthocyanin biosynthetic genes to determine the effects of night temperature on ‘Hongro’ apple (Malus domestica Borkh.). Trees were grown under low night temperatures (LNT; 3°C lower than the control) and high night temperatures (HNT; 3°C higher than the control) for 2 months from July to August. LNT promoted an increase of the a* value and decreases of the L*, b*, and h° values in fruit skins, but HNT produced the opposite results. Anthocyanins accumulated in fruit skins with increasing days after full bloom. The anthocyanin biosynthesis was promoted by LNT, but inhibited by HNT. Quantitative real-time polymerase chain reaction analysis revealed that LNT increased the expressions of anthocyanin biosynthetic genes, MdCHS, MdF3H, MdDFR, MdANS, and MdUFGT, but HNT decreased them. These results suggest that temperatures at night affect anthocyanin accumulation in apple fruit skins by regulating expressions of the anthocyanin biosynthetic genes.

Keywords anthocyanidin, CIE color scales, fruit quality, high night temperature, transcription factors

Significance of this study

What is already known on this subject?

  • Apples grown at high temperature during fruit development are poorly colored, while those grown at low temperature are well colored. Coloration of apple fruit skins is determined by their anthocyanin contents. The anthocyanin accumulation in apple fruit skins is inhibited by high temperatures under light conditions.
What are the new findings?
  • Anthocyanin accumulation in apple fruit skins was promoted by low temperature at night, but suppressed by high temperature. The reduced anthocyanin accumulation caused by high temperature at night was due to the decreased expressions of anthocyanin biosynthetic genes, MdCHS, MdF3H, MdDFR, MdANS, and MdUFGT. These results suggest that temperatures at night affect anthocyanin accumulation in apple fruit skins by regulating expressions of the anthocyanin biosynthetic genes.
What is the expected impact on horticulture?
  • As a result of global warming, not only high temperatures in the daytime but also tropical night high temperatures are increasing. Our results provide fundamental information for controlling the fruit skin coloration of apples under different temperatures at night.

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  • Arakawa, O., Kikuya, S., Pungpomin, P., Zhang, S., and Tanaka, N. (2016). Accumulation of anthocyanin in apples in response to blue light at 450 nm: recommendations for producing quality fruit color under global warming. Eur. J. Hortic. Sci. 81, 297–302.

  • Ban, Y., Honda, C., Hatsuyama, Y., Igarashi, M., Bessho, H., and Moriguchi, T. (2007). Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant Cell Physiol. 48, 958–970.

  • Ban, Y., Kondo, S., Ubi, B.E., Honda, C., Bessho, H., and Moriguchi, T. (2009). UDP-sugar biosynthetic pathway: contribution to cyanidin 3-galactoside biosynthesis in apple skin. Planta 230, 871–881.

  • Bergh, O. (1990). Effect of temperature during the first 42 days following full bloom on apple fruit growth and size at harvest. S. Afr. J. Plant Soil 7, 11–18.

  • Bergh, O., and Cloete, D.V. (1992). Effect of different day and night temperatures on the diurnal growth rate of terminal and lateral fruits in Golden Delicious apple. S. Afr. J. Plant Soil 9, 68–72.

  • Blankenship, S.M. (1987). Night-temperature effects on rate of apple fruit maturation and fruit quality. Sci. Hortic. 33, 205–212.

  • Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622.

  • Espley, R.V., Hellens, R.P., Putterill, J., Stevenson, D.E., Amma, S.K., and Allan, A.C. (2007). Red coloration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J. 49, 414–427.

  • Felicetti, D.A., and Schrader, L.E. (2008). Changes in pigment concentrations associated with the degree of sunburn browning of ‘Fuji’ apple. J. Amer. Soc. Hortic. Sci. 133, 27–34.

  • Fisher, G., Ebert, G., and Ludders, P. (2007). Production, seeds, and carbohydrate contents of cape gooseberry (Physalis peruviana L.) fruits grown at two contrasting Colombian altitudes. J. Appl. Bot. Food Qual. 81, 29–35.

  • Honda, C., Kotoda, N., Wada, M., Kondo, S., Kobayashi, S., Soejima, J., Zhang, Z., Tsuba, T., and Moriguchi, T. (2002). Anthocyanin biosynthetic genes are coordinately expressed during red coloration in apple skin. Plant Physiol. Biochem. 40, 955–962.

  • Jaakola, L., Pirttila, A.M., Halonen, M., and Hohtola, A. (2001). Isolation of high quality RNA from bilberry (Vaccinium myrtillus L.) fruit. Mol. Biotechnol. 19, 201–203.

  • Jacob, D., Petersen, J., Eggert, B., Alias, A., Christensen, O.B., Bouwer, L.M., Braun, A., Colette, A., Deque, M., Georgievski, G., et al. (2014). EURO-CORDEX: new high-resolution climate change projections for European impact research. Reg. Environ. Change 14, 563–578.

  • Kim, S.H., Heo, S., Shin, I.S., Kim, J.H., Cho, K.H., Kim, D.H., and Hwang, J.H. (2010). Identifying genes related with self-thinning characteristics in apple by differential display PCR. Kor. J. Breed. Sci. 42, 565–573.

  • Lancaster, J.E., and Dougall, D.K. (1992). Regulation of skin color in apples. Crit. Rev. Plant Sci. 10, 487–502.

  • Lancaster, L.E., Lister, C.E., Reay, P.F., and Triggs, C.M. (1997). Influence of pigment composition on skin color in a wide range of fruit and vegetables. J. Amer. Soc. Hortic. Sci. 122, 594–598.

  • Li, S. (2014). Transcriptional control of flavonoid biosynthesis. Plant Signal. Behav. 9, 1.

  • Lin-Wang, K., Bolitho, K., Grafton, K., Kortstee, A., Karunairetnam, S., McGhie, T.K., Espley, R.V., Hellens, R.P., and Allan, A.C. (2010). An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol. 10, 1.

  • 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., and Allan, A.C. (2011). High temperature reduces apple fruit color via modulation of the anthocyanin regulatory complex. Plant Cell Environ. 34, 1176–1190.

  • Liu, Y., Che, F., Wang, L., Meng, R., Zhang, X., and Zhao, Z. (2013). Fruit coloration and anthocyanin biosynthesis after bag removal in non-red and red apples (Malus Χ domestica Borkh.). Molecules 18, 1549–1563.

  • Marais, E., Jacobs, G., and Holcroft, D.M. (2001). Color response of ‘Cripps’ Pink’ apples to postharvest irradiation is influenced by maturity and temperature. Sci. Hortic. 90, 31–41.

  • McGuire, R.G. (1992). Reporting of objective color measurements. HortScience 27, 1254–1255.

  • Peng, T., and Moriguchi, T. (2013). The molecular network regulating the coloration in apple. Sci. Hortic. 163, 1–9.

  • Petroni, K., and Tonelli, C. (2011). Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci. 181, 219–229.

  • Reay, P.F. (1999). The role of low temperatures in the development of the red blush on apple fruit (‘Granny Smith’). Sci. Hortic. 79, 113–119.

  • Ririe, K.M., Rasmussen, R.P., and Wittwer, C.T. (1997). Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal. Biochem. 245, 154–160.

  • Saure, M.C. (1990). External control of anthocyanin formation in apple. Sci. Hortic. 42, 181–218.

  • Seo, Y.W., Kim, H., Yun, K.S., Lee, J.Y., Ha, K.J., and Moon, J.Y. (2014). Future change of extreme temperature climate indices over East Asia with uncertainties estimation in the CMIP5. Asia-Pac. J. Atmos. Sci. 50, 57–72.

  • Stanley, C.J., Tustin, D.S., Lupton, G.B., McArtney, S., Cashmore, W.M., and De Silva, H.N. (2000). Towards understanding the role of temperature in apple fruit growth responses in three geographical regions within New Zealand. J. Hortic. Sci. Biotechnol. 75, 413–422.

  • Starck, Z., and Ciesla, E. (1989). Possible role of growth regulators in adaptation to heat stress affecting partitioning of photosynthates to tomato plants. Acta Soc. Bot. Pol. 58, 71–84.

  • Takos, A.M., Jaffe, F.W., Jacob, S.R., Bogs, J., Robinson, S.P., and Walker, A.R. (2006). Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol. 142, 1216–1232.

  • Tan, S.C. (1980). Phenylalanine ammonia-lyase and the phenylalanine ammonia-lyase inactivating system: effects of light, temperature, and mineral deficiencies. Aust. J. Plant Physiol. 7, 159–167.

  • Thibeault, J.M., and Seth, A. (2014). Changing climate extremes in the Northeast United States: observations and projections from CMIP5. Climatic Changes 127, 273–287.

  • Ubi, B.E. (2004). External stimulation of anthocyanin biosynthesis in apple fruit. Food Agric. Environ. 2, 65–70.

  • Ubi, B.E., Honda, C., Bessho, H., Kondo, S., Wada, M., Kobayashi, S., and Moriguchi, T. (2006). Expression analysis of anthocyanin biosynthetic gene in apple skin: effect of UV-B and temperature. Plant Sci. 170, 571–578.

  • Warrington, I.J., Fulton, T.A., Halligan, E.A., and De Silva, H.N. (1999). Apple fruit growth and maturity are affected by early season temperatures. J. Amer. Soc. Hortic. Sci. 124, 468–477.

Received: 24 February 2017 | Accepted: 25 April 2017 | Published: 23 October 2017 | Available online: 23 October 2017

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