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Effects of Low Temperature during Ripening on Amylose Content and Enzyme Activities Associated with Starch Biosynthesis in Rice Endosperm

  • Baek, Jung-sun (Foundation of Agri. Tech. Commercialization & Transfer) ;
  • Jeong, Han-Yong (Crop Production and Physiology Division, National Institute of Crop Science) ;
  • An, Sung-Hyun (Crop Production and Physiology Division, National Institute of Crop Science) ;
  • Jeong, Jae-Heok (Crop Production and Physiology Division, National Institute of Crop Science) ;
  • Lee, Hyen-Seok (Crop Production and Physiology Division, National Institute of Crop Science) ;
  • Yoon, Jong-Tak (Crop Production and Physiology Division, National Institute of Crop Science) ;
  • Choi, Kyung-Jin (Crop Production and Physiology Division, National Institute of Crop Science) ;
  • Hwang, Woon-Ha (Crop Production and Physiology Division, National Institute of Crop Science)
  • Received : 2017.12.11
  • Accepted : 2018.05.08
  • Published : 2018.06.30

Abstract

The objective of this study was to determine the effects of low temperature on starch accumulation in rice grains. We used four major Japonica-type Korean rice cultivars as materials: Jinbu (JB), Junamjosaeng (JJ), Geumyoung (GY), and Hwawang (HW). Rice plants were moved into two phytotrons the day after heading. Temperatures in the two phytotrons were maintained at $19/29^{\circ}C$ (night/day) as the control, and $13/23^{\circ}C$ as the low temperature condition, both under natural daylight with a relative humidity of 65%. The ripening rates of JB and JJ showed no significant difference between the low temperature and control conditions at 45 days after heading (DAH). In contrast, the ripening rates of GY and HW were 86% and 57% lower than those of JB and JJ under the low temperature condition at 45 DAH, respectively. However, the ripening rates of these four varieties at 61 DAH (when accumulated temperature reached $1,100^{\circ}C$) under the low temperature condition were similar to those at 45 DAH under the control condition (JB, 94%; JJ, 97%; GY, 97%; HW, 88%). The total starch contents showed no significant difference between the control and low temperature conditions. However, the amylose contents in the cultivars were higher under the low temperature than under the control condition. The enzyme activities of starch biosynthesis were about 5-10 days slower in cultivars under the low temperature than under the control. The grain-filling rate showed significant correlations with the enzyme activities of SuSase ($r^2=0.70^{***}$), AGPase ($r^2=0.63^{***}$), UDPase ($r^2=0.36^{***}$), StSase ($r^2=0.51^{***}$), and SBE ($r^2=0.59^{***}$). In conclusion, although StSase activity was increased at $13/23^{\circ}C$ up to 20 DAH, there might not be enough time for SBE to synthesize amylopectin, thus affecting the amylose content of HW, which had the slowest grain filling rate. Notably, the decreased activity of SuSase and SBE and late increase in AGPase activity under the low temperature during the ripening stage are considered to be disadvantageous, as they delay ripening and increase the amylose content.

Keywords

References

  1. Abe, N., H. Asai, H. Yago, N. F. Oitome, R. Itoh, N. Crofts, Y. Nakamura, and N. Fujita. 2014. Relationships between starch synthase I and branching enzyme isozymes determined using double mutant rice lines. BMC Plant Biology 14 : 80. https://doi.org/10.1186/1471-2229-14-80
  2. Ahmadi, A. and D. A. Baker. 2001. The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat. Plant Growth Regulation 35 : 81-91. https://doi.org/10.1023/A:1013827600528
  3. Ahmed, N., I. J. Tetlow, S. Nawaz, A. Iqbal, M. Mubin, N. Rehman, M. Shah, A. Butt, D. A. Lightfoot, and M. Maekawa. 2015. Effect of high temperature on grain filling period, yield, amylose content and activity of starch biosynthesis enzymes in endosperm of basmati rice. Journal of the Science of Food and Agriculture 95 : 2237-2243. https://doi.org/10.1002/jsfa.6941
  4. AOAC. 2005 'Official Methods of Analysis. 18th ed.' (Association of Official Agricultural Chemists, Washington DC, USA.
  5. Asaoka, M., K. Okuno, and H. Fuwa. 1985. Effect of environmental temperature at the milky stage on amylose content and fine structure of amylopectin of waxy and nonwaxy endosperm starches of rice (Oryza sativa L.). Agricultural and Biological Chemistry 49 : 373-379.
  6. Bahuguna, R. N., C. A. Solis, W. Shi, and K. S. Jagadish. 2017. Post-flowering night respiration and altered sink activity account for high night temperature‐induced grain yield and quality loss in rice (Oryza sativa L.). Physiologia Plantarum 159 : 59-73. https://doi.org/10.1111/ppl.12485
  7. Ballicora, M. A., A. A. Iglesias, and J. Preiss. 2004. ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynthesis Research 79 : 1-24. https://doi.org/10.1023/B:PRES.0000011916.67519.58
  8. Ciereszko, I., H. Johansson, and L. A. KLECZKOWSKI. 2001. Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Biochemical Journal 354 : 67-72. https://doi.org/10.1042/bj3540067
  9. Gupta, S. K., and J. R. Sowokinos. 2003. Physicochemical and kinetic properties of unique isozymes of UDP-Glc pyrophosphorylase that are associated with resistance to sweetening in cold-stored potato tubers. Journal of Plant Physiology 160 : 589-600. https://doi.org/10.1078/0176-1617-01045
  10. Hendriks, J. H., A. Kolbe, Y. Gibon, M. Stitt, and P. Geigenberger. 2003. ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiology 133 : 838-849. https://doi.org/10.1104/pp.103.024513
  11. Hurkman, W. J., K. F. McCue, S. B. Altenbach, A. Korn, CK. Tanaka, K. M. Kothari, E. L. Johnson, D. B. Bechtel, J. D. Wilson, and O. D. Anderson. 2003. Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm. Plant Science 164 : 873-881. https://doi.org/10.1016/S0168-9452(03)00076-1
  12. Jagadish, S., P. Craufurd, and T. Wheeler. 2007. High temperature stress and spikelet fertility in rice (Oryza sativa L.). Journal of Experimental Botany 58, 1627-1635. https://doi.org/10.1093/jxb/erm003
  13. Jiang, H., W. Dian, and P. Wu,. 2003. Effect of high temperature on fine structure of amylopectin in rice endosperm by reducing the activity of the starch branching enzyme. Phytochemistry 63 : 53-59. https://doi.org/10.1016/S0031-9422(03)00005-0
  14. Keeling, P., P. Bacon, and D. Holt. 1993. Elevated temperature reduces starch deposition in wheat endosperm by reducing the activity of soluble starch synthase. Planta 191 : 342-348.
  15. Kim, D. H., S. M. Lee, J. S. Park, S. J. Kim, B. K. Kim, I. S. Yun, D. I. Kim, and M.O. Byun. 2010. Current status on carbon metabolic engineering in plants. Journal of Plant Biotechnology 37 : 205-211. https://doi.org/10.5010/JPB.2010.37.2.205
  16. Kleczkowski, L. A., M. Geisler, I. Ciereszko, and H. Johansson. 2004. UDP-glucose pyrophosphorylase. An old protein with new tricks. Plant physiology 134 : 912-918. https://doi.org/10.1104/pp.103.036053
  17. Kobata, T., and N. Uemuki. 2004. High temperatures during the grain-filling period do not reduce the potential grain dry matter increase of rice. Agronomy Journal 96 : 406-414. https://doi.org/10.2134/agronj2004.0406
  18. Lobell, D. B., and M. B. Burke. 2010. On the use of statistical models to predict crop yield responses to climate change. Agricultural and Forest Meteorology 150 : 1443-1452. https://doi.org/10.1016/j.agrformet.2010.07.008
  19. Matsue, Y. 1995. Studies on palatability of rice in northern Kyushu: V. Influence of abnormal weather in 1993 on the palatability and physicochemical characteristics of rice. Japanese Journal of Crop Science 64 : 709-713. https://doi.org/10.1626/jcs.64.709
  20. McCleary, B. V., T. S. Gibson, and D. C. Mugford. 1997. Measurement of total starch in cereal products by amyloglucosidase-a-amylase method: Collaborative study. Journal of AOAC International 80 : 571-579.
  21. Nakamura, Y. 2002. Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant and Cell Physiology 43 : 718-725. https://doi.org/10.1093/pcp/pcf091
  22. Nakamura, Y., K. Yuki, S. Y. Park, and T. Ohya. 1989. Carbohydrate metabolism in the developing endosperm of rice grains. Plant and Cell Physiology 30 : 833-839. https://doi.org/10.1093/oxfordjournals.pcp.a077813
  23. Nishi, A., Y. Nakamura, N. Tanaka, and H. Satoh. 2001. Biochemical and genetic analysis of the effects of amylose-Extender mutation in rice endosperm. Plant Physiology 127 : 459-472. https://doi.org/10.1104/pp.010127
  24. Peng, S., J. Huang, J. E. Sheehy, R. C. Laza, R. M. Visperas, X. Zhong, G. S. Centeno, K. G. S. hush, and K. G. Cassman. 2004. Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences of the United States of America 101 : 9971-9975. https://doi.org/10.1073/pnas.0403720101
  25. Richards, F. 1959. A flexible growth function for empirical use. Journal of experimental botany 10 : 290-301. https://doi.org/10.1093/jxb/10.2.290
  26. Schmolzer, K., A. Gutmann, M. Diricks, T. Desmet, and B. Nidetzky. 2016. Sucrose synthase: A unique glycosyltransferase for biocatalytic glycosylation process development. Biotechnology Advances 34 : 88-111. https://doi.org/10.1016/j.biotechadv.2015.11.003
  27. Smith, A. M. 2008. Prospects for increasing starch and sucrose yields for bioethanol production. The Plant Journal 54 : 546-558. https://doi.org/10.1111/j.1365-313X.2008.03468.x
  28. Sun, M. M., H. J. Lee, S. E. Abdula, M. G. Jee, and Y. G. Cho. 2013. Overexpression of starch branching enzyme 1 gene improves eating quality in japonica rice. Journal of Plant Biotechnology 40 : 88-101. https://doi.org/10.5010/JPB.2013.40.2.088
  29. Tian, Y., H. Chen, X. Zhang, J. Zhan, Z. Jin, and J. Wang. 2016. Highly branched dextrin prepared from high-amylose maize starch using waxy rice branching enzyme (WRBE). Food Chemistry 203 : 530-535. https://doi.org/10.1016/j.foodchem.2016.02.061
  30. Umemoto, T., Y. Nakamura, and N. Ishikura. 1995. Activity of starch synthase and the amylose content in rice endosperm. Phytochemistry 40 : 1613-1616. https://doi.org/10.1016/0031-9422(95)00380-P
  31. Yamakawa, H., and M. Hakata. 2010. Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant and Cell Physiology 51 : 795-809. https://doi.org/10.1093/pcp/pcq034
  32. Yamanouchi, H., and Y. Nakamura. 1992. Organ specificity of isoforms of starch branching enzyme (Q-enzyme) in rice. Plant and Cell Physiology 33 : 985-991.
  33. Yang, J., J. Zhang, Z. Wang, G. Xu, and Q. Zhu. 2004. Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiology 135 : 1621-1629. https://doi.org/10.1104/pp.104.041038
  34. Yang, J., J. Zhang, Z. Wang, Q. Zhu, and L. Liu. 2003. Activities of enzymes involved in sucrose-to-starch metabolism in rice grains subjected to water stress during filling. Field Crops Research 81 : 69-81. https://doi.org/10.1016/S0378-4290(02)00214-9
  35. Yiqi, Z. Q. C. X. L. 1988. Growth analysis on the process of grain filling in rice. Acta Agronomica Sinica 3 : 182-193.
  36. Yun, S. H., and J. T. Lee. 2001. Climate change impacts on optimum ripening periods of rice plant and its countermeasure in rice cultivation. Korean Journal of Agricultural and Forest Meteorology 3 : 55-70.

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