Biologia plantarum 2016, 60:532-542 | DOI: 10.1007/s10535-016-0606-6

Growth characteristics and endosperm structure of superior and inferior spikelets of indica rice under high-temperature stress

Y. Y. Cao1,2, Y. H. Chen1, M. X. Chen2, Z. Q. Wang3, C. F. Wu4, X. C. Bian4, J. C. Yang3,*, J. H. Zhang2,*
1 College of Life Science, Nantong University, Nantong, P.R. China
2 School of Life Sciences and State Key Laboratory of Agrobiotechnology, Chinese University of Hong Kong, Hong Kong, P.R. China
3 Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou University, Yangzhou, P.R. China
4 Jiangsu Yanjiang Institute of Agricultural Sciences, Rugao, P.R. China

Heat stress severely reduces rice yield and quality; however, differences between the superior, early-flowering and inferior, later-flowering spikelets of indica rice in response to high-temperature stress during grain filling remain unclear. This study investigated the effects of high temperature (HT, 33.6/20.7 °C day/night) on growth, endosperm structure, and hormone and polyamine content of superior and inferior spikelets of heat-sensitive (SG-1) and heat-tolerant (HHZ) indica cultivars. The HT decreased fertilization rate, caused earlier grain filling, and reduced duration of grain filling, thus resulting in decreased grain mass and a poor endosperm structure. In addition, soluble sugar and sucrose content increased, and starch synthesis decreased by HT at the early stage of grain filling. The HT increased polyamine [spermidine (Spd) and spermine (Spm)] and abscisic acid (ABA) content, but reduced zeatin (Z) + zeatin riboside (ZR) and indole-3-acetic acid (IAA) content in the grains. Such effects were more apparent in the inferior than superior spikelets; however, the inferior spikelets of SG-1 were more affected than those of HHZ. At the middle grain filling stage, HT produced little difference between the two cultivars. Our results suggest that the poor development of inferior spikelets of SG-1 under the HT could be attributed, at least in part, to the changed content and ratios of free polyamines [putrescine (Put), Spd, and Spm] and phytohormones (Z+ZR, IAA, and ABA) and the conversion efficiency of sucrose into starch.

Keywords: abscisic acid; auxin; cytokinin; Oryza sativa; polyamines; starch; sugars
Subjects: endosperm; temperture - high; abscisic acid; auxin; cytokinin; polyamines; starch; sugars; rice; grain development
Species: Oryza sativa

Received: August 18, 2015; Revised: November 19, 2015; Accepted: December 1, 2015; Published: September 1, 2016Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Cao, Y.Y., Chen, Y.H., Chen, M.X., Wang, Z.Q., Wu, C.F., Bian, X.C., Yang, J.C., & Zhang, J.H. (2016). Growth characteristics and endosperm structure of superior and inferior spikelets of indica rice under high-temperature stress. Biologia plantarum60(3), 532-542. doi: 10.1007/s10535-016-0606-6.
Download citation

Supplementary files

Download filebpl-201603-0016_S1.pdf

File size: 560.08 kB

References

  1. Alcazar, R., Marco, F., Cuevas, J. C., Patron, M., Ferrando, A., Carrasco, P., Tiburcio, A. F., Altabella, T.: Involvement of polyamines in plant response to abiotic stress. - Biotechnol Lett. 28: 1867-1876, 2006.
  2. Cao, Y., Duan, H., Yang, L., Wang, Z., Zhou, S., Yang, J.: Effect of heat stress during meiosis on grain yield of rice cultivars differing in heat tolerance and its physiological mechanism. - Acta agron. sin. 34: 2134-2142, 2008. Go to original source...
  3. Cao, Y., Duan, H., Yang, L., Wang, Z., Liu, L., Yang, J.: Effect of high temperature during heading and early filling on grain yield and physiological characteristics in indica rice. - Acta agron. Sin. 35: 512-521, 2009. Go to original source...
  4. Chakrabarti, B., Aggarwal, P.K., Singh, S.D., Nagarajan, S., Pathak, H.: Impact of high temperature on pollen germination and spikelet sterility in rice: comparison between basmati and non-basmati varieties. - Crop Pasture Sci. 61: 363-368, 2010. Go to original source...
  5. Chen, T., Xu, Y., Wang, J., Wang, Z., Yang, J., Zhang, J.: Polyamines and ethylene interact in rice grains in response to soil drying during grain filling. - J. exp. Bot. 64: 2523-2538, 2013. Go to original source...
  6. Cheng, F., Hu, D., Ding, Y.: Dynamic change of chalkiness and observation of grain endosperm structure with scanning electron microscope under controlled temperature condition. - Chin. Rice Sci. 14: 83-87, 1999.
  7. Coast, O., Ellis, R.H., Murdoch, A.J., Quinones, C., Jagadish, K.S.V.: High night temperature induces contrasting responses for spikelet fertility, spikelet tissue temperature, flowering characteristics and grain quality in rice. - Funct. Plant Biol. 42: 149-161, 2015. Go to original source...
  8. Crowley, T.J.: Causes of climate change over the past 1000 years. - Science 289: 270-277, 2000. Go to original source...
  9. Cvikrova, M., Gemperlova, L., Dobra, J., Martincova, O., Prasil, I.T., Gubis, J., Vankova, R.: Effect of heat stress on polyamine metabolism in proline-over-producing tobacco plants. - Plant Sci. 182: 49-58, 2012. Go to original source...
  10. Fitzgerald, M.A., Resurreccion, A.P.: Maintaining the yield of edible rice in a warming world. - Funct. Plant Biol. 36: 1037-1045, 2009. Go to original source...
  11. Hakata, M., Kuroda, M., Miyashita, T., Yamaguchi, T., Kojima, M., Sakakibara, H., Mitsui, T., Yamakawa, H.: Suppression of alpha-amylase genes improves quality of rice grain ripened under high temperature. - Plant Biotechnol. J. 10: 1110-1117, 2012. Go to original source...
  12. Jagadish, S.V., Craufurd, P.Q., Wheeler, T.R.: High temperature stress and spikelet fertility in rice (Oryza sativa L.). - J. exp. Bot. 58: 1627-1635, 2007. Go to original source...
  13. Kobata, T., Uemuki, N.: High temperatures during the grainfilling period do not reduce the potential grain dry matter increase of rice. - Agron. J. 96: 406-414, 2004. Go to original source...
  14. Mohammed, A., Tarpley, L.: Effects of night temperature, spikelet position and salicylic acid on yield and yieldrelated parameters of rice (Oryza sativa L.) plants. - J. Agron. Crop Sci. 197: 40-49, 2011. Go to original source...
  15. Morita, S., Yonemaru, J., Takanashi, J.: Grain growth and endosperm cell size under high night temperatures in rice (Oryza sativa L.). - Ann. Bot. 95: 695-701, 2005. Go to original source...
  16. Peng, S., Huang, J., Sheehy, J.E., Laza, R.C., Visperas, R.M., Zhong, X., Centeno, G.S., Khush, G.S., Cassman, K.G.: Rice yields decline with higher night temperature from global warming. - Proc. nat. Acad. Sci. USA 101: 9971-9975, 2004. Go to original source...
  17. Phan, T.T.T., Ishibashi, Y., Miyazaki, M., Tran, H.T., Okamura, K., Tanaka, S., Nakamura, J., Yuasa, T., Iwaya-Inoue, M.: High temperature-induced repression of the rice sucrose transporter (OsSUT1) and starch synthesis-related genes in sink and source organs at milky ripening stage causes chalky grains. - J. Agron. Crop Sci. 199: 178-188, 2013. Go to original source...
  18. Prasad, P.V.V., Boote, K.J., Allen, L.H., Sheehy, J.E., Thomas, J.M.G.: Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. - Field Crops Res. 95: 398-411, 2006. Go to original source...
  19. Richards, F.: A flexible growth function for empirical use. - J. exp. Bot. 10: 290-301, 1959. Go to original source...
  20. Tashiro, T., Wardlaw, I.F.: The Effect of high temperature on the accumulation of dry matter, carbon and nitrogen in the kernel of rice. - Aust. J. Plant Physiol. 18: 259-265, 1991. Go to original source...
  21. Wakasa, Y., Yasuda, H., Oono, Y., Kawakatsu, T., Hirose, S., Takahashi, H., Hayashi, S., Yang, L., Takaiwa, F.: Expression of ER quality control-related genes in response to changes in BiP1 levels in developing rice endosperm. - Plant J. 65: 675-689, 2011. Go to original source...
  22. Wang, F., Cheng, F., Liu, Y., Zhong, L., Zhang, G.: Dynamic changes of plant hormones in developing grains at rice filling stage under different temperatures. - Acta agron. sin. 32: 25-29, 2005.
  23. Wang, Z., Xu, Y., Wang, J., Yang, J., Zhang, J.: Polyamine and ethylene interactions in grain filling of superior and inferior spikelets of rice. - Plant Growth Regul. 66: 215-228, 2011.
  24. Williams, V.R., Wu, W., Tsai, H.Y., Bates, H.G.: Rice starch, varietal differences in amylose content of rice starch. - J. Agr. Food Chem. 6: 47-48, 1958. Go to original source...
  25. Xu, Z., Xiao, L., Liu, H., Ren, Y., Li, Z.: Effect of temperature during grain filling stage on endosperm structure and apperance quality of aromatic rice. - Adv. Mater. Res. 460: 286-289, 2012. Go to original source...
  26. Yamakawa, H., Hakata, M.: 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 Cell Physiol. 51: 795-809, 2010. Go to original source...
  27. Yang, J., Cao, Y., Zhang, H., Liu, L., Zhang, J.: Involvement of polyamines in the post-anthesis development of inferior and superior spikelets in rice. - Planta 228: 137-149, 2008. Go to original source...
  28. Yang, J., Zhang, J., Liu, K., Liu, K., Wang, Z., Liu, L.: Abscisic acid and ethylene interact in rice spikelets in response to water stress during meiosis. - J. Plant Growth Regul. 26: 318-328, 2007. Go to original source...
  29. Yang, J., Zhang, J., Wang, Z., Zhu, Q.: Hormones in the grains in relation to sink strength and postanthesis development of spikelets in rice. - Plant Growth Regul. 41: 185-195, 2003. Go to original source...
  30. Yemm, E.W., Willis, A.J.: The estimation of carbohydrates in plant extracts by anthrone. - Biochem. J. 57: 508-514, 1954. Go to original source...
  31. Zakaria, S., Matsuda, T., Tajima, S., Nitta, Y.: Effect of high temperature at ripening stage on the reserve accumulation in seed in some rice cultivars. - Plant Prod. Sci. 5: 160-168, 2002. Go to original source...
  32. Zhao, L., Zhang, P., Wang, R.: Effect of high temperature after flowering on growth and development of superior and inferior maize kernels. - Acta agron. sin. 10: 1839-1845, 2014.