Skip to main content
SpringerLink
Log in

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

  • Original papers
  • Published:
Biologia Plantarum

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

G:

grain filling rate

HT:

high temperature

IAA:

indole-3-acetic acid

PAs:

polyamines

Put:

putrescine

Spd:

spermidine

Spm:

spermine

Z:

zeatin

ZR:

zeatin riboside

References

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Crowley, T.J.: Causes of climate change over the past 1000 years. — Science 289: 270–277, 2000.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Fitzgerald, M.A., Resurreccion, A.P.: Maintaining the yield of edible rice in a warming world. — Funct. Plant Biol. 36: 1037–1045, 2009.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Richards, F.: A flexible growth function for empirical use. — J. exp. Bot. 10: 290–301, 1959.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Yemm, E.W., Willis, A.J.: The estimation of carbohydrates in plant extracts by anthrone. — Biochem. J. 57: 508–514, 1954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Life Science, Nantong University, Nantong, P.R. China

    Y. Y. Cao & Y. H. Chen

  2. School of Life Sciences and State Key Laboratory of Agrobiotechnology, Chinese University of Hong Kong, Hong Kong, P.R. China

    Y. Y. Cao, M. X. Chen & J. H. Zhang

  3. Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou University, Yangzhou, P.R. China

    Z. Q. Wang & J. C. Yang

  4. Jiangsu Yanjiang Institute of Agricultural Sciences, Rugao, P.R. China

    C. F. Wu & X. C. Bian

Authors
  1. Y. Y. Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. H. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. X. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Z. Q. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. F. Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. X. C. Bian
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. C. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. J. H. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to J. C. Yang or J. H. Zhang.

Additional information

Acknowledgement

This study was supported by the National “973”sub-project (2012CB114306), the University Natural Science Research Project of Jiangsu Province (13KJB210005), the Jiangsu Agricultural Science and Technology Innovation Fund (JASTIF, CX(13)5086), and the Shenzhen Vegetable Molecular Biotechnological Engineering Lab Scheme (Development and Reform Commission of Shenzhen Municipal Government).

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, Y.Y., Chen, Y.H., Chen, M.X. et al. Growth characteristics and endosperm structure of superior and inferior spikelets of indica rice under high-temperature stress. Biol Plant 60, 532–542 (2016). https://doi.org/10.1007/s10535-016-0606-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-016-0606-6

Additional key words

Search

Navigation