Abstract
High temperature (HT) at the filling stage is a major environmental constraint to rice (Oryza sativa L.) grain quality. However, the effects of HT on the accumulation and composition of storage proteins are not well understood. In this study, the transcriptional expressions of genes related to storage protein synthesis responsive to HT, and their relationship with storage protein composition, were comprehensively analyzed under controlled temperature using two non-waxy indica rice cultivars, 9311 and II-7954. HT reduced grain weight and increased total protein content (TPC) irrespective of rice genotype, and HT-inducible increase in TPC was attributable to the relative increase in proportion of the aleurone fraction to whole grain, as well as increased absolute amount of TPC in rice grain; HT resulted in a relatively higher ratio of glutelin to prolamin compared with the control temperature, as reflected by a significant decrease in amount of 13-kDa prolamin polypeptide and an enhanced accumulation of proglutelin, α-glutelin and β-glutelin subunits throughout the whole grain filling; The remarkably lowering of transcripts of glutelin and/or prolamin family genes in HT-ripening grain at the middle and late filling stage possibly were closely associated with the repressing regulation of RPBF induced by HT, while RISBZ1 was possibly mainly responsible for regulating the response of glutelin family genes to HT at the earlier filling stage. In addition, HT accelerated expressions of PDI and BiP to assist with the proper folding and assembly of proglutelin.
Similar content being viewed by others
References
Ashida K, Araki E, Maruyama-Funatsuki W, Fujimoto H, Ikegami M (2013) Temperature during grain ripening affects the ratio of type-II/type-I protein body and starch pasting properties of rice (Oryza sativa L.) J Cereal Sci 57:153–159
Bollag DM, Edelstein SJ (1990) Protein methods. Wiley-Liss, New York, pp 50–56
Cooper NTW, Siebenmorgen TJ, Counce PA (2008) Effects of nighttime temperature during kernel development on rice physicochemical properties. Cereal Chem 85:276–282
Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155:1566–1577
Holme DJ, Peck H (1998) Peck analytical biotechnology, 3rd edn. Addison Wesley Longman Limited, New York, pp 388–390
Jagadish SVK, Murty MVR, Quick WP (2015) Rice responses to rising temperatures—challenges, perspectives and future directions. Plant Cell Environ 38:1686–1698
Kawakatsu T, Takaiwa F (2010) Cereal seed storage protein synthesis: fundamental processes for recombinant protein production in cereal grains. Plant Biotechnol J 8:939–953
Kawakatsu T, Yamamoto MP, Touno SM, Yasuda H, Takaiwa F (2009) Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant J 59:908–920
Kawakatsu T, Hirose S, Yasuda H, Takaiwa F (2010) Reducing rice seed storage protein accumulation leads to changes in nutrient quality and storage organelle formation. Plant Physiol 154:1842–1854
Kim YJ, Yeu SY, Park BS, Koh HJ, Song JT, Seo HS (2012) Protein disulfide isomerase-like protein 1–1 controls endosperm development through regulation of the amount and composition of seed proteins in rice. Plos One 7(9):e44493
Krishnan P, Ramakrishnan B, Raja Reddy K, Reddy VR (2011) High-temperature effects on rice growth, yield, and grain quality. Adv Agron 111:87
Kumamaru T, Uemura Y, Inoue Y, Takemoto Y, Siddiqui SU, Ogawa M, Hara-Nishimura I, Satoh H (2010) Vacuolar processing enzyme plays an essential role in the crystalline structure of glutelin in rice seed. Plant Cell Physiol 51:38–46
Li X, Wu Y, Zhang DZ, Gillikin JW, Boston RS, Franceschi VR, Okita TW (1993) Rice prolamine protein body biogenesis: a BiP-mediated process. Science 262:1054–1056
Lin CJ, Li CY, Lin SK, Yang FH, Huang JJ, Liu YH, Lur HS (2010) Influence of high temperature during grain filling on the accumulation of storage proteins and grain quality in rice (Oryza sativa L.) J Agric Food Chem 58:10545–10552
Nuttall J, Vine N, Hadlington JL, Drake P, Frigerio L, Ma JKC (2002) ER-resident chaperone interactions with recombinant antibodies in transgenic plants. Eur J Biochem 269:6042–6051
Ogawa M, Kumamaru T, Satoh H, Iwata N, Omura T, Kasai Z, Tanaka K (1987) Purification of protein body-I of rice seed and its polypeptide composition. Plant Cell Physiol 28:1517–1527
Onodera Y, Suzuki A, Wu CY, Washida H, Takaiwa F (2001) A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif. J Biol Chem 276:14139–14152
Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA 101:9971–9975
Saito Y, Shigemitsu T, Yamasaki R, Sasou A, Goto F, Kishida K, Kuroda M, Tanaka K, Morita S, Satoh S, Masumura T (2012) Formation mechanism of the internal structure of type I protein bodies in rice endosperm: relationship between the localization of prolamin species and the expression of individual genes. Plant J 70:1043–1055
Satoh-Cruz M, Crofts AJ, Takemoto-Kuno Y, Sugino A, Washida H, Crofts N, Okita TW, Ogawa M, Satoh H, Kumamaru T (2010) Protein disulfide isomerase like 1–1 participates in the maturation of proglutelin within the endoplasmic reticulum in rice endosperm. Plant Cell Physiol 51:1581–1593
Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947–958
Su D, Lei BT, Li ZW, Cao ZZ, Huang FD, Pan G, Ding Y, Cheng FM (2014) Influence of high temperature during filling period on grain phytic acid and its relation to spikelet sterility and grain weight in non-lethal low phytic acid mutations in rice. J Cereal Sci 60:331–338
Takahashi H, Saito Y, Kitagawa T, Morita S, Masumura T, Tanaka K (2005) A novel vesicle derived directly from endoplasmic reticulum is involved in the transport of vacuolar storage proteins in rice endosperm. Plant Cell Physiol 46:245–249
Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T (2002) The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol 128:1212–1222
Tan Y, Corke H (2002) Factor analysis of physicochemical properties of 63 rice varieties. J Sci Food Agric 82:745–752
Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. Febs J 274:1152–1171
Wang KM, Wu JG, Li G, Yang ZW, Shi CH (2011) Distribution of phytic acid and mineral elements in three indica rice (Oryza sativa L.) cultivars. J Cereal Sci 54:116–121
Yamagata H, Tanaka K (1986) The site of synthesis and accumulation of rice storage proteins. Plant Cell Physiol 27:135–145
Yamagata H, Sugimoto T, Tanaka K, Kasai Z (1982) Biosynthesis of storage proteins in developing rice seeds. Plant Physiol 70:1094–1100
Yamakawa H, Hirose T, Kuroda M, Yamaguchi T (2007) Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA microarray. Plant Physiol 144:258–277
Yamamoto MP, Onodera Y, Touno SM, Takaiwa F (2006) Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiol 141:1694–1707
Acknowledgments
The authors are deeply indebted to National Natural Science Foundation of China (No. 31271655) for its financial support to this research project.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Cao, Z., Zhao, Q., Pan, G. et al. Comprehensive expression of various genes involved in storage protein synthesis in filling rice grain as affected by high temperature. Plant Growth Regul 81, 477–488 (2017). https://doi.org/10.1007/s10725-016-0225-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-016-0225-4