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Major QTLs reduce the deleterious effects of high temperature on rice amylose content by increasing splicing efficiency of Wx pre-mRNA

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Abstract

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We discovered four QTLs that maintain proper rice amylose content at high temperature by increasing the splicing efficiency of Wx gene.

Abstract

Amylose content mainly controlled by Wx gene is a key physicochemical property for eating and cooking quality in rice. During the grain filling stage, high temperature can harm rice grain quality by significantly reducing the amylose content in many rice varieties. Here, we provide genetic evidences between Wx gene expression and rice amylose content at high temperature, and identified several quantitative trait loci (QTLs) in this pathway. We performed a genome-wide survey on a set of chromosome segment substitution lines (CSSLs) which carried chromosomal segments from the heat resistant indica 9311 in the heat-sensitive japonica Nipponbare background. Four QTLs, qHAC4, qHAC8a, qHAC8b and qHAC10, which can reduce the deleterious effects of amylose content at high temperature, were identified and mapped to chromosome 4, 8, 8 and 10, respectively. The major QTL qHAC8a, with the highest LOD score of 6.196, was physically mapped to a small chromosome segment (~300 kb). The CSSLs carrying the qHAC8a, qHAC8b and/or qHAC4 from 9311 have the high pre-mRNA splicing efficiency of Wx gene and likely lead to stable amylose content at high temperature. Thus, increasing pre-mRNA processing efficiency of Wx gene could be an important regulation mechanism for maintaining stable amylose content in rice seeds at high temperature. In addition, our results provide a theoretical basis for breeding heat-stable grain in rice.

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Abbreviations

CSSL:

Chromosome segment substitution line

DAF:

Days after flowering

DBE:

Starch debranching enzyme

D-value:

Difference value

DD-value:

Difference in the D-values

GBSS:

Granule-bound starch synthase

HT:

High temperature

HTC:

High temperature condition

QTL:

Quantitative trait locus

qHAC:

QTLs for amylose content responsive to high temperatures

SBE:

Starch branching enzyme

SSS:

Soluble starch synthase

RT:

Room temperature

RTC:

Room temperature condition

LT:

Low temperature

LTC:

Low temperature condition

References

  • Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  PubMed  Google Scholar 

  • Cai XL, Wang ZY, Xing YY, Zhang JL, Hong MM (1998) Aberrant splicing of intron 1 leads to the heterogeneous 5′ UTR and decreased expression of waxy gene in rice cultivars of intermediate amylose content. Plant J 14:459–465

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Wang M, Ouwerkerk PBF (2012) Molecular and environmental factors determining grain quality in rice. Food Energy Security 1:111–132

    Article  Google Scholar 

  • Cheng F, Zhong L, Zhao N, Liu Y, Zhang G (2005) Temperature induced changes in the starch components and biosynthetic enzymes of two rice varieties. Plant Growth Regul 46:87–95

    Article  CAS  Google Scholar 

  • Hakata M, Kuroda M, Miyashita T, Yamaguchi T, Kojima M, Sakakibara H, Mitsui T, Yamakawa H (2012) Suppression of alpha-amylase genes improves quality of rice grain ripened under high temperature. Plant Biotechnol J 10:1110–1117

    Article  CAS  PubMed  Google Scholar 

  • Haleyand CS, Knott SA (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69:315–324

    Article  Google Scholar 

  • Hirano HY, Sano Y (1998) Enhancement of Wx gene expression and the accumulation of amylose in response to cool temperatures during seed development in rice. Plant Cell Physiol 39:807–812

    Article  CAS  Google Scholar 

  • Hori Y, Fujimoto R, Sato Y, Nishio T (2007) A novel wx mutation caused by insertion of a retrotransposon-like sequence in a glutinous cultivar of rice (Oryza sativa). Theor Appl Genet 115:217–224

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2007) In: IPCC fourth assessment report: climate change 2007 (AR4)

  • Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651

    Article  CAS  PubMed  Google Scholar 

  • James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6:215–222

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Dian W, Wu P (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

    Article  CAS  PubMed  Google Scholar 

  • Juliano B (1971) A simplified assay for milled-rice amylose. Cereal Sci Today 16:334–340

    Google Scholar 

  • Juliano B (1985) Criteria and test for rice grain quality. In: Juliano B (ed) Rice chemistry and technology. American Association of Cereal Chemists, Saint Paul, Minnesota, pp 443–513

    Google Scholar 

  • Larkin PD, Park WD (1999) Transcript accumulation and utilization of alternate and non-consensus splice sites in rice granule-bound starch synthase are temperature-sensitive and controlled by a single-nucleotide polymorphism. Plant Mol Biol 40:719–727

    Article  CAS  PubMed  Google Scholar 

  • Lin SK, Chang MC, Tsai YG, Lur HS (2005) Proteomic analysis of the expression of proteins related to rice quality during caryopsis development and the effect of high temperature on expression. Proteomics 5:2140–2156

    Article  CAS  PubMed  Google Scholar 

  • Liu DR, Huang WX, Cai XL (2013) Oligomerization of rice granule-bound starch synthase 1 modulates its activity regulation. Plant Sci 210:141–150

    Article  CAS  PubMed  Google Scholar 

  • Lumdubwong N, Seib PA (2000) Rice starch isolation by alkaline protease digestion of wet-milled rice flour. J Cereal Sci 31:63–74

    Article  CAS  Google Scholar 

  • Ma Q, Li Y, Tian X, Yan S, Lei W, Nakata N (2009) Influence of high temperature stress on composition and accumulation configuration of storage protein in rice. Sci Agric Sin 42:714–718

    CAS  Google Scholar 

  • Mitsui T, Shiraya T, Kaneko K, Wada K (2013) Proteomics of rice grain under high temperature stress. Front Plant Sci 4:36

    Article  PubMed Central  PubMed  Google Scholar 

  • Nakamura Y (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol 30:833–839

    CAS  Google Scholar 

  • 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 101:9971–9975

    Article  CAS  PubMed  Google Scholar 

  • Sano Y (1984) Differential regulation of waxy gene expression in rice endosperm. Theor Appl Genet 68:467–473

    Article  CAS  PubMed  Google Scholar 

  • She KC, Kusano H, Koizumi K, Yamakawa H, Hakata M, Imamura T, Fukuda M, Naito N, Tsurumaki Y, Yaeshima M, Tsuge T, Matsumoto K, Kudoh M, Itoh E, Kikuchi S, Kishimoto N, Yazaki J, Ando T, Yano M, Aoyama T, Sasaki T, Satoh H, Shimada H (2010) A novel factor FLOURY ENDOSPERM2 is involved in regulation of rice grain size and starch quality. Plant Cell 22:3280–3294

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Su Y, Rao Y, Hu S, Yang Y, Gao Z, Zhang G, Liu J, Hu J, Yan M, Dong G, Zhu L, Guo L, Qian Q, Zeng D (2011) Map-based cloning proves qGC-6, a major QTL for gel consistency of japonica/indica cross, responds by Waxy in rice (Oryza sativa L.). Theor Appl Genet 123:859–867

    Article  PubMed  Google Scholar 

  • Tian Z, Qian Q, Liu Q, Yan M, Liu X, Yan C, Liu G, Gao Z, Tang S, Zeng D, Wang Y, Yu J, Gu M, Li J (2009) Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proc Natl Acad Sci 106:21760–21765

    Article  CAS  PubMed  Google Scholar 

  • Wang ZY, Zheng FQ, Shen GZ, Gao JP, Snustad DP, Li MG, Zhang JL, Hong MM (1995) The amylose content in rice endosperm is related to the post-transcriptional regulation of the waxy gene. Plant J 7:613–622

    Article  CAS  PubMed  Google Scholar 

  • Wei KS, Zhang QF, Cheng FM, Zhong LJ, Chen N, Xie LH (2009) Expression profiles of rice soluble starch synthase isoform genes in response to high temperature stress at filling stage. Acta Agron Sin 35:18–24

    Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang H, Dong H, Yao H, Xiang Y, Tan X, Fang Y, Deng Y, Jin Q, Daniel C, Jiang Y, Dai C, Yan W, Li D (2005) Isolation of total RNA from rice endosperm and expression of important genes related to grain quality in rice (Oryza sativa). Chinese J Rice Sci 19:105–110

    CAS  Google Scholar 

  • Zhang G, Wang S, You J, Wang Q, Ding Y, Ji Z (2006) Effect of higher temperature in different filling stages on rice qualities. Acta Agron Sin 32:283–287

    CAS  Google Scholar 

  • Zhang H, Zhang CQ, Sun ZZ, Yu W, Gu MH, Liu QQ, Li YS (2011a) A major locus qS12, located in a duplicated segment of chromosome 12, causes spikelet sterility in an indica–japonica rice hybrid. Theor Appl Genet 123:1247–1256

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhao Q, Sun ZZ, Zhang CQ, Feng Q, Tang SZ, Liang GH, Gu MH, Han B, Liu QQ (2011b) Development and high-throughput genotyping of substitution lines carrying the chromosome segments of indica 9311 in the background of japonica Nipponbare. J Genet Genomics 38:603–611

    Article  CAS  PubMed  Google Scholar 

  • Zhong LJ, Cheng FM, Wen X, Sun ZX, Zhang GP (2005) The deterioration of eating and cooking quality caused by high temperature during grain filling in early-season indica rice cultivars. J Agron Crop Sci 191:218–225

    Article  Google Scholar 

  • Zhu LJ, Liu QQ, Sang Y, Gu MH, Shi YC (2010) Underlying reasons for waxy rice flours having different pasting properties. Food Chem 120:94–100

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Jian Hua for commenting on the manuscript (Department of Plant Biology, Cornell University, Ithaca, New York). We thank Professor Xiuling Cai and Dr. Derui Liu (Institute of Plant physiology and ecology, CAS) for supervising the enzyme activity assay. This work was supported by Ministry of Science and Technology (2012AA10A302 and 2012CB944803), China Postdoctoral Science Foundation (2013M541799), Zhejiang Provincial Postdoctoral Science Foundation (Bsh1202081), Jiangsu Natural Science Foundation (BK2012010) and Scientific Program of Zhejiang Academy of Agricultural Sciences of China.

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Authors and Affiliations

  1. State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China

    Hua Zhang, Lian Duan, Ji-Song Dai & Ying Zhu

  2. Key Laboratory of Plant Functional Genomics of the Ministry of Education, Jiangsu Key Laboratory of Crop Genetics and Physiology, College of Agriculture, Yangzhou University, Yangzhou, 225009, China

    Chang-Quan Zhang, Juan Li, Ming-Hong Gu & Qiao-Quan Liu

  3. College of Chemistry and Life Science, Zhejiang Normal University, Jinhua, 321004, China

    Lian Duan

  4. College of Life Science, Anhui Agricultural University, Heifei, 230036, China

    Ji-Song Dai

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  1. Hua Zhang
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  2. Lian Duan
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  3. Ji-Song Dai
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  4. Chang-Quan Zhang
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  5. Juan Li
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Corresponding authors

Correspondence to Qiao-Quan Liu or Ying Zhu.

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Communicated by T. Sasaki.

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Zhang, H., Duan, L., Dai, JS. et al. Major QTLs reduce the deleterious effects of high temperature on rice amylose content by increasing splicing efficiency of Wx pre-mRNA. Theor Appl Genet 127, 273–282 (2014). https://doi.org/10.1007/s00122-013-2216-4

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  • DOI: https://doi.org/10.1007/s00122-013-2216-4

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