Skip to main content
Log in

Du1, encoding a novel Prp1 protein, regulates starch biosynthesis through affecting the splicing of Wx b pre-mRNAs in rice (Oryza sativa L.)

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Starch is the major component of cereal grains. In rice, starch properties determine the eating and cooking quality. The dull endosperm of rice grains is a classical morphological and agronomical trait that has long been exploited for breeding and genetics study. To understand the molecular mechanism that regulates the starch biosynthesis in rice grains, we characterized a classic rice mutant dull endosperm1 (du1) and isolated Du1 through a map-based cloning approach. Du1, encoding a member of pre-mRNA processing (Prp1) family, is expressed mainly in panicles. Du1 specifically affects the splicing efficiency of Wx b and regulates starch biosynthesis by mediating the expression of starch biosynthesis genes. Analysis of du1wx shows that Du1 acts upstream of Wx b. These results strongly suggest that Du1 may function as a regulator of the starch biosynthesis by affecting the splicing of Wx b and the expression of other genes involved in the rice starch biosynthetic pathways.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AC:

Amylose content

AGPase:

ADP-glucose pyrophosphorylase

ASV:

Alkali spreading values

BAC:

Bacterial artificial chromosome

CAPS:

Cleaved amplified polymorphic sequences

DAP:

Days after pollinating

DBE:

Starch debraching enzyme

du1 :

Dull endosperm1

Du1L:

Du1-like

GBSS:

Granule-bound starch synthase

GC:

Gel consistency

Prp:

Pre-mRNA processing

QTL:

Quantitative trait locus

SBE:

Starch branching enzyme

SR:

Serine–arginine-rich

SSS:

Soluble starch synthase

STS:

Sequence tagged site

TPR:

Tetratric peptide repeats

UTR:

Untranslated region

References

  • Aluko G, Martinez C, Tohme J, Castano C, Bergman C, Oard JH (2004) QTL mapping of grain quality traits from the interspecific cross Oryza sativa x O. glaberrima. Theor Appl Genet 109:630–639

    Article  PubMed  CAS  Google Scholar 

  • Bao JS, Sun M, Corke H (2002) Analysis of the genetic behavior of some starch properties in indica rice (Oryza sativa L.): thermal properties, gel texture, swelling volume. Theor Appl Genet 104:408–413

    Article  PubMed  CAS  Google Scholar 

  • Bao J, Kong X, Xie J, Xu L (2004) Analysis of genotypic and environmental effects on rice starch. 1. Apparent amylose content, pasting viscosity, and gel texture. J Agric Food Chem 52:6010–6016

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Chung S, McLean MR, Rymond BC (1999) Yeast ortholog of the Drosophila crooked neck protein promotes spliceosome assembly through stable U4/U6.U5 snRNP addition. RNA 5:1042–1054

    Article  PubMed  CAS  Google Scholar 

  • Eguchi T, Ashikari M, Yoshimura A, Iwata N (1998) Loci of physiological and morphological characters on RFLP linkage map in rice. Breeding Sci 48:80

    Google Scholar 

  • Fan CC, Yu XQ, Xing YZ, Xu CG, Luo LJ, Zhang Q (2005) The main effects, epistatic effects and environmental interactions of QTLs on the cooking and eating quality of rice in a doubled-haploid line population. Theor Appl Genet 110:1445–1452

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (2000) PHYLIP: Phylogeny Inference Package, v3.6. Seattle, WA

  • Frances H, Bligh J, Larkin PD, Roach PS, Jones CA, Fu H, Park WD (1998) Use of alternate splice sites in granule-bound starch synthase mRNA from low-amylose rice varieties. Plant Mol Biol 38:407–415

    Article  PubMed  CAS  Google Scholar 

  • Fujita N, Kubo A, Suh DS, Wong KS, Jane JL, Ozawa K, Takaiwa F, Inaba Y, Nakamura Y (2003) Antisense inhibition of isoamylase alters the structure of amylopectin and the physicochemical properties of starch in rice endosperm. Plant Cell Physiol 44:607–618

    Article  PubMed  CAS  Google Scholar 

  • Gao Z, Zeng D, Cui X, Zhou Y, Yan M, Huang D, Li J, Qian Q (2003) Map-based cloning of the ALK gene, which controls the gelatinization temperature of rice. Sci China Ser C 46:661–668

    Article  CAS  Google Scholar 

  • Hirano HY, Sano Y (2000) Comparison of Waxy gene regulation in the endosperm and pollen in Oryza sativa L. Genes Genet Syst 75:245–249

    Article  PubMed  CAS  Google Scholar 

  • Hirano HY, Eiguchi M, Sano Y (1998) A single base change altered the regulation of the Waxy gene at the posttranscriptional level during the domestication of rice. Mol Biol Evol 15:978–987

    PubMed  CAS  Google Scholar 

  • Isshiki M, Morino K, Nakajima M, Okagaki RJ, Wessler SR, Izawa T, Shimamoto K (1998) A naturally occurring functional allele of the rice waxy locus has a GT to TT mutation at the 5’ splice site of the first intron. Plant J 15:133–138

    Article  PubMed  CAS  Google Scholar 

  • Itoh K, Ozaki H, Okada K, Hori H, Takeda Y, Mitsui T (2003) Introduction of Wx transgene into rice wx mutants leads to both high- and low-amylose rice. Plant Cell Physiol 44:473–480

    Article  PubMed  CAS  Google Scholar 

  • Juliano BO (1971) A simplified assay for milled rice amylose. Cereal Sci Today 16:334–360

    Google Scholar 

  • Kinoshita T (1987) Report of the committee on gene symbolization, nomenclature and linkage groups. II. Registration of new gene symbols. Rice Genet Newslett 4:3–7

    Google Scholar 

  • Koh HJ, Cha KW, Heu MH (1997) Inheritance and some physicochemical properties of newly induced “low-amylose endosperm” mutants in rice. Korean J Breed 29:368–375

    Google Scholar 

  • Kubo A, Fujita N, Harada K, Matsuda T, Satoh H, Nakamura Y (1999) The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiol 121:399–410

    Article  PubMed  CAS  Google Scholar 

  • Lamb JR, Tugendreich S, Hieter P (1995) Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem Sci 20:257–259

    Article  PubMed  CAS  Google Scholar 

  • Lan L, Chen W, Lai Y, Suo J, Kong Z, Li C, Lu Y, Zhang Y, Zhao X, Zhang X, Han B, Cheng J, Xue Y (2004) Monitoring of gene expression profiles and isolation of candidate genes involved in pollination and fertilization in rice (Oryza sativa L.) with a 10K cDNA microarray. Plant Mol Biol 54:471–487

    Article  PubMed  CAS  Google Scholar 

  • Lanceras JC, Huang ZL, Naivikul O, Vanavichit A, Ruanjaichon V, Tragoonrung S (2000) Mapping of genes for cooking and eating qualities in Thai jasmine rice (KDML105). DNA Res 7:93–101

    Article  PubMed  CAS  Google Scholar 

  • Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003a) Control of tillering in rice. Nature 422:618–621

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X, Chen M, Li J (2003b) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Wang Z, Chen X, Cai X, Tang S, Yu H, Zhang J, Hong M, Gu M (2003) Stable inheritance of the antisense Waxy gene in transgenic rice with reduced amylose level and improved quality. Transgenic Res 12:71–82

    Article  PubMed  Google Scholar 

  • Lockhart SR, Rymond BC (1994) Commitment of yeast pre-mRNA to the splicing pathway requires a novel U1 small nuclear ribonucleoprotein polypeptide, Prp39p. Mol Cell Biol 14:3623–3633

    PubMed  CAS  Google Scholar 

  • Makarov EM, Makarova OV, Achsel T, Luhrmann R (2000) The human homologue of the yeast splicing factor prp6p contains multiple TPR elements and is stably associated with the U5 snRNP via protein-protein interactions. J Mol Biol 298:567–575

    Article  PubMed  CAS  Google Scholar 

  • Mou Z, He Y, Dai Y, Liu X, Li J (2000) Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12:405–418

    Article  PubMed  CAS  Google Scholar 

  • Nakamura Y (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant Cell Physiol 43:718–725

    Article  PubMed  CAS  Google Scholar 

  • Okuno K, Fuwa H., Yano M (1983) A new mutant gene lowering amylose content in endosperm starch of rice, Oryza Sativa L. Jpn J Breed 33:387–394

    CAS  Google Scholar 

  • Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Qian Q, Lin J, Song J, Yang C (1991) Genetic analysis of dull and its effect on kernal traits. Annual Report China National Rice Research Institute, p 3

  • Qian Q, Zhu X, Zeng D, Xiong Z, Min S (1996) The improvement of three new-type rice with special embryo and endosperm (in Chinese). Zhejiang Agricult Sci 4:155–156

    Google Scholar 

  • Sano Y, Maekawa M, Kikuchi H (1985) Temperature effects on the Wx protein level an amylose content in the endosperm of rice. J Hered 76:221–223

    CAS  Google Scholar 

  • Satoh H, Omura T (1981) New endosperm mutations induced by chemical mutagen in rice, Oryza sativa L. Japan J Breed 31:316–326

    CAS  Google Scholar 

  • Satoh H, Omura T (1986) Mutagenesis in rice by treating fertilized egg cells with nitroso compounds. Rice Genet, p 707–717

  • Septiningsih EM, Trijatmiko KR, Moeljopawiro S, McCouch SR (2003) Identification of quantitative trait loci for grain quality in an advanced backcross population derived from the Oryza sativa variety IR64 and the wild relative O. rufipogon. Theor Appl Genet 107:1433–1441

    Article  PubMed  CAS  Google Scholar 

  • Simpson GG, Filipowicz W (1996) Splicing of precursors to mRNA in higher plants: mechanism, regulation and sub-nuclear organisation of the spliceosomal machinery. Plant Mol Biol 32:1–41

    Article  PubMed  CAS  Google Scholar 

  • Tan YF, Li JX, Yu SB, Xing YZ, Xu CG, Zhang Q (1999) The three important traits for cooking and eating quality of rice grains are controlled by a single locus in an elite rice hybrid, Shanyou 63. Theor Appl Genet 99:642–648

    Article  CAS  Google Scholar 

  • Terada R, Nakajima M, Isshiki M, Okagaki RJ, Wessler SR, Shimamoto K (2000) Antisense waxy genes with highly active promoters effectively suppress waxy gene expression in transgenic rice. Plant Cell Physiol 41:881–888

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Urushiyama S, Tani T, Ohshima Y (1997) The prp1 gene required for pre-mRNA splicing in Schizosaccharomyces pombe encodes a protein that contains TPR motifs and is similar to Prp6p of budding yeast. Genetics 147:101–115

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Yano M, Okuno K, Satoh H, Omura T (1988) Chromosomal location of genes conditioning low amylose content of endosperm starches in rice, Oryza sativa L. Theor Appl Genet 76:183–189

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Zhixi Tian for the assistance in the analyses of starch properties and his critical comments on the manuscript, Kyushu University for providing the original du1 seeds, Bin Han (National Center for Gene Research, Chinese Academy of Sciences) for providing BAC and cDNA clones. This work was supported by grants from the State Key Basic Research Program (2005CB1208), the National Natural Science Foundation of China (30530470, 30425034), Natural Science Foundation of Zhejiang Province (Y304442).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Qian Qian or Jiayang Li.

Electronic supplementary material

Below are the electronic supplementary materials

11103_2007_9186_MOESM1_ESM.tif

Structural features of the Du1 gene. Numbers at left refer to the position of nucleotides. Red stands for the mutation in du1, blue for polymorphic bases between indica and japonica subspecies, pink for the N terminal domain, and green or orange for the TPR motifs (TIF 2,497 KB)

Alignment of deduced amino acid sequences of Du1 and Du1L. The identical amino acid was marked (TIF 976 KB)

Comparison of the grain ASV between du1 and the wild type XS11 or the complemented transgenic line ZD6-3 (TIF 2,163 KB)

ESM4 (DOC 144 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeng, D., Yan, M., Wang, Y. et al. Du1, encoding a novel Prp1 protein, regulates starch biosynthesis through affecting the splicing of Wx b pre-mRNAs in rice (Oryza sativa L.). Plant Mol Biol 65, 501–509 (2007). https://doi.org/10.1007/s11103-007-9186-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-007-9186-3

Keywords

Navigation