Skip to main content
SpringerLink
Log in

The wheat (T. aestivum) sucrose synthase 2 gene (TaSus2) active in endosperm development is associated with yield traits

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Sucrose synthase catalyzes the reaction sucrose + UDP → UDP-glucose + fructose, the first step in the conversion of sucrose to starch in endosperm. Previous studies identified two tissue-specific, yet functionally redundant, sucrose synthase (SUS) genes, Sus1 and Sus2. In the present study, the wheat Sus2 orthologous gene (TaSus2) series was isolated and mapped on chromosomes 2A, 2B, and 2D. Based on sequencing in 61 wheat accessions, three single-nucleotide polymorphisms (SNPs) were detected in TaSus2-2B. These formed two haplotypes (Hap-H and Hap-L), but no diversity was found in either TaSus2-2A or TaSus2-2D. Based on the sequences of the two haplotypes, we developed a co-dominant marker, TaSus2-2B tgw , which amplified 423 or 381-bp fragments in different wheat accessions. TaSus2-2B tgw was located between markers Xbarc102.2 and Xbarc91 on chromosome 2BS in a RIL population from Xiaoyan 54 × Jing 411. Association analysis suggested that the two haplotypes were significantly associated with 1,000 grain weight (TGW) in 89 modern wheat varieties in the Chinese mini-core collection. Mean TGW difference between the two haplotypes over three cropping seasons was 4.26 g (varying from 3.71 to 4.94 g). Comparative genomics analysis detected major kernel weight QTLs not only in the chromosome region containing TaSus2-2B tgw, but also in the collinear regions of TaSus2 on rice chromosome 7 and maize chromosome 9. The preferred Hap-H haplotype for high TGW underwent very strong positive selection in Chinese wheat breeding, but not in Europe. The geographic distribution of Hap-H was perhaps determined by both latitude and the intensity of selection in wheat breeding.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abler BSB, Edwards MD, Stuber CW (1991) Isoenzymatic identification of quantitative trait loci in crosses of elite maize inbreds. Crop Sci 31:267–274

    Article  CAS  Google Scholar 

  • Barratt DHP, Barber L, Kruger NJ, Smith AM, Wang TL, Martin C (2001) Multiple, distinct isoforms of sucrose synthase in pea. Plant Physiol 127:655–664

    Article  PubMed  CAS  Google Scholar 

  • Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409

    Article  PubMed  CAS  Google Scholar 

  • Brondani C, Rangel N, Brondani V, Ferreira E (2002) QTL mapping and introgression of yield-related traits from Oryza glumaepatula to cultivated rice (Oryza sativa) using microsatellite markers. Theor Appl Genet 104:1192–1203

    Article  PubMed  CAS  Google Scholar 

  • Carlson SJ, Chourey PS, Helentjaris T, Datta R (2002) Gene expression studies on developing kernels of maize sucrose synthase (SuSy) mutants show evidence for a third SuSy gene. Plant Mol Biol 49:15–29

    Article  PubMed  CAS  Google Scholar 

  • Causse M, Rocher JP, Henry AM, Charcosset A, Prioul JL, de Vienne D (1995) Genetic dissection of the relationship between carbon metabolism and early growth in maize, with emphasis on key-enzyme loci. Mol Breed 1:259–272

    Article  CAS  Google Scholar 

  • Chevalier P, Lingle SE (1983) Sugar metabolism in developing kernels of wheat and barley. Crop Sci 23:272–277

    Article  CAS  Google Scholar 

  • Chourey PS, Nelson OE (1976) The enzymatic deficiency conditioned by the shrunken-1 mutation in maize. Biochem Genet 14:1041–1055

    Article  PubMed  CAS  Google Scholar 

  • Chourey PS, Taliercio EW, Carlson SJ, Ruan YL (1998) Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol Gen Genet 259:88–96

    Article  PubMed  CAS  Google Scholar 

  • Dale EM, Housley TL (1986) Sucrose synthase activity in developing wheat endosperms differing in maximum weight. Plant Physiol 82:7–10

    Article  PubMed  CAS  Google Scholar 

  • Dong YS, Cao YS, Zhang XY, Liu SC, Wang LF, You GX, Pang BS, Li LH, Jia JZ (2003) Development of candidate core collections in Chinese common wheat germplasm. J Plant Genet Res 4:1–8 (in Chinese)

    Google Scholar 

  • Drenkard E, Richter BG, Rozen S, Stutius LM, Angell NA, Mindrinos M, Cho RJ, Oegner PJ, Davis RW, Ausubel FM (2000) A simple procedure for the analysis of single nucleotide polymorphisms facilitates map-based cloning in Arabidopsis. Plant Physiol 124:1483–1492

    Article  PubMed  CAS  Google Scholar 

  • Fallahi H, Scofield GN, Badger MR, Chow WS, Furbank RT, Ruan YL (2008) Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development. J Exp Bot 59:3283–3295

    Article  PubMed  CAS  Google Scholar 

  • Flint-Garcia S, Jeffry M, Thornsberry ES, Buckler IV (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  PubMed  CAS  Google Scholar 

  • Guo ZA, Song YX, Zhou RH, Ren ZL, Jia JZ (2010) Discovery, evaluation and distribution of haplotypes of the wheat Ppd-D1 gene. New Phytol 185:841–851

    Article  PubMed  CAS  Google Scholar 

  • Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Mol Biol 47:29–51

    Article  PubMed  CAS  Google Scholar 

  • Hao CY, Wang LF, Zhang XY, You GX, Dong YS, Jia JZ, Liu X, Shang XW, Liu SC, Cao YS (2006) Genetic diversity in Chinese modern wheat varieties revealed by microsatellite markers. Sci China C Life Sci 49:218–226

    Article  PubMed  CAS  Google Scholar 

  • Hao CY, Dong YS, Wang LF et al (2008) Genetic diversity and construction of core collection in Chinese wheat genetic resources. Chinese Sci Bull 53:1518–1526

    Article  CAS  Google Scholar 

  • Harada T, Satoh S, Yoshioka T, Ishizawa K (2005) Expression of sucrose synthase genes involved in enhanced elongation of pondweed (Potamogeton distinctus) turions under anoxia. Annals Bot 96:683–692

    Article  CAS  Google Scholar 

  • Hayashi K, Hashimoto N, Daigen M, Ashikawa I (2004) Development of PCR-based SNP markers for rice blast resistance genes at the Piz locus. Theor Appl Genet 108:1212–1220

    Article  PubMed  CAS  Google Scholar 

  • Hayashi K, Yoshida H, Ashikawa I (2006) Development of PCR-based allele-specific and InDel marker sets for nine rice blast resistance genes. Theor Appl Genet 113:251–260

    Article  PubMed  CAS  Google Scholar 

  • He ZH, Rajaram S, Xin ZY, Huang GZ (eds) (2001) A history of wheat breeding in China. CIMMYT, Mexico DF, Mexico

    Google Scholar 

  • Hirose T, Scofield GN, Terao T (2008) An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Sci 174:534–543

    CAS  Google Scholar 

  • Horst I, Welham T, Kelly S, Kaneko T, Sato S, Tabata S, Parniske M, Wang TL (2007) TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol 144:806–820

    Article  PubMed  CAS  Google Scholar 

  • Housley TL, Kirkeis AW, Ohm HW, Patterson FL (1981) An evaluation of seed growth in soft red winter wheat. Can J Plant Sci 61:525–534

    Article  CAS  Google Scholar 

  • Huang J, Chen J, Yu W, Shyur L, Wang A, Sung H, Lee P, Su JC (1996) Complete structures of three rice sucrose synthase isogenes and differential regulation of their expressions. Biosci Biotechnol Biochem 60:233–239

    Article  PubMed  CAS  Google Scholar 

  • Hurkman WJ, McCue KF, Altenbach SB, Korn A et al (2003) Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm. Plant Sci 164:873–881

    Article  CAS  Google Scholar 

  • Jin SB, Zhuang QS, Wu ZS, Huang PM, Bo YJ (1983) Chinese wheat varieties and their genealogies. China Agricultural Publishing House, Beijing, China (in Chinese)

    Google Scholar 

  • Kanazin D, Talbert VH, Blake T (2000) Electrophoretic detection of single-nucleotide polymorphisms. Biotechniques 28:710–716

    PubMed  Google Scholar 

  • Kato T (1995) Change of sucrose synthase activity in developing endosperm of rice cultivars. Crop Sci 35:827–831

    Article  CAS  Google Scholar 

  • Kim MY, Van K, Lestari P, Moon JK, Lee SH (2005) SNP identification and SNAP marker development for a GmNARK gene controlling supernodulation in soybean. Theor Appl Genet 110:1003–1010

    Article  PubMed  CAS  Google Scholar 

  • King SP, Lunn JE, Furbank RT (1997) Carbohydrate content and enzyme metabolism in developing canola siliques. Plant Physiol 114:153–160

    PubMed  CAS  Google Scholar 

  • Kumar R, Singh R (1980) The relationship of starch metabolism to grain size in wheat. Phytochemistry 19:2299–2303

    Article  CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 21:185–199

    Google Scholar 

  • Maraña C, García-Olmedo F, Carbonero P (1990) Differential expression of two types of sucrose synthase-encoding genes in wheat in response to anaerobiosis, cold shock and light. Gene 88:167–172

    Article  PubMed  Google Scholar 

  • Maraña C, Garcla-Olmedo F, Carbonero P (1988) Linked sucrose synthase genes in group-7 chromosomes in hexaploid wheat (Triticum aestivum L.). Gene 63:253–260

    Article  PubMed  Google Scholar 

  • Martinez de Ilarduya O, Vicente-Carbajosa J, Sanchez de la Hoz P, Carbonero P (1993) Sucrose synthase genes in barley. cDNA cloning of the Ss2 type and tissue-specific expression of Ss1 and Ss2. FEBS Lett 320:177–181

    Article  PubMed  CAS  Google Scholar 

  • Melchinger AE, Utz HF, Schon CC (1998) Quantitative trait locus (QTL) mapping using different testers and independent population samples in maize reveals low power of QTL detection and large bias in estimates of QTL effects. Genetics 149:383–403

    PubMed  CAS  Google Scholar 

  • Nolte KD, Koch KE (1993) Companion-cell specific localization of sucrose synthase in zones of phloem loading and unloading. Plant Physiol 101:899–905

    PubMed  CAS  Google Scholar 

  • Pritchard JK (2001) Deconstructing maize population structure. Nat Genet 28:203–204

    Article  PubMed  CAS  Google Scholar 

  • Rouhier H, Usuda H (2001) Spatial and temporal distribution of sucrose synthase in the radish hypocotyl in relation to thickening growth. Plant Cell Physiol 42:583–593

    Article  PubMed  CAS  Google Scholar 

  • Ruan YL, Chourey PS (1998) A fiberless seed mutation in cotton is associated with lack of fiber cell initiation in ovule epidermis and alterations in sucrose synthase expression and carbon partitioning in developing seeds. Plant Physiol 118:399–406

    Article  PubMed  CAS  Google Scholar 

  • Ruan YL, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. Plant Cell 15:952–964

    Article  PubMed  CAS  Google Scholar 

  • Sánchez de la Hoz P, Vicente-Carbajosa J, Mena M, Carbonero P (1992) Homologous sucrose synthase genes in barley (Hordeum vulgare) are located in chromosomes 7H (syn.1) and 2H. Evidence for a gene translocation? FEBS Lett 310:46–50

    Article  PubMed  Google Scholar 

  • Sharp PJ, Kreis M, Shewry PR, Gale MD (1988) Location of b-amylase sequence in wheat and its relatives. Theor Appl Genet 75:289–290

    Article  Google Scholar 

  • Shaw JR, Ferl RJ, Baier J, St Clair D, Carson C, McCarty DR, Hannah LC (1994) Structural features of the maize susl gene and protein. Plant Physiol 106:1659–1665

    Article  PubMed  CAS  Google Scholar 

  • Shin JH, Kwon SJ, Lee JK, Min HK, Kim NS (2006) Genetic diversity of maize kernel starch-synthesis genes with SNAPs. Genome 49:1287–1296

    Article  PubMed  CAS  Google Scholar 

  • Sommer SS, Groszbar AR, Bottema CDK (1992) PCR amplification of specific alleles (PASA) is a general method for rapidly detecting known single base-pair changes. Biotechniques 12:82–87

    PubMed  CAS  Google Scholar 

  • Sourdille P, Singh S, Cadalen T, Brown-Guedira GL, Gay G, Qi L, Gill BS, Dufour P, Murigneux A, Bernard M (2004) Microsatellite-based deletion bin system for the establishment of genetic-physical map relationships in wheat (Triticum aestivum L.). Funct Integr Genomics 4:12–25

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Loboda T, Sung SJS, CCJr B (1992) Sucrose synthase in wild tomato, Lycopersicon chmielewskii, and tomato fruit sink strength. Plant Physiol 98:1163–1169

    Article  PubMed  CAS  Google Scholar 

  • Takano-Kai N, Jiang H, Kubo T, Sweeney M, Matsumoto T, Kanamori H, Padhukasahasram B, Bustamante C, Yoshimura A, Doi K, McCouch S (2009) Evolutionary history of GS3, a gene conferring grain length in rice. Genetics 182:1323–1334

    Article  PubMed  CAS  Google Scholar 

  • Tang GQ, Sturm A (1999) Antisense repression of sucrose synthase in carrot (Daucus carota L.) affects growth rather than sucrose partitioning. Plant Mol Biol 41:465–479

    Article  PubMed  CAS  Google Scholar 

  • Van Bel AJE, Knoblauch M (2000) Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse. Funct Plant Biol 27:477–487

    Article  Google Scholar 

  • Wang AY, Yu WP, Juang RH, Huang JW, Sung HY, Su JC (1992) Presence of three rice sucrose synthase genes as revealed by cloning and sequencing of cDNA. Plant Mol Biol 18:1191–1194

    Article  PubMed  CAS  Google Scholar 

  • Wei B, Jing RL, Wang CS, Jb C, Mao XG, Chang XP, Jia JZ (2009) Dreb1 genes in wheat (Triticum aestivum L.): development of functional markers and gene mapping based on SNPs. Mol Breed 23:13–22

    Article  CAS  Google Scholar 

  • Wright AF, Carothers AD, Pirastu M (1999) Population choice in mapping genes for complex diseases. Nat Genet 23:397–404

    Article  PubMed  CAS  Google Scholar 

  • Yuan CP, Li YH, Liu ZX, Guan RX, Chang RZ, Qiu LJ (2007) A method of SNP genotyping in soybean. Soybean Sci 26:447–459

    Google Scholar 

  • Zhang XY, Li CW, Wang LF, Wang HM, You GX, Dong YS (2002) An estimation of the minimum number of SSR alleles needed to reveal genetic relationships in wheat varieties. I. Information from large-scale planted varieties and cornerstone breeding parents in Chinese wheat improvement and production. Theor Appl Genet 106:112–117

    PubMed  CAS  Google Scholar 

  • Zanetti S, Winzeler M, Feuillet C, Keller B, Messmer M (2001) Genetic analysis of bread-making quality in wheat and spelt. Plant Breed 120:13–19

    Article  CAS  Google Scholar 

  • Zhuang QS (2003) Chinese wheat improvement and pedigree analysis. China Agricultural Publishing House, Beijing, China (in Chinese)

    Google Scholar 

  • Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 7:97–107

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully appreciate the help of Prof. Robert A McIntosh, University of Sydney, with English editing and discussion. Thanks were also given to the group of Prof. Tong YP and Li ZS, Institute of Genetics and Developmental Biology, CAS, for their help in mapping the haplotypes in their RIL population. Thanks were also given to Prof. Liu ZY and Yan JB, China Agricultural University; Mao L, Chinese Academy of Agricultural Sciences, for their help in comparative genetic analysis. This research was supported by the Chinese Ministry of Science and Technology (2010CB125902), funding from Ministry of Agriculture (2008ZX08009) and Modern Agricultural Technical System.

Author information

Authors and Affiliations

  1. Key Laboratory of Crop Germplasm Resources and Utilization, Ministry of Agriculture/Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Qiyan Jiang, Jian Hou, Chenyang Hao, Lanfen Wang, Yushen Dong & Xueyong Zhang

  2. Key Laboratory of Huanghuaihai Crop Genetic Improvement and Biotechnology, Ministry of Agriculture/Crop Research Institute, Qingdao Academy of Agricultural Sciences, Qingdao, 266100, China

    Hongmei Ge

Authors
  1. Qiyan Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jian Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chenyang Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lanfen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hongmei Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yushen Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xueyong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xueyong Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Alignment of partial DNA sequences of Sus2 genes from wheat 2A, 2D, and the alleles Sus2-2B-L and Sus2-2B-H located on wheat chromosome 2B. The sequence of the genome-specific primers for 2B (Sus2-SNP-185 and Sus2-SNP-227) and complementary sequence of the allele-specific primers (Sus2-SNP-589L2 and Sus2-SNP-589H2) are shadowed. The genome-specific alleles at the 3′end contained in the genome-specific primers are underlined. The allele-specific primers contain SNP2-variants (boxed) at the 3′end and, in addition, had one mismatch with the nonspecific allele at the 2nd nucleotides in the 3′-end (G-C) (DOC 35.0 kb)

Supplementary Fig. 2

The effect of mismatches within three bases of the 3′-end on the specificity of allele-specific PCR. In this test, we tried to generate allele-specific PCR primers to discriminate between Xiaoyan 54 and Jing 411 at SNP589. The incorporating mismatched bases are underlined in the sequences of the primers used in the test. The presence or absence of each PCR product was analyzed on 1.5% agarose gels. Sus2-SNP-185 and Sus2-SNP-227 were Forward primers. Sus2-SNP-589L1 (H1) primers contained SNP variants at the 3′-end; Sus2-SNP-563L2(H2), primers contained SNP variants at the 3′-end and, in addition, had one mismatch with the nonspecific allele at the 2nd nucleotide in the 3′-end; Sus2-SNP-563L3(H3) primers contained SNP variants at the 3′-end and, in addition, had two mismatches with the nonspecific allele at the 2nd and 3rd nucleotides in the 3′-end. M: 100 bp DNA ladder (Trans, BM301) (DOC 122 kb)

Supplementary Fig. 3

Genetic structure of the Chinese wheat mini-core collection (DOC 76 kb)

Supplementary Fig. 4

Genetic structure of Chinese modern varieties (DOC 176 kb)

Supplementary Fig. 5

Wheat 2B consensus map and QTLs in the consensus map (DOC 48 kb)

Supplementary Fig. 6

Orthologous of TaSus2 gene (LOC_Os07g42490) and co-localized QTLs in rice (DOC 60 kb)

Supplementary Fig. 7

Orthologous sus1 gene and co-localized QTLs in maize (DOC 33 kb)

Supplementary Fig. 8

Distribution of haplotype Hap-H and Hap-L at TaSus2-2B in different wheat ecological zones in China. (DOC 157 kb)

Supplementary Fig. 9

PCR amplification of Chinese Spring (CS) and its group 7 nullisomic-tetrasomic lines with the PCR primer pairs shown on right and the size of the amplification product on the left. M: 100 bp DNA ladder (Trans, BM301) on (a and b); 1 kb DNA ladder (Fermentas, SM0311) on (c and d). Each genome-specific primer set amplified the products from CS and each CS nullisomic-tetrasomic line (DOC 263 kb)

Supplementary Table 1

Mean measurements in three cropping seasons for agronomic traits and haplotypes (HT) at the TaSus2-2B locus of 245 wheat accessions in the mini-core collection.(Hap-H = H; Hap-L = L; heterozygote = HL; missing data = M) (XLS 121 kb)

Supplementary Table 2

Haplotypes (HT) at the TaSus2-2B locus and origins, wheat region and year of release for 348 wheat accessions in the core collection (Hap-H = H; Hap-L = L; heterozygote = HL; missing data = M) (XLS 69 kb)

Supplementary Table 3

Origins, heading date (HD), maturity date (MD) and haplotypes (HT) at the TaSus2-2B locus for 384 European wheat accessions (Hap-H = H; Hap-L = L; Heterozygote = HL; NM, cannot mature normally; NH, cannot heading normally) (XLS 82 kb)

Supplementary Table 4

Haplotypes (HT) at the TaSus2-2B locus of 184 RILs (Xiaoyan 54 × Jing 411; Hap-H = H; Hap-L = L; heterozygote = HL; missing data = M) (XLS 34 kb)

Supplementary Table 5

Geographical distribution across zones of haplotypes Hap-H and Hap-L at Tasus2-2B in Chinese modern varieties (DOC 38 kb)

Supplementary Table 6

Geographical distribution (different provinces) of haplotypes Hap-H and Hap-L at Tasus2-2B in Chinese modern varieties (DOC 40 kb)

Supplementary Table 7

Geographical distribution (different countries) of haplotypes Hap-H and Hap-L at Tasus2-2B in European wheat varieties (DOC 48 kb)

Supplementary sequences (ZIP 17 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, Q., Hou, J., Hao, C. et al. The wheat (T. aestivum) sucrose synthase 2 gene (TaSus2) active in endosperm development is associated with yield traits. Funct Integr Genomics 11, 49–61 (2011). https://doi.org/10.1007/s10142-010-0188-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-010-0188-x

Keywords

Search

Navigation