Abstract
Key message
We isolated a novel allele associated with grain length and grain weight in wheat, TaGL3-5A-G. The TaGL3-5A-G allele frequency is low in wheat, so it has potential for breeding.
Abstract
Selection of large-grain wheat showing big grain sink potential and strong sink activity is becoming an important objective in breeding programs. Here, we cloned a wheat TaGL3-5A gene that was orthologous to rice GL3 and was phylogenetically clustered with both monocot PPKL1 and its expression pattern was similar to grain size change at early and middle stages of seed development. The isolated TaGL3-5A genomic sequence was 10,227 bp long and included 21 exons and 20 introns. Alignment of the TaGL3-5A sequences in Beinong 6 and Yanda 1817 showed a G/A substitution in the 11th exon (position 5946) that would lead to an amino acid change (Met/Ile). Subsequently, a KASP marker was designed based on this SNP. Genotyping of RILs showed that TaGL3-5A was located on the wheat 5AL chromosome and was colocated with a significant grain length QTL in three independent environments and mean value. Association analysis revealed that the TaGL3-5A-G allele was significantly correlated with longer grains and higher thousand-kernel weight. Haplotype association analysis indicated that TaGL3-5A-G could enhance grain traits in combination with TaGS5-3A and TaGW2-6B. The frequency of TaGL3-5A-G was higher in modern cultivars than in landraces but was still low in major Chinese wheat production areas. Additionally, the frequency of the TaGL3-5A-G allele in hexaploid wheat was slightly lower than in Triticum dicoccoides and much lower than in Triticum turgidum. Hence, T. dicoccoides and T. turgidum represent valuable resources for transferring the TaGL3-5A-G allele into common wheat, which should lead to longer grain length.
Similar content being viewed by others
References
Abbo S, van-Oss RP, Gopher A, Saranga Y, Ofner I, Peleg Z (2014) Plant domestication versus crop evolution: a conceptual framework for cereals and grain legumes. Trends Plant Sci 19:351–360. https://doi.org/10.1016/j.tplants.2013.12.002
Ahn S, Anderson JA, Sorrells ME, Tanksley SD (1993) Homoeologous relationships of rice, wheat and maize chromosomes. Mol Gen Genet 241:483–490. https://doi.org/10.1007/bf00279889
Barrero RA, Bellgard M, Zhang X (2011) Diverse approaches to achieving grain yield in wheat. Funct Integr Genom 11:37–48. https://doi.org/10.1007/s10142-010-0208-x
Bednarek J, Boulaflous A, Girousse C, Ravel C, Tassy C, Barret P, Bouzidi MF, Mouzeyar S (2012) Down-regulation of the TaGW2 gene by RNA interference results in decreased grain size and weight in wheat. J Exp Bot 63:5945–5955. https://doi.org/10.1093/jxb/ers249
Belkhadir Y, Chory J (2006) Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science 314:1410–1411. https://doi.org/10.1126/science.1134040
Bevan MW, Uauy C, Wulff BBH, Zhou J, Krasileva K, Clark MD (2017) Genomic innovation for crop improvement. Nature 543:346. https://doi.org/10.1038/nature22011
Campbell KG, Bergman CJ, Gualberto DG, Anderson JA, Giroux MJ, Hareland G, Fulcher RG, Sorrells ME, Finney PL (1999) Quantitative trait loci associated with kernel traits in a soft × hard wheat cross. Crop Sci 39:1184–1195. https://doi.org/10.2135/cropsci1999.0011183X003900040039x
Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, da Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci USA 110:8057–8062. https://doi.org/10.1073/pnas.1217133110
Evans L, Dunstone R (1970) Some physiological aspects of evolution in wheat. Aust J Biol Sci 23:725–742. https://doi.org/10.1071/BI9700725
Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Li X, Zhang Q (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171. https://doi.org/10.1007/s00122-006-0218-1
Farkas I, Dombrádi V, Miskei M, Szabados L, Koncz C (2007) Arabidopsis PPP family of serine/threonine phosphatases. Trends Plant Sci 12:169–176. https://doi.org/10.1016/j.tplants.2007.03.003
Gegas VC, Nazari A, Griffiths S, Simmonds J, Fish L, Orford S, Sayers L, Doonan JH, Snape JW (2010) A genetic framework for grain size and shape variation in wheat. Plant Cell 22:1046–1056. https://doi.org/10.1105/tpc.110.074153
Huang Y, Kong Z, Wu X, Cheng R, Yu D, Ma Z (2015) Characterization of three wheat grain weight QTLs that differentially affect kernel dimensions. Theor Appl Genet 128:2437–2445. https://doi.org/10.1007/s00122-015-2598-6
Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338. https://doi.org/10.1146/annurev.genet.39.073003.114725
Kuchel H, Williams KJ, Langridge P, Eagles HA, Jefferies SP (2007) Genetic dissection of grain yield in bread wheat. I. QTL analysis. Theor Appl Genet 115:1029–1041. https://doi.org/10.1007/s00122-007-0629-7
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, Shao D, Xu C, Li X, Xiao J, He Y, Zhang Q (2011) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43:1266–1269. https://doi.org/10.1038/ng.977
Ling H-Q, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, Lou X, Chen J, Feng M, Jian J, Zhang X, Luo G, Jiang Y, Liu J, Wang Z, Sha Y, Zhang B, Wu H, Tang D, Shen Q, Xue P, Zou S, Wang X, Liu X, Wang F, Yang Y, An X, Dong Z, Zhang K, Zhang X, Luo M-C, Dvorak J, Tong Y, Wang J, Yang H, Li Z, Wang D, Zhang A, Wang J (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496:87. https://doi.org/10.1038/nature11997
Long X-Y, Wang J-R, Ouellet T, Rocheleau H, Wei Y-M, Pu Z-E, Jiang Q-T, Lan X-J, Zheng Y-L (2010) Genome-wide identification and evaluation of novel internal control genes for Q-PCR based transcript normalization in wheat. Plant Mol Biol 74:307–311. https://doi.org/10.1007/s11103-010-9666-8
Lopes MS, Reynolds MP, Manes Y, Singh RP, Crossa J, Braun HJ (2012) Genetic yield gains and changes in associated traits of CIMMYT spring bread wheat in a “historic” set representing 30 years of breeding. Crop Sci 52:1123–1131. https://doi.org/10.2135/cropsci2011.09.0467
Ma L, Li T, Hao C, Wang Y, Chen X, Zhang X (2016) TaGS5-3A, a grain size gene selected during wheat improvement for larger kernel and yield. Plant Biotechnol J 14:1269–1280. https://doi.org/10.1111/pbi.12492
Mora-García S, Vert G, Yin Y, Caño-Delgado A, Cheong H, Chory J (2004) Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev 18:448–460. https://doi.org/10.1101/gad.1174204
Qi P, Lin YS, Song XJ, Shen JB, Huang W, Shan JX, Zhu MZ, Jiang L, Gao JP, Lin HX (2012) The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res 22:1666–1680. https://doi.org/10.1038/cr.2012.151
Qin L, Hao C, Hou J, Wang Y, Li T, Wang L, Ma Z, Zhang X (2014) Homologous haplotypes, expression, genetic effects and geographic distribution of the wheat yield gene TaGW2. BMC Plant Biol 14:107. https://doi.org/10.1186/1471-2229-14-107
Quarrie SA, Steed A, Calestani C, Semikhodskii A, Lebreton C, Chinoy C, Steele N, Pljevljakusić D, Waterman E, Weyen J, Schondelmaier J, Habash DZ, Farmer P, Saker L, Clarkson DT, Abugalieva A, Yessimbekova M, Turuspekov Y, Abugalieva S, Tuberosa R, Sanguineti M-C, Hollington PA, Aragués R, Royo A, Dodig D (2005) A high-density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring × SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110:865–880. https://doi.org/10.1007/s00122-004-1902-7
Rasheed A, Wen W, Gao F, Zhai S, Jin H, Liu J, Guo Q, Zhang Y, Dreisigacker S, Xia X, He Z (2016) Development and validation of KASP assays for genes underpinning key economic traits in bread wheat. Theor Appl Genet 129:1843–1860. https://doi.org/10.1007/s00122-016-2743-x
Reif JC, Zhang P, Dreisigacker S, Warburton ML, van Ginkel M, Hoisington D, Bohn M, Melchinger AE (2005) Wheat genetic diversity trends during domestication and breeding. Theor Appl Genet 110:859–864. https://doi.org/10.1007/s00122-004-1881-8
Sadras VO (2007) Evolutionary aspects of the trade-off between seed size and number in crops. Field Crops Research 100(2–3):125–138. https://doi.org/10.1016/j.fcr.2006.07.004
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Simmonds J, Scott P, Brinton J, Mestre TC, Bush M, Del Blanco A, Dubcovsky J, Uauy C (2016) A splice acceptor site mutation in TaGW2-A1 increases thousand grain weight in tetraploid and hexaploid wheat through wider and longer grains. Theor Appl Genet 129:1099–1112. https://doi.org/10.1007/s00122-016-2686-2
Singh NK, Dalal V, Batra K, Singh BK, Chitra G, Singh A, Ghazi IA, Yadav M, Pandit A, Dixit R, Singh PK, Singh H, Koundal KR, Gaikwad K, Mohapatra T, Sharma TR (2007) Single-copy genes define a conserved order between rice and wheat for understanding differences caused by duplication, deletion, and transposition of genes. Funct Integr Genom 7:17–35. https://doi.org/10.1007/s10142-006-0033-4
Slafer GA (2003) Genetic basis of yield as viewed from a crop physiologist’s perspective. Ann Appl Biol 142:117–128. https://doi.org/10.1111/j.1744-7348.2003.tb00237.x
Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630. https://doi.org/10.1038/ng2014
Song XJ, Kuroha T, Ayano M, Furuta T, Nagai K, Komeda N, Segami S, Miura K, Ogawa D, Kamura T, Suzuki T, Higashiyama T, Yamasaki M, Mori H, Inukai Y, Wu J, Kitano H, Sakakibara H, Jacobsen SE, Ashikari M (2015) Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proc Natl Acad Sci USA 112:76–81. https://doi.org/10.1073/pnas.1421127112
Su Z, Hao C, Wang L, Dong Y, Zhang X (2011) Identification and development of a functional marker of TaGW2 associated with grain weight in bread wheat (Triticum aestivum L.). Theor Appl Genet 122:211–223. https://doi.org/10.1007/s00122-010-1437-z
Sun X-Y, Wu K, Zhao Y, Kong F-M, Han G-Z, Jiang H-M, Huang X-J, Li R-J, Wang H-G, Li S-S (2008) QTL analysis of kernel shape and weight using recombinant inbred lines in wheat. Euphytica 165:615. https://doi.org/10.1007/s10681-008-9794-2
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. https://doi.org/10.1534/genetics.109.103002
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035. https://doi.org/10.1073/pnas.0404206101
Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822. https://doi.org/10.1126/science.1183700
Tyagi S, Mir RR, Kaur H, Chhuneja P, Ramesh B, Balyan HS, Gupta PK (2014) Marker-assisted pyramiding of eight QTLs/genes for seven different traits in common wheat (Triticum aestivum L.). Mol Breed 34:167–175. https://doi.org/10.1007/s11032-014-0027-1
Wang RX, Hai L, Zhang XY, You GX, Yan CS, Xiao SH (2009) QTL mapping for grain filling rate and yield-related traits in RILs of the Chinese winter wheat population Heshangmai × Yu8679. Theor Appl Genet 118:313–325. https://doi.org/10.1007/s00122-008-0901-5
Wang C, Chen S, Yu S (2011) Functional markers developed from multiple loci in GS3 for fine marker-assisted selection of grain length in rice. Theor Appl Genet 122:905–913. https://doi.org/10.1007/s00122-010-1497-0
Williams K, Sorrells ME (2014) Three-dimensional seed size and shape QTL in hexaploid wheat (Triticum aestivum L.) populations. Crop Sci 54:98–110. https://doi.org/10.2135/cropsci2012.10.0609
Wu Q-H, Chen Y-X, Zhou S-H, Fu L, Chen J-J, Xiao Y, Zhang D, Ouyang S-H, Zhao X-J, Cui Y, Zhang D-Y, Liang Y, Wang Z-Z, Xie J-Z, Qin J-X, Wang G-X, Li D-L, Huang Y-L, Yu M-H, Lu P, Wang L-L, Wang L, Wang H, Dang C, Li J, Zhang Y, Peng H-R, Yuan C-G, You M-S, Sun Q-X, Wang J-R, Wang L-X, Luo M-C, Han J, Liu Z-Y (2015) High-density genetic linkage map construction and QTL mapping of grain shape and size in the wheat population Yanda 1817 × Beinong6. PLoS ONE 10:e0118144. https://doi.org/10.1371/journal.pone.0118144
Xia T, Li N, Dumenil J, Li J, Kamenski A, Bevan MW, Gao F, Li Y (2013) The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell Online. https://doi.org/10.1105/tpc.113.115063
Zanke CD, Ling J, Plieske J, Kollers S, Ebmeyer E, Korzun V, Argillier O, Stiewe G, Hinze M, Neumann F, Eichhorn A, Polley A, Jaenecke C, Ganal MW, Roder MS (2015) Analysis of main effect QTL for thousand grain weight in European winter wheat (Triticum aestivum L.) by genome-wide association mapping. Front Plant Sci 6:644. https://doi.org/10.3389/fpls.2015.00644
Zeng D, Tian Z, Rao Y, Dong G, Yang Y, Huang L, Leng Y, Xu J, Sun C, Zhang G, Hu J, Zhu L, Gao Z, Hu X, Guo L, Xiong G, Wang Y, Li J, Qian Q (2017) Rational design of high-yield and superior-quality rice. Nat Plant 3:17031. https://doi.org/10.1038/nplants.2017.31
Zhai H, Feng Z, Du X, Song Y, Liu X, Qi Z, Song L, Li J, Li L, Peng H, Hu Z, Yao Y, Xin M, Xiao S, Sun Q, Ni Z (2018) A novel allele of TaGW2-A1 is located in a finely mapped QTL that increases grain weight but decreases grain number in wheat (Triticum aestivum L.). Theor Appl Genet 131:539–553. https://doi.org/10.1007/s00122-017-3017-y
Zhang X, Wang J, Huang J, Lan H, Wang C, Yin C, Wu Y, Tang H, Qian Q, Li J, Zhang H (2012) Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. Proc Natl Acad Sci USA 109:21534–21539. https://doi.org/10.1073/pnas.1219776110
Zhang Y, Liu J, Xia X, He Z (2014) TaGS-D1, an ortholog of rice OsGS3, is associated with grain weight and grain length in common wheat. Mol Breed 34:1097–1107. https://doi.org/10.1007/s11032-014-0102-7
Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu J-L, Gao C (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617. https://doi.org/10.1038/ncomms12617
Zhang Y, Li D, Zhang D, Zhao X, Cao X, Dong L, Liu J, Chen K, Zhang H, Gao C, Wang D (2018) Analysis of the functions of TaGW2 homoeologs in wheat grain weight and protein content traits. Plant J 94:857–866. https://doi.org/10.1111/tpj.13903
Zuo J, Li J (2014) Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu Rev Genet 48:99–118. https://doi.org/10.1146/annurev-genet-120213-092138
Acknowledgements
This research was supported by the Special Fund for Henan Agricultural Research System (S2010-01-G03). We also acknowledge Dr. Daowen Wang (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) for providing Triticum urartu germplasm.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declared that they have no conflict of interest.
Additional information
Communicated by Takuji Sasaki.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Figure 1.
Gene structure of TaGL3-5A, TaGL3-5B and TaGL3-5D genes based on Chinese Spring RefSeq v1.0 (from initial codon to stop codon). (PDF 258 kb)
Rights and permissions
About this article
Cite this article
Yang, J., Zhou, Y., Wu, Q. et al. Molecular characterization of a novel TaGL3-5A allele and its association with grain length in wheat (Triticum aestivum L.). Theor Appl Genet 132, 1799–1814 (2019). https://doi.org/10.1007/s00122-019-03316-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-019-03316-1