Abstract
Key message
This study precisely mapped and validated a major quantitative trait locus (QTL) on chromosome 4AL for thousand-grain weight in wheat using multiple near-isogenic lines.
Abstract
Thousand-grain weight (TGW) is an essential yield component. Following the previous identification of a major QTL for TGW within the interval of 15.7 cM (92.7–108.4 cM) on chromosome 4AL using the Nongda3338 (ND3338)/**gdong6 (JD6) doubled haploid population, the aim of this study was to perform more precise map** and validate the genetic effect of the QTL. Multiple near-isogenic lines (NILs) were developed using ND3338 as the recurrent parent through marker-assisted selection. Based on five independent BC3F3:4 segregating populations derived from BC3F3 plants with different heterozygous segments for the target QTL site and the results of genoty** analysis performed using the Wheat660 K SNP array, it was possible to delimit the QTL region to a physical interval of approximately 6.5 Mb (677.11–683.61 Mb, IWGSC Ref Seq v1.0). Field trials across multiple environments showed that NILsJD6 had a consistent effect on increasing the TGW by 5.16–27.48% and decreasing the grain number per spike (GNS) by 3.98–32.91% compared to the corresponding NILsND3338, which exhibited locus-specific TGW-GNS trade-offs. Moreover, by using RNA sequencing (RNA-Seq) of whole grains at 10 days after pollination stage of multiple NILs, we found that differentially expressed genes between the NIL pairs were significantly enriched for cell cycle and the replication of chromosome-related genes, hence affecting cell division and cell proliferation. Overall, our results provide a basis for map-based cloning of the major QTL and determining the mechanisms underlying TGW–GNS trade-offs in wheat, which would help to fine-tune these two components and maximize the grain yield for breeders.
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References
Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan KW, Golan G, Deek J, Ben-Zvi B, Ben-Zvi G, Himmelbach A, MacLachlan RP, Sharpe AG, Fritz A, Ben-David R, Budak H, Fahima T, Korol A, Faris JD, Hernandez A, Mikel MA, Levy AA, Steffenson B, Maccaferri M, Tuberosa R, Cattivelli L, Faccioli P, Ceriotti A, Kashkush K, Pourkheirandish M, Komatsuda T, Eilam T, Sela H, Sharon A, Ohad N, Chamovitz DA, Mayer KFX, Stein N, Ronen G, Peleg Z, Pozniak CJ, Akhunov ED, Distelfeld A (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97. https://doi.org/10.1126/science.aan0032
Balcarkova B, Frenkel Z, Skopova M, Abrouk M, Kumar A, Chao S, Kianian SF, Akhunov E, Korol AB, Dolezel J, Valarik M (2016) A High Resolution Radiation Hybrid Map of Wheat Chromosome 4A. Front Plant Sci 7:2063. https://doi.org/10.3389/fpls.2016.02063
Barrero JM, Cavanagh C, Verbyla KL, Tibbits JFG, Verbyla AP, Huang BE, Rosewarne GM, Stephen S, Wang PH, Whan A, Rigault P, Hayden MJ, Gubler F (2015) Transcriptomic analysis of wheat near-isogenic lines identifies PM19-A1 and A2 as candidates for a major dormancy QTL. Genome Biol 16:93. https://doi.org/10.1186/s13059-015-0665-6
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Brinton J, Simmonds J, Minter F, Leverington-Waite M, Snape J, Uauy C (2017) Increased pericarp cell length underlies a major quantitative trait locus for grain weight in hexaploid wheat. New Phytol 215:1026–1038. https://doi.org/10.1111/nph.14624
Brinton J, Simmonds J, Uauy C (2018) Ubiquitin-related genes are differentially expressed in isogenic lines contrasting for pericarp cell size and grain weight in hexaploid wheat. BMC Plant Biol 18(1):22. https://doi.org/10.1186/s12870-018-1241-5
Clavijo BJ, Venturini L, Schudoma C, Accinelli GG, Kaithakottil G, Wright J, Borrill P, Kettleborough G, Heavens D, Chapman H, Lipscombe J, Barker T, Lu FH, McKenzie N, Raats D, Ramirez-Gonzalez RH, Coince A, Peel N, Percival-Alwyn L, Duncan O, Trosch J, Yu GT, Bolser DM, Namaati G, Kerhornou A, Spannagl M, Gundlach H, Haberer G, Davey RP, Fosker C, Di Palma F, Phillips AL, Millar AH, Kersey PJ, Uauy C, Krasileva KV, Swarbreck D, Bevan MW, Clark MD (2017) An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations. Genome Res 27:885–896. https://doi.org/10.1101/gr.217117.116
Dobin A, Gingeras TR (2015) Map** RNA-seq Reads with STAR. Curr Protoc Bioinform 51:11–14. https://doi.org/10.1002/0471250953.bi1114s51
Dvorak J, Wang L, Zhu T, Jorgensen CM, Luo MC, Deal KR, Gu YQ, Gill BS, Distelfeld A, Devos KM, Qi P, McGuire PE (2018) Reassessment of the evolution of wheat chromosomes 4A, 5A, and 7B. Theor Appl Genet 131:2451–2462. https://doi.org/10.1007/s00122-018-3165-8
FAOSTAT (2015). http://faostat3.fao.org/home
Golan G, Ayalon I, Perry A, Zimran G, Ade-Ajayi T, Mosquna A, Distelfeld A, Peleg Z (2019) GNI-A1 mediates trade-off between grain number and grain weight in tetraploid wheat. Theor Appl Genet. https://doi.org/10.1007/s00122-019-03358-5
Griffiths S, Wingen L, Pietragalla J, Garcia G, Hasan A, Miralles D, Calderini DF, Ankleshwaria JB, Waite ML, Simmonds J, Snape J, Reynolds M (2015) Genetic dissection of grain size and grain number trade-offs in CIMMYT wheat germplasm. PLoS ONE 10:e0118847. https://doi.org/10.1371/journal.pone.0118847
Guan P, Lu L, Jia L, Kabir MR, Zhang J, Lan T, Zhao Y, **n M, Hu Z, Yao Y, Ni Z, Sun Q, Peng H (2018) Global QTL Analysis identifies genomic regions on chromosomes 4A and 4B harboring stable loci for yield-related traits across different environments in wheat (Triticum aestivum L.). Front Plant Sci 9:529. https://doi.org/10.3389/fpls.2018.00529
Guo Y, Sun J, Zhang G, Wang Y, Kong F, Zhao Y, Li S (2013) Haplotype, molecular marker and phenotype effects associated with mineral nutrient and grain size traits of TaGS1a in wheat. Field Crops Res 154:119–125. https://doi.org/10.1016/j.fcr.2013.07.012
Hanif M, Gao F, Liu J, Wen W, Zhang Y, Rasheed A, **a X, He Z, Cao S (2015) TaTGW6-A1, an ortholog of rice TGW6, is associated with grain weight and yield in bread wheat. Mol Breed 36:1. https://doi.org/10.1007/s11032-015-0425-z
Hernandez P, Martis M, Dorado G, Pfeifer M, Galvez S, Schaaf S, Jouve N, Simkova H, Valarik M, Dolezel J, Mayer KF (2012) Next-generation sequencing and syntenic integration of flow-sorted arms of wheat chromosome 4A exposes the chromosome structure and gene content. Plant J 69:377–386. https://doi.org/10.1111/j.1365-313X.2011.04808.x
Hill K (2015) Post-translational modifications of hormone-responsive transcription factors: the next level of regulation. J Exp Bot 66:4933–4945. https://doi.org/10.1093/jxb/erv273
Hu MJ, Zhang HP, Cao JJ, Zhu XF, Wang SX, Jiang H, Wu ZY, Lu J, Chang C, Sun GL, Ma CX (2016) Characterization of an IAA-glucose hydrolase gene TaTGW6 associated with grain weight in common wheat (Triticum aestivum L.). Mol Breed 36:25. https://doi.org/10.1007/s11032-016-0449-z
Huang RY, Jiang LR, Zheng JS, Wang TS, Wang HC, Huang YM, Hong ZL (2013) Genetic bases of rice grain shape: so many genes, so little known. Trends Plant Sci 18:218–226. https://doi.org/10.1016/j.tplants.2012.11.001
Hunter MC, Smith RG, Schipanski ME, Atwood LW, Mortensen DA (2017) Agriculture in 2050: recalibrating Targets for Sustainable Intensification. Bioscience 67:385–390. https://doi.org/10.1093/biosci/bix010
International Wheat Genome Sequencing Consortium (IWGSC) (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788. https://doi.org/10.1126/science.1251788
International Wheat Genome Sequencing Consortium (IWGSC), Appels R, Eversole K, Feuillet C et al (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361(6403):eaar7191. https://doi.org/10.1126/science.aar7191
Jiang Y, Jiang Q, Hao C, Hou J, Wang L, Zhang H, Zhang S, Chen X, Zhang X (2015) A yield-associated gene TaCWI, in wheat: its function, selection and evolution in global breeding revealed by haplotype analysis. Theor Appl Genet 128:131–143. https://doi.org/10.1007/s00122-014-2417-5
Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci U S A 102:3117–3122. https://doi.org/10.1073/pnas.0409893102
Jorgensen C, Luo MC, Ramasamy R, Dawson M, Gill BS, Korol AB, Distelfeld A, Dvorak J (2017) A High-density genetic map of wild emmer wheat from the Karaca Dag region provides new evidence on the structure and evolution of wheat chromosomes. Front Plant Sci 8:1798. https://doi.org/10.3389/fpls.2017.01798
Kang GZ, Liu GQ, Peng XQ, Wei LT, Wang CY, Zhu YJ, Ma Y, Jiang YM, Guo TC (2013) Increasing the starch content and grain weight of common wheat by overexpression of the cytosolic AGPase large subunit gene. Plant Physiol Biochem 73:93–98. https://doi.org/10.1016/j.plaphy.2013.09.003
Krasileva KV, Vasquez-Gross HA, Howell T, Bailey P, Paraiso F, Clissold L, Simmonds J, Ramirez-Gonzalez RH, Wang XD, Borrill P, Fosker C, Ayling S, Phillips AL, Uauy C, Dubcovsky J (2017) Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci USA 114:E913–E921. https://doi.org/10.1073/pnas.1619268114
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
Li N, Li Y (2016) Signaling pathways of seed size control in plants. Curr Opin Plant Biol 33:23–32. https://doi.org/10.1016/j.pbi.2016.05.008
Li W, Yang B (2017) Translational genomics of grain size regulation in wheat. Theor Appl Genet 130(9):1765–1771. https://doi.org/10.1007/s00122-017-2953-x
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Proc GPD (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Luo MC, Gu YQ, Puiu D, Wang H, Twardziok SO, Deal KR, Huo N, Zhu T, Wang L, Wang Y, McGuire PE, Liu S, Long H, Ramasamy RK, Rodriguez JC, Van SL, Yuan L, Wang Z, **a Z, **ao L, Anderson OD, Ouyang S, Liang Y, Zimin AV, Pertea G, Qi P, Bennetzen JL, Dai X, Dawson MW, Muller HG, Kugler K, Rivarola-Duarte L, Spannagl M, Mayer KFX, Lu FH, Bevan MW, Leroy P, Li P, You FM, Sun Q, Liu Z, Lyons E, Wicker T, Salzberg SL, Devos KM, Dvorak J (2017) Genome sequence of the progenitor of the wheat D genome Aegilops tauschii. Nature 551:498–502. https://doi.org/10.1038/nature24486
Ma D, Yan J, He Z, Wu L, **a X (2012) Characterization of a cell wall invertase gene TaCwi-A1 on common wheat chromosome 2A and development of functional markers. Mol Breed 29:43–52. https://doi.org/10.1007/s11032-010-9524-z
Ma J, Stiller J, Berkman PJ, Wei Y, Rogers J, Feuillet C, Dolezel J, Mayer KF, Eversole K, Zheng YL, Liu C (2013) Sequence-based analysis of translocations and inversions in bread wheat (Triticum aestivum L). PLoS One 8:e79329. https://doi.org/10.1371/journal.pone.0079329
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
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303. https://doi.org/10.1101/gr.107524.110
Miftahudin Ross K, Ma XF, Mahmoud AA, Layton J, Milla MA, Chikmawati T, Ramalingam J, Feril O, Pathan MS, Momirovic GS, Kim S, Chema K, Fang P, Haule L, Struxness H, Birkes J, Yaghoubian C, Skinner R, McAllister J, Nguyen V, Qi LL, Echalier B, Gill BS, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dvorak J, Dilbirligi M, Gill KS, Peng JH, Lapitan NL, Bermudez-Kandianis CE, Sorrells ME, Hossain KG, Kalavacharla V, Kianian SF, Lazo GR, Chao S, Anderson OD, Gonzalez-Hernandez J, Conley EJ, Anderson JA, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Nguyen HT, Gustafson JP (2004) Analysis of expressed sequence tag loci on wheat chromosome group 4. Genetics 168:651–663. https://doi.org/10.1534/genetics.104.034827
Pimentel H, Bray NL, Puente S, Melsted P, Pachter L (2017) Differential analysis of RNA-seq incorporating quantification uncertainty. Nat Methods 14:687–690. https://doi.org/10.1038/nmeth.4324
R TC (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org
Ramirez-Gonzalez RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, van Ex F, Pasha A, Khedikar Y, Robinson SJ, Cory AT, Florio T, Concia L, Juery C, Schoonbeek H, Steuernagel B, **ang D, Ridout CJ, Chalhoub B, Mayer KFX, Benhamed M, Latrasse D, Bendahmane A, Wulff BBH, Appels R, Tiwari V, Datla R, Choulet F, Pozniak CJ, Provart NJ, Sharpe AG, Paux E, Spannagl M, Brautigam A, Uauy C, Sequencing IWG (2018) The transcriptional landscape of polyploid wheat. Science 361:662. https://doi.org/10.1126/science.aar6089
Roder MS, Huang XQ, Borner A (2008) Fine map** of the region on wheat chromosome 7D controlling grain weight. Funct Integr Genom 8:79–86. https://doi.org/10.1007/s10142-007-0053-8
Sajjad M, Ma X, Habibullah Khan S, Shoaib M, Song Y, Yang W, Zhang A, Liu D (2017) TaFlo2-A1, an ortholog of rice Flo2, is associated with thousand grain weight in bread wheat (Triticum aestivum L.). BMC Plant Biol 17:164. https://doi.org/10.1186/s12870-017-1114-3
Sakuma S, Golan G, Guo Z, Ogawa T, Tagiri A, Sugimoto K, Bernhardt N, Brassac J, Mascher M, Hensel G, Ohnishi S, **no H, Yamashita Y, Ayalon I, Peleg Z, Schnurbusch T, Komatsuda T (2019) Unleashing floret fertility in wheat through the mutation of a homeobox gene. Proc Natl Acad Sci U S A 116(11):5182–5187. https://doi.org/10.1073/pnas.1815465116
Shi L, Wu Y, Sheen J (2018) TOR signaling in plants: conservation and innovation. Development 145:dev160887. https://doi.org/10.1242/dev.160887
Silva Lda C, Wang S, Zeng ZB (2012) Composite interval map** and multiple interval map**: procedures and guidelines for using Windows QTL Cartographer. Methods Mol Biol 871:75–119. https://doi.org/10.1007/978-1-61779-785-9_6
Stam P (1993) Construction of integrated genetic-linkage maps by means of a new computer package: joinmap. Plant J 3:739e–744e. https://doi.org/10.1111/j.1365-313X.1993.00739.x
Su ZQ, Hao CY, Wang LF, Dong YC, Zhang XY (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
Uauy C (2017) Wheat genomics comes of age. Curr Opin Plant Biol 36:142–148. https://doi.org/10.1016/j.pbi.2017.01.007
Uauy C, Wulff BBH, Dubcovsky J (2017) Combining traditional mutagenesis with new high-throughput sequencing and genome editing to reveal hidden variation in polyploid wheat. Annu Rev Genet 51:435–454. https://doi.org/10.1146/annurev-genet-120116-024533
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63. https://doi.org/10.1038/nrg2484
Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q, Zhang G, Fu X (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954. https://doi.org/10.1038/ng.2327
Wang S, Yan X, Wang Y, Liu H, Cui D, Chen F (2016) Haplotypes of the TaGS5-A1 gene are associated with thousand-kernel weight in Chinese Bread wheat. Front Plant Sci 7:783. https://doi.org/10.3389/fpls.2016.00783
Wang M, Wang S, Liang Z, Shi W, Gao C, **a G (2017) From genetic stock to genome editing: gene exploitation in wheat. Trends Biotechnol 36(2):160–172. https://doi.org/10.1016/j.tibtech.2017.10.002
**ong Y, Sheen J (2015) Novel links in the plant TOR kinase signaling network. Curr Opin Plant Biol 28:83–91. https://doi.org/10.1016/j.pbi.2015.09.006
Yue A, Li A, Mao X, Chang X, Li R, **g R (2015) Identification and development of a functional marker from 6-SFT-A2 associated with grain weight in wheat. Mol Breed 35:63. https://doi.org/10.1007/s11032-015-0266-9
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 map**. Front Plant Sci 6:644. https://doi.org/10.3389/fpls.2015.00644
Zhai H, Feng Z, Du X, Song Y, Liu X, Qi Z, Song L, Li J, Li L, Peng H, Hu Z, Yao Y, **n M, **ao 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 LY, Liu DC, Guo XL, Yang WL, Sun JZ, Wang DW, Zhang A (2010) Genomic distribution of quantitative trait loci for yield and yield-related traits in common wheat. J Integr Plant Biol 52:996–1007. https://doi.org/10.1111/j.1744-7909.2010.00967.x
Zhang L, Zhao YL, Gao LF, Zhao GY, Zhou RH, Zhang BS, Jia JZ (2012) TaCKX6-D1, the ortholog of rice OsCKX2, is associated with grain weight in hexaploid wheat. New Phytol 195:574–584. https://doi.org/10.1111/j.1469-8137.2012.04194.x
Zhang YJ, Liu JD, **a XC, He ZH (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 ZG, Lv GD, Li B, Wang JJ, Zhao Y, Kong FM, Guo Y, Li SS (2017) Isolation and characterization of the TaSnRK2.10 gene and its association with agronomic traits in wheat (Triticum aestivum L.). PLoS One 12:0174425. https://doi.org/10.1371/journal.pone.0174425
Zhao G, Zou C, Li K, Wang K, Li T, Gao L, Zhang X, Wang H, Yang Z, Liu X, Jiang W, Mao L, Kong X, Jiao Y, Jia J (2017) The Aegilops tauschii genome reveals multiple impacts of transposons. Nat Plants 3:946–955. https://doi.org/10.1038/s41477-017-0067-8
Zimin AV, Puiu D, Hall R, Kingan S, Clavijo BJ, Salzberg SL (2017) The first near-complete assembly of the hexaploid bread wheat genome, Triticum aestivum. Gigascience 6:1–7. https://doi.org/10.1093/gigascience/gix097
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
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This work was financially supported by the National Key Research and Development Program of China (Grant No. 2016YFD0100402) and China Postdoctoral Science Foundation (2018M641541).
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Guan, P., Di, N., Mu, Q. et al. Use of near-isogenic lines to precisely map and validate a major QTL for grain weight on chromosome 4AL in bread wheat (Triticum aestivum L.). Theor Appl Genet 132, 2367–2379 (2019). https://doi.org/10.1007/s00122-019-03359-4
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DOI: https://doi.org/10.1007/s00122-019-03359-4