Abstract
Key message
We identified stable QTL for grain morphology and yield component traits in a wheat defective grain filling line and validated genetic effects in a panel of cultivars using breeding-relevant markers.
Abstract
Grain filling capacity is essential for grain yield and appearance quality in cereal crops. Identification of genetic loci for grain filling is important for wheat improvement. However, there are few genetic studies on grain filling in wheat. Here, a defective grain filling (DGF) line wdgf1 characterized by shrunken grains was identified in a population derived from multi-round crosses involving nine parents and a recombinant inbreed line (RIL) population was generated from the cross between wdgf1 and a sister line with normal grains. We constructed a genetic map of the RIL population using the wheat 15K single nucleotide polymorphism chip and detected 25 stable quantitative trait loci (QTL) for grain morphology and yield components, including three for DGF, eleven for grain size, six for thousand grain weight, three for grain number per spike and two for spike number per m2. Among them, QDGF.caas-7A is co-located with QTGW.caas-7A and can explain 39.4–64.6% of the phenotypic variances, indicating that this QTL is a major locus controlling DGF. Sequencing and linkage mapping showed that TaSus2-2B and Rht-B1 were candidate genes for QTGW.caas-2B and the QTL cluster (QTGW.caas-4B, QGNS.caas-4B, and QSN.caas-4B), respectively. We developed kompetitive allele-specific PCR markers tightly linked to the stable QTL without corresponding to known yield-related genes, and validated their genetic effects in a diverse panel of wheat cultivars. These findings not only lay a solid foundation for genetic dissection underlying grain filling and yield formation, but also provide useful tools for marker-assisted breeding.
Similar content being viewed by others
Data availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Braun DM, Wang L, Ruan YL (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signaling to enhance crop yield and food security. J Exp Bot 65:1713–1735. https://doi.org/10.1093/jxb/ert416
Cao SH, Xu DG, Hanif M, Xia XC, He ZH (2020) Genetic architecture underpinning yield component traits in wheat. Theor Appl Genet 133:1811–1823. https://doi.org/10.1007/s00122-020-03562-8
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. https://doi.org/10.1007/s004380050792
Cui F, Zhao CH, Ding AM, Li J, Wang L, Li XF, Bao YG, Li JM, Wang HG (2014) Construction of an integrative linkage map and QTL mapping of grain yield-related traits using three related wheat RIL populations. Theor Appl Genet 127:659–675. https://doi.org/10.1007/s00122-013-2249-8
Cuthbert JL, Somers DJ, Brûlé-Babel AL, Brown PD, Crow GH (2008) Molecular mapping of quantitative trait loci for yield and yield components in spring wheat (Triticum aestivum L.). Theor Appl Genet 117:595–608. https://doi.org/10.1007/s00122-008-0804-5
Fei HH, Yang ZP, Lu QT, Wen XG, Zhang Y, Zhang AH, Lu CM (2021) OsSWEET14 cooperates with OsSWEET11 to contribute to grain filling in rice. Plant Sci 306:110851. https://doi.org/10.1016/j.plantsci.2021.110851
Fu C, Du JY, Tian XL, He ZH, Fu LP, Wang Y, Xu DG, Xu XT, Xia XC, Zhang Y, Cao SH (2019) Rapid identification and characterization of genetic loci for defective kernel in bread wheat. BMC Plant Biol 19:1–11. https://doi.org/10.1186/s12870-019-2102-6
Greene TW, Hannah LC (1998) Maize endosperm ADP-glucose pyrophosphorylase SHRUNKEN2 and BRITTLE2 subunit interactions. Plant Cell 10:1295–1306. https://doi.org/10.1105/tpc.10.8.1295
Huang XQ, Cloutier S, Lycar L, Radovanovic N, Humphreys DG, Noll JS, Somers DJ, Brown PD (2006) Molecular detection of QTLs for agronomic and quality traits in a doubled haploid population derived from two Canadian wheats (Triticum aestivum L.). Theor Appl Genet 113:753–766. https://doi.org/10.1007/s00122-006-0346-7
International Wheat Genome Sequencing Consortium (IWGSC) (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191. https://doi.org/10.1126/science.aar7191
Jiang QY, Hou J, Hao CY, Wang LF, Ge HM, Dong YS, Zhang XY (2011) The wheat (T. aestivum) sucrose synthase 2 gene (TaSus2) active in endosperm development is associated with yield traits. Funct Integr Genom 11:49–61. https://doi.org/10.1007/s10142-010-0188-x
Jones DB, Peterson ML, Geng S (1979) Association between grain flling rate and duration and yield components in rice. Crop Sci 19:641–644. https://doi.org/10.2135/cropsci1979.0011183X001900050023x
Kang BH, Xiong YQ, Williams DS, Pozueta-Romero D, Chourey PS (2009) Miniature1-encoded cell wall invertase is essential for assembly and function of wall-in-growth in the maize endosperm transfer cell. Plant Physiol 151:1366–1376. https://doi.org/10.1104/pp.109.142331
Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65:531–546. https://doi.org/10.1007/s11103-007-9153-z
Li FJ, Wen WE, Liu JD, Zhang Y, Cao SH, He ZH, Rasheed A, Jin H, Zhang C, Yan J, Zhang PZ, Wan YX, Xia XC (2019) Genetic architecture of grain yield in bread wheat based on genome-wide association studies. BMC Plant Biol 19:1–19. https://doi.org/10.1186/s12870-019-1781-3
Li LL, Bian YJ, Dong YC, Song J, Liu D, Zeng JQ, Cao SH (2022) Identification and validation of stable quantitative trait loci for yield component traits in wheat. Crop J 11:558–563. https://doi.org/10.1016/j.cj.2022.09.012
Liu EB, Zeng SY, Zhu SS, Liu Y, Wu GC, Zhao KM, Liu XL, Liu QM, Dong ZY, Dang XJ, Li DL, Hu XX, Hong DL (2019) Favorable alleles of GRAIN-FILLING RATE1 increase the grain-filling rate and yield of rice. Plant Physiol 181:1207–1222. https://doi.org/10.1104/pp.19.00413
Lin Y, Jiang XJ, Tao Y, Yang XL, Wang ZA, Wu FK, Liu SH, Li CX, Deng M, Ma J, Chen GD, Wei YN, Zheng YL, Liu YX (2020) Identification and validation of stable quantitative trait loci for grain filling rate in common wheat (Triticum aestivum L.). Theor Appl Genet 133:2377–2385. https://doi.org/10.1007/s00122-020-03605-0
Liu D, Zhao DH, Zeng JQ, Shawai RS, Tong JY, Li M, Li FJ, Zhou S, Hu WL, Xia XC, Tian YB, Zhu Q, Wang CP, Wang DS, He ZH, Liu JD, Zhang Y (2022) Identification of genetic loci for grain yield-related traits in the wheat population Zhongmai 578/Jimai 22. J Integr Agric. https://doi.org/10.1016/j.jia.2022.12.002
Liu GY, Zhang RQ, Li S, Ullah R, Yang FP, Wang ZH, Guo WL, You MS, Li BY, Xie CJ, Wang LS, Liu J, Ni ZF, Sun QX, Liang RQ (2023a) TaMADS29 interacts with TaNF-YB1 to synergistically regulate early grain development in bread wheat. Sci China Life Sci. https://doi.org/10.1007/s11427-022-2286-0
Liu HX, Si XM, Wang ZY, Cao LJ, Gao LF, Zhou XL, Wang WX, Wang K, Jiao CZ, Zhuang L, Liu YC, Hou J, Li T, Hao CY, Guo WL, Liu J, Zhang XY (2023b) TaTPP-7A positively feedback regulates grain filling and wheat grain yield through T6P-SnRK1 signalling pathway and sugar-ABA interaction. Plant Biotechnol J. https://doi.org/10.1111/pbi.14025
Ma L, Zhang DC, Miao QS, Yang J, Xuan YH, Hu YB (2017) Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiol 58:863–873. https://doi.org/10.1093/pcp/pcx040
Ma B, Zhang L, He ZH (2023) Understanding the regulation of cereal grain filling: the way forward. J Integr Plant Biol 65:526–547. https://doi.org/10.1111/jipb.13456
Meng L, Li HH, Zhang LY, Wang JK (2015) QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283. https://doi.org/10.1016/j.cj.2015.01.001
Mohler V, Albrecht T, Castell A, Diethelm M, Schweizer G, Hartl L (2016) Considering causal genes in the genetic dissection of kernel traits in common wheat. J Appl Genet 57:467–476. https://doi.org/10.1007/s13353-016-0349-2
Raza A, Razzaq A, Mehmood SS, Zou XL, Zhang XK, Lv Y, Xu JS (2019) Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8:34. https://doi.org/10.3390/plants8020034
Shen S, Ma S, Chen XM, Yi F, Li BB, Liang XG, Liao SJ, Gao LH, Zhou SL, Ruan YL (2022) A transcriptional landscape underlying sugar import for grain set in maize. Plant J 110:228–242. https://doi.org/10.1111/tpj.15668
Sosso D, Luo DP, Li QB, Sasse J, Yang JL, Gendrot G, Suzuki M, Koch KE, McCarty DR, Chourey PS, Rogowsky PM, Ross-Ibarra J, Yang B, Frommer WB (2015) Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat Genet 47:1489–1493. https://doi.org/10.1038/ng.3422
Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: join Map. Plant J 3(5):739–744. https://doi.org/10.1111/j.1365-313X.1993.00739.x
Su QN, Zhang XL, Zhang W, Zhang N, Song LQ, Liu L, Xue X, Liu GT, Liu JJ, Meng DY, Zhi LY, Ji J, Zhao XQ, Yang CL, Tong YP, Liu ZY, Li JM (2018) QTL detection for kernel size and weight in bread wheat (Triticum aestivum L.) using a high-density SNP and SSR-based linkage map. Front Plant Sci 9:1484. https://doi.org/10.3389/fpls.2018.01484
Sun H, Li JJ, Song HY, Yang D, Deng XB, Liu J, Wang YM, Ma JY, Xiong YQ, Liu YL, Yang M (2020) Comprehensive analysis of AGPase genes uncovers their potential roles in starch biosynthesis in lotus seed. BMC Plant Biol 20:1–15. https://doi.org/10.1186/s12870-020-02666-z
Wang ET, Wang JJ, Zhu XD, Hao W, Wang LY, Li Q, Zhang LX, He W, Lu B, Lin HX, Ma H, Zhang GQ, He ZH (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40:1370–1374. https://doi.org/10.1038/ng.220
Wei XJ, Jiao GA, Lin HY, Sheng ZH, Shao GN, Xie LH, Tang SQ, Xu QG, Hu PS (2017) GRAIN INCOMPLETE FILLING 2 regulates grain filling and starch synthesis during rice caryopsis development. J Integr Plant Biol 59:134–153. https://doi.org/10.1111/jipb.12510
Wen SZ, Zhang MH, Tu KL, Fan CF, Tian S, Bi C, Chen ZL, Zhao HH, Wei CX, Shi XT, Yu JZ, Sun QX, You MS (2022) A major quantitative trait loci cluster controlling three components of yield and plant height identified on chromosome 4B of common wheat. Front Plant Sci 12:3107. https://doi.org/10.3389/fpls.2021.799520
Xu DA, Bian YJ, Luo XM, Jia CF, Hao QL, Tian XL, Cao Q, Chen W, Ma WJ, Ni ZF, Fu XD, He ZH, Xia XC, Cao SH (2023) Dissecting pleiotropic functions of the wheat Green Revolution gene Rht-B1b in plant morphogenesis and yield formation. Development. https://doi.org/10.1242/dev.201601
Yang JL, Luo DP, Yang B, Frommer WB, Eom JS (2018) SWEET11 and 15 as key players in seed filling in rice. New Phytol 218:604–615. https://doi.org/10.1111/nph.15004
Yang L, Zhao DH, Meng ZL, Xu KJ, Yan J, Xia XH, Cao SH, Tian YB, He ZH, Zhang Y (2020) QTL mapping for grain yield-related traits in bread wheat via SNP-based selective genotyping. Theor Appl Genet 133:857–872. https://doi.org/10.1007/s00122-019-03511-0
Acknowledgements
We are grateful to Prof. Robert McIntosh, Plant Breeding Institute, University of Sydney, for revising this manuscript.
Funding
This work was supported by National Key Research and Development Program of China (2022YFF1002904, 2022YFD1201500) and the Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (CAAS).
Author information
Authors and Affiliations
Contributions
B. Y. Liu and S. H. Cao wrote the draft manuscript; B. Y. Liu, L. L. Li and C. Fu performed the experiments; B. Y. Liu, L. L. Li, J. Y. Du, Y. J. Zhang, B. Bai, J. Q. Zeng; Y. J. Bian, S. Y. Liu, J. Song, L. X. Luo, L. N. Xie, M. J. Sun and X. W. Xu participated in field trials; J. Y. Du, Y. J. Zhang, B. Bai and S. H. Cao generated and screened mutant materials; S. H. Cao designed the experiments; X. C. Xia, J. Y. Du, Y. J. Zhang and B. Bai assisted in writing the paper.
Corresponding author
Ethics declarations
Conflict of interest
We declare no conflicts of interest in regard to this manuscript.
Ethical standards
These experiments complied with the ethical standards in China.
Additional information
Communicated by Diane E. Mather.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, B., Li, L., Fu, C. et al. Genetic dissection of grain morphology and yield components in a wheat line with defective grain filling. Theor Appl Genet 136, 165 (2023). https://doi.org/10.1007/s00122-023-04410-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00122-023-04410-1