Mapping and Characterization of QTLs for Awn Morphology Using Crosses between “Double-Awn” Wheat 4045 and Awnless Wheat Zhiluowumai
Abstract
:1. Introduction
2. Results
2.1. Phenotypic and Genetic Analysis of Awn Trait in 4045 and ZLWM
2.2. Primary Mapping of the Awnless Trait
2.3. Fine Mapping of Qawn-5A Locus
2.4. Analysis of Candidate Genes in the Mapping Interval
2.5. Overexpression of TraesCS5A02G542800 in a “Double-Awn” Acceptor
3. Discussion
4. Materials and Methods
4.1. Plant Materials and Growth Conditions
4.2. Genetic Map Construction and Primary Mapping
4.3. KASP Marker Development and Genotyping
4.4. RNA Sequencing and Gene Expression Analysis
4.5. Gene Cloning and Structure Analysis of TraesCS5A02G542800
4.6. Generation of Overexpression Transgenic Wheat
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Elbaum, R.; Zaltzman, L.; Burgert, I.; Fratzl, P. The Role of Wheat Awns in the Seed Dispersal Unit. Science 2007, 316, 884–886. [Google Scholar] [CrossRef]
- Li, X.; Du, B.; Wang, H.G. Awn Anatomy of Common Wheat (Triticum Aestivum L.) and Its Relatives. Caryologia 2010, 63, 391–397. [Google Scholar] [CrossRef] [Green Version]
- Grundbacher, F.J. The physiological function of the cereal awn. Bot. Rev. 1963, 29, 366–381. [Google Scholar] [CrossRef]
- Li, X.; Wang, H.; Li, H.; Zhang, L.; Teng, N.; Lin, Q.; Wang, J.; Kuang, T.; Li, Z.; Li, B.; et al. Awns play a dominant role in carbohydrate production during the grain-filling stages in wheat (Triticum aestivum). Physiol. Plant. 2006, 127, 701–709. [Google Scholar] [CrossRef]
- Motzo, R.; Giunta, F. Awnedness affects grain yield and kernel weight in near-isogenic lines of durum wheat. Aust. J. Agric. Res. 2002, 53, 1285–1293. [Google Scholar] [CrossRef]
- Blum, A. Photosynthesis and Transpiration in Leaves and Ears of Wheat and Barley Varieties. J. Exp. Bot. 1985, 36, 432–440. [Google Scholar] [CrossRef]
- Bort, J.; Febrero, A.; Amaro, T.; Araus, J. Role of awns in ear water-use efficiency and grain weight in barley. Agronomie 1994, 14, 133–139. [Google Scholar] [CrossRef]
- Martin, J.N.; Carver, B.F.; Hunger, R.M.; Cox, T.S. Contributions of Leaf Rust Resistance and Awns to Agro-nomic and Grain Quality Performance in Winter Wheat. Crop Sci. 2003, 43, 1712–1717. [Google Scholar] [CrossRef] [Green Version]
- Evans, L.T.; Bingham, J.; Jackson, P.; Sutherland, J. Effect of Awns and Drought on the Supply of Photosyn-thate and Its Distribution within Wheat Ears. Ann. Appl. Biol. 1972, 70, 67–76. [Google Scholar] [CrossRef]
- Maydup, M.; Antonietta, M.; Guiamet, J.; Graciano, C.; López, J.; Tambussi, E. The contribution of ear photosynthesis to grain filling in bread wheat (Triticum aestivum L.). Field Crop. Res. 2010, 119, 48–58. [Google Scholar] [CrossRef]
- Luo, J.; Liu, H.; Zhou, T.; Gu, B.; Huang, X.; Shangguan, Y.; Zhu, J.; Li, Y.; Zhao, Y.; Wang, Y.; et al. An-1 Encodes a Basic Helix-Loop-Helix Protein That Regulates Awn Development, Grain Size, and Grain Number in Rice. Plant Cell 2013, 25, 3360–3376. [Google Scholar] [CrossRef] [Green Version]
- Gu, B.; Zhou, T.; Luo, J.; Liu, H.; Wang, Y.; Shangguan, Y.; Zhu, J.; Li, Y.; Sang, T.; Wang, Z.; et al. An-2 Encodes a Cytokinin Synthesis Enzyme that Regulates Awn Length and Grain Production in Rice. Mol. Plant 2015, 8, 1635–1650. [Google Scholar] [CrossRef]
- Hua, L.; Wang, D.R.; Tan, L.; Fu, Y.; Liu, F.; Xiao, L.; Zhu, Z.; Fu, Q.; Sun, X.; Gu, P.; et al. LABA1, a Domestication Gene Associated with Long, Barbed Awns in Wild Rice. Plant Cell 2015, 27, 1875–1888. [Google Scholar] [CrossRef] [Green Version]
- Bessho-Uehara, K.; Wang, D.R.; Furuta, T.; Minami, A.; Nagai, K.; Gamuyao, R.; Asano, K.; Angeles-Shim, R.B.; Shimizu, Y.; Ayano, M.; et al. Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice. Proc. Natl. Acad. Sci. USA 2016, 113, 8969–8974. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jing, J.; Hua, L.; Zhu, Z.; Tan, L.; Zhao, X.; Zhang, W.; Liu, F.; Fu, Y.; Cai, H.; Sun, X. Gad1 Encodes a Secreted Peptide That Regulates Grain Number, Grain Length, and Awn Development in Rice Domes-tication. Plant Cell 2016, 28, 2453–2463. [Google Scholar]
- Taiyo, T.; Hirano, H.-Y. The Drooping Leaf and O S Ettin 2 Genes Promote Awn Development in Rice. Plant J. 2014, 77, 616–626. [Google Scholar]
- Yuo, T.; Yamashita, Y.; Kanamori, H.; Matsumoto, T.; Lundqvist, U.; Sato, K.; Ichii, M.; Jobling, S.A.; Taketa, S. A SHORT INTERNODES (SHI) family transcription factor gene regulates awn elongation and pistil morphology in barley. J. Exp. Bot. 2012, 63, 5223–5232. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Müller, K.J.; Romano, N.; Gerstner, O.; Garcia-Marotot, F.; Pozzi, C.; Salamini, F.; Rohde, W. The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature 1995, 374, 727–730. [Google Scholar] [CrossRef] [PubMed]
- Yoshioka, M.; Iehisa, J.C.M.; Ohno, R.; Kimura, T.; Enoki, H.; Nishimura, S.; Nasuda, S.; Takumi, S. Three dominant awnless genes in common wheat: Fine mapping, interaction and contribution to diversity in awn shape and length. PLoS ONE 2017, 12, e0176148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Watkins, A.E.; Ellerton, S. Variation and genetics of the awn inTriticum. J. Genet. 1940, 40, 243–270. [Google Scholar] [CrossRef]
- Sourdille, P.; Cadalen, T.; Gay, G.; Gill, B.; Bernard, M. Molecular and physical mapping of genes affecting awning in wheat. Plant Breed. 2002, 121, 320–324. [Google Scholar] [CrossRef]
- Kato, K.; Miura, H.; Akiyama, M.; Kuroshima, M.; Sawada, S. RFLP mapping of the three major genes, Vrn1, Q and B1, on the long arm of chromosome 5A of wheat. Euphytica 1998, 101, 91–95. [Google Scholar] [CrossRef]
- Mackay, I.J.; Bansept-Basler, P.; Barber, T.; Bentley, A.R.; Cockram, J.; Gosman, N.; Greenland, A.J.; Horsnell, R.; Howells, R.; O’Sullivan, D.; et al. An Eight-Parent Multiparent Advanced Generation Inter-Cross Population for Winter-Sown Wheat: Creation, Properties, and Validation. G3 Genes Genomes Genet. 2014, 4, 1603–1610. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Le Couviour, F.; Faure, S.; Poupard, B.; Flodrops, Y.; Dubreuil, P.; Praud, S. Analysis of genetic structure in a panel of elite wheat varieties and relevance for association mapping. Theor. Appl. Genet. 2011, 123, 715–727. [Google Scholar] [CrossRef] [PubMed]
- Goncharov, N.P.; Mitina, R.L.; Anfilova, N.A. Inheritance of Awnlessness in Tetraploid Wheat Species. Russ. J. Genet. 2003, 39, 463–466. [Google Scholar] [CrossRef]
- Ma, C.-Y.; Gao, L.-Y.; Li, N.; Li, X.-H.; Ma, W.-J.; Appels, R.; Yan, Y.-M. Proteomic Analysis of Albumins and Globulins from Wheat Variety Chinese Spring and Its Fine Deletion Line 3BS-8. Int. J. Mol. Sci. 2012, 13, 13398–13413. [Google Scholar] [CrossRef] [Green Version]
- Nishijima, R.; Ikeda, T.M.; Takumi, S. Genetic mapping reveals a dominant awn-inhibiting gene related to differentiation of the variety anathera in the wild diploid wheat Aegilops tauschii. Genetica 2017, 146, 75–84. [Google Scholar] [CrossRef] [Green Version]
- Wang, S.; Wong, D.; Forrest, K.; Allen, A.; Chao, S.; Huang, B.E.; Maccaferri, M.; Salvi, S.; Milner, S.G.; Cattivelli, L.; et al. Characterization of polyploid wheat genomic diversity using a high-density 90 000 single nucleotide polymorphism array. Plant Biotechnol. J. 2014, 12, 787–796. [Google Scholar] [CrossRef] [Green Version]
- Waddington, S.R.; Cartwright, P.M.; Wall, P.C. A Quantitative Scale of Spike Initial and Pistil Development in Barley and Wheat. Ann. Bot. 1983, 51, 119–130. [Google Scholar] [CrossRef]
- Dominguez, R.; Holmes, K.C. Actin Structure and Function. Annu. Rev. Biophys. 2011, 40, 169–186. [Google Scholar] [CrossRef] [Green Version]
- Rebetzke, G.J.; Bonnett, D.G.; Reynolds, M.P. Awns reduce grain number to increase grain size and harvestable yield in irrigated and rainfed spring wheat. J. Exp. Bot. 2016, 67, 2573–2586. [Google Scholar] [CrossRef]
- Chhabra, A.K.; Sethi, S.K. Contribution and Association of Awns and Flag-Leaf with Yield and Its Components in Durum Wheat. Cereal Res. Commun. 1989, 17, 265–271. [Google Scholar]
- DeWitt, N.; Guedira, M.; Lauer, E.; Sarinelli, M.; Tyagi, P.; Fu, D.; Hao, Q.; Murphy, J.P.; Marshall, D.; Akhunova, A.; et al. Sequence-based mapping identifies a candidate transcription repressor underlying awn suppression at the B1 locus in wheat. New Phytol. 2019, 225, 326–339. [Google Scholar] [CrossRef] [Green Version]
- Huang, D.; Zheng, Q.; Melchkart, T.; Bekkaoui, Y.; Konkin, D.J.F.; Kagale, S.; Martucci, M.; You, F.M.; Clarke, M.; Adamski, N.M.; et al. Dominant inhibition of awn development by a putative zinc-finger transcriptional repressor expressed at the B1 locus in wheat. New Phytol. 2020, 225, 340–355. [Google Scholar] [CrossRef] [Green Version]
- Niu, J.; Zheng, S.; Shi, X.; Si, Y.; Tian, S.; He, Y.; Ling, H.-Q. Fine mapping and characterization of the awn inhibitor B1 locus in common wheat (Triticum aestivum L.). Crop. J. 2020, 8, 613–622. [Google Scholar] [CrossRef]
- Wang, D.; Yu, K.; Jin, D.; Sun, L.; Chu, J.; Wu, W.; Xin, P.; Gregová, E.; Li, X.; Sun, J.; et al. Natural variations in the promoter of Awn Length Inhibitor 1 (ALI-1) are associated with awn elongation and grain length in common wheat. Plant J. 2019, 101, 1075–1090. [Google Scholar] [CrossRef]
- Ali, M.A.; Hussain, M.; Khan, M.I.; Ali, Z.; Zulkiffal, M.; Anwar, J.; Sabir, W.; Zeeshan, M. Source-Sink Relationship between Photosynthetic Organs and Grain Yield Attributes During Grain Filling Stage in Spring Wheat (Triticum Aestivum). Int. J. Agric. Biol. 2010, 12, 509–515. [Google Scholar]
- Maydup, M.; Antonietta, M.; Graciano, C.; Guiamet, J.; Tambussi, E. The contribution of the awns of bread wheat (Triticum aestivum L.) to grain filling: Responses to water deficit and the effects of awns on ear temperature and hydraulic conductance. Field Crop. Res. 2014, 167, 102–111. [Google Scholar] [CrossRef]
- Tambussi, E.A.; Bort, J.; Guiamet, J.J.; Nogués, S.; Araus, J.L. The Photosynthetic Role of Ears in C3 Cereals: Metabolism, Water Use Efficiency and Contribution to Grain Yield. Crit. Rev. Plant Sci. 2007, 26, 1–16. [Google Scholar] [CrossRef]
- Cingolani, P.; Platts, A.; Wang, L.L.; Coon, M.; Nguyen, T.; Wang, L.; Land, S.J.; Lu, X.; Ruden, D.M. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012, 6, 80–92. [Google Scholar] [CrossRef] [Green Version]
- Jiang, W.; Liu, T.; Nan, W.; Jeewani, D.C.; Niu, Y.; Li, C.; Wang, Y.; Shi, X.; Wang, C.; Wang, J.; et al. Two transcription factors TaPpm1 and TaPpb1 co-regulate anthocyanin biosynthesis in purple pericarps of wheat. J. Exp. Bot. 2018, 69, 2555–2567. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, S.-R.; Lee, D.-Y.; Yang, J.-I.; Moon, S.; An, G. Cloning Vectors for Rice. J. Plant Biol. 2009, 52, 73–78. [Google Scholar] [CrossRef]
- Zhao, T.-J.; Zhao, S.-Y.; Chen, H.-M.; Zhao, Q.-Z.; Hu, Z.-M.; Hou, B.-K.; Xia, G.-M. Transgenic wheat progeny resistant to powdery mildew generated by Agrobacterium inoculum to the basal portion of wheat seedling. Plant Cell Rep. 2006, 25, 1199–1204. [Google Scholar] [CrossRef] [PubMed]
Chromosome | No. of Bins | No. of SNPs | No. of Linkage Groups * | Length (cm) | Density | Max Interval (cm) |
---|---|---|---|---|---|---|
1A | 172 | 289 | 4 | 829.25 | 4.82 | 27.79 |
1B | 225 | 389 | 7 | 1105.54 | 4.91 | 26.43 |
1D | 118 | 314 | 8 | 678.66 | 5.75 | 27.12 |
2A | 212 | 561 | 6 | 1148.53 | 5.42 | 29.69 |
2B | 242 | 626 | 8 | 1167.14 | 4.82 | 28.88 |
2D | 99 | 365 | 13 | 415.6 | 4.20 | 25.29 |
3A | 198 | 416 | 9 | 977.92 | 4.94 | 26.03 |
3B | 318 | 607 | 3 | 1443.05 | 4.54 | 28.6 |
3D | 42 | 79 | 8 | 390.64 | 9.30 | 35.62 |
4A | 148 | 310 | 9 | 991.85 | 6.70 | 29.16 |
4B | 130 | 233 | 8 | 688.47 | 5.30 | 27.89 |
4D | 25 | 89 | 3 | 124.95 | 5.00 | 19.05 |
5A | 164 | 372 | 7 | 977.08 | 5.96 | 29.21 |
5B | 370 | 875 | 5 | 1332.7 | 3.60 | 28.47 |
5D | 21 | 32 | 5 | 187.41 | 8.92 | 25.21 |
6A | 164 | 373 | 5 | 1035.51 | 6.31 | 28.46 |
6B | 232 | 505 | 3 | 1010.31 | 4.35 | 29.6 |
6D | 18 | 33 | 3 | 87.64 | 4.87 | 26.57 |
7A | 207 | 507 | 8 | 1056.22 | 5.10 | 27.8 |
7B | 171 | 401 | 6 | 737.07 | 4.31 | 28.87 |
7D | 11 | 13 | 3 | 53.65 | 4.88 | 24.54 |
A genome | 1265 | 2828 | 48 | 7016.36 | 5.55 | 29.69 |
B genome | 1688 | 3636 | 40 | 7484.28 | 4.43 | 29.6 |
D genome | 334 | 925 | 43 | 1938.55 | 5.80 | 35.62 |
Whole genome | 3287 | 7389 | 131 | 16,439.19 | 5.00 | 35.62 |
QTLs | Chromosome | Position | Left Marker | Right Marker | LOD | PVE (%) | Add |
---|---|---|---|---|---|---|---|
Qawn-1D | 1D | 37 | IWB48378 | IWB29002 | 3.2713 | 0.6319 | 0.0699 |
Qawn-5A | 5A | 1 | IWB65661 | IWB60644 | 97.3171 | 91.2205 | −0.5019 |
Qawn-7B | 7B | 200 | IWB3369 | IWB10089 | 25.5369 | 2.7552 | −0.0106 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Liu, T.; Shi, X.; Wang, J.; Song, J.; Xiao, E.; Wang, Y.; Gao, X.; Nan, W.; Wang, Z. Mapping and Characterization of QTLs for Awn Morphology Using Crosses between “Double-Awn” Wheat 4045 and Awnless Wheat Zhiluowumai. Plants 2021, 10, 2588. https://doi.org/10.3390/plants10122588
Liu T, Shi X, Wang J, Song J, Xiao E, Wang Y, Gao X, Nan W, Wang Z. Mapping and Characterization of QTLs for Awn Morphology Using Crosses between “Double-Awn” Wheat 4045 and Awnless Wheat Zhiluowumai. Plants. 2021; 10(12):2588. https://doi.org/10.3390/plants10122588
Chicago/Turabian StyleLiu, Tianxiang, Xue Shi, Jun Wang, Jiawang Song, Enshi Xiao, Yong Wang, Xin Gao, Wenzhi Nan, and Zhonghua Wang. 2021. "Mapping and Characterization of QTLs for Awn Morphology Using Crosses between “Double-Awn” Wheat 4045 and Awnless Wheat Zhiluowumai" Plants 10, no. 12: 2588. https://doi.org/10.3390/plants10122588