Abstract
Key Message
QMS-5B, a major QTL for photo-thermo-sensitive genic male sterility in wheat, was fine mapped in a 2.15 Mb region harboring a serine/threonine protein kinase gene TraesCS5B03G0887500, which was the most likely candidate gene.
Abstract
Genic male sterility is an essential trait in the utilization of heterosis and hybrid seed production for wheat. Currently, genic male sterile genes have been reported in wheat mutants, but the sterile genes controlling photo-thermo-sensitive genic male sterility in wheat have not been studied systematically. Here, 235 doubled haploid lines derived from a cross between photo-thermo-sensitive genic male sterile line BS462 and its restorer line CP279 were used to map male sterile gene by GenoBaits® Wheat 100 K Panel, bulked segregant exome sequencing (BSE-Seq) and wheat 660 K array. As a result, the major stable QTL on chromosome 5B, QMS-5B, was identified in all four environments, accounting for 7.3–36.4% of the phenotypic variances. Ulteriorly, QMS-5B was delimited to an approximate 2.15 Mb physical interval between KASP-5B5 and KASP-5B6 using kompetitive allele-specific PCR (KASP) markers. Within the interval, twenty-nine high-confidence genes were predicted according to Chinese Spring RefSeq v2.1. TraesCS5B03G0887500, encoding a serine/threonine protein kinase, was identified as the most likely candidate gene for QMS-5B based on weighted gene co-expression network analysis. Expression analysis confirmed that TraesCS5B03G0887500 was significantly differentially expressed in anthers of BS462 and CP279 at different stages under fertile and sterile environments. In addition, flanking KASP marker KASP-5B6 can effectively genotype male sterile lines and restorer lines, and can be used for molecular marker-assisted selection. This study provides insights into for exploring the mechanism of photo-thermo-sensitive genic male sterility in wheat.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Abbreviations
- Bns:
-
Binucleate stage
- BSE-Seq:
-
Bulked segregant exome sequencing
- DH:
-
Doubled haploid
- Ds:
-
Dyad stage
- KASP:
-
Kompetitive allele-specific PCR
- Mmcs:
-
Microspore mother cell stage
- QTL:
-
Quantitative trait locus
- SNP:
-
Single nucleotide polymorphism
- Tns:
-
Trinucleate stage
- Ts:
-
Tetrad stage
- Uns:
-
Uninucleate stage
- WGCNA:
-
Weighted gene co-expression network analysis
References
Anderberg RJ, Walker-Simmons MK (1992) Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. Proc Natl Acad Sci USA 89:10183–10187. https://doi.org/10.1073/pnas.89.21.10183
Cao SH, Guo XL, Liu DC, Zhang XQ, Zhang AM (2004) Preliminary gene-mapping of photoperiod-temperature sensitive genic male sterility in wheat (Triticum aestivum L.). J Genet Genom 31:293–298. https://doi.org/10.1088/1009-0630/6/5/011
Chang Z, Chen Z, Wang N, Xie G, Lu J, Yan W, Zhou J, Tang X, Deng XW (2016) Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene. Proc Natl Acad Sci USA 113:14145–14150. https://doi.org/10.1073/pnas.1613792113
Chen X, Sun D, Rong DF, Sun G, Peng J (2010) Relationship of genetic distance and hybrid performance in hybrids derived from a new photoperiod-thermo sensitive male sterile wheat line 337S. Euphytica 175:365–371. https://doi.org/10.1007/s10681-010-0182-3
Deng XW, Wang H, Tang X, Zhou J, Xu Z (2013) Hybrid rice breeding welcomes a new era of molecular crop design. Sci Sin Vitae 43:864–868. https://doi.org/10.1360/052013-299
Deng Z, Li X, Wang Z, Jiang Y, Wan L, Dong F, Chen F, Hong D, Yang G (2016) Map-based cloning reveals the complex organization of the BnRf locus and leads to the identification of BnRf (b), a male sterility gene, in Brassica napus. Theor Appl Genet 129:53–64. https://doi.org/10.1007/s00122-015-2608-8
Dong Y, Xu D, Xu X, Ren Y, Gao F, Song J, Jia A, Hao Y, He Z, Xia X (2022) Fine mapping of QPm.caas-3BS, a stable QTL for adult-plant resistance to powdery mildew in wheat (Triticum aestivum L.). Theor Appl Genet 135:1083–1099. https://doi.org/10.1007/s00122-021-04019-2
Ferreira PC, Hemerly AS, Villarroel R, Van Montagu M, Inzé D (1991) The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 3:531–540. https://doi.org/10.1105/tpc.3.5.531
Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockström J, Sheehan J, Siebert S, Tilman D, Zaks DP (2011) Solutions for a cultivated planet. Nature 478:337–342. https://doi.org/10.1038/nature10452
Guo RX, Sun DF, Tan ZB, Rong DF, Li CD (2006) Two recessive genes controlling thermophotoperiod-sensitive male sterility in wheat. Theor Appl Genet 112:1271–1276. https://doi.org/10.1007/s00122-006-0228-z
Han Y, Zhao F, Gao S, Wang X, Wei A, Chen Z, Liu N, Tong X, Fu X, Wen C (2017) Fine mapping of a male sterility gene ms-3 in a novel cucumber (Cucumis sativus L.) mutant. Theor Appl Genet 131:449–460. https://doi.org/10.1007/s00122-017-3013-2
Huang S, Zhang Y, Ren H, Zhang X, Yu R, Liu S, Zeng Q, Wang Q, Yuan F, Singh RP, Bhavani S, Wu J, Han D, Kang Z (2023) High density mapping of wheat stripe rust resistance gene QYrXN3517-1BL using QTL mapping, BSE-Seq and candidate gene analysis. Theor Appl Genet 136:39. https://doi.org/10.1007/s00122-023-04282-5
Ji G, Xu Z, Fan X, Zhou Q, Yu Q, Liu X, Liao S, Feng B, Wang T (2021) Identification of a major and stable QTL on chromosome 5A confers spike length in wheat (Triticum aestivum L.). Mol Breed 41:56. https://doi.org/10.1007/s11032-021-01249-6
Ji G, Xu Z, Fan X, Zhou Q, Chen L, Yu Q, Liao S, Jiang C, Feng B, Wang T (2023) Identification and validation of major QTL for grain size and weight in bread wheat (Triticum aestivum L.). Crop J 11:9. https://doi.org/10.1016/j.cj.2022.06.014
Jiang Y, Duan L, Guan F, Yao F, Long L, Wang Y, Zhao X, Li H, Li W, Xu Q, Jiang Q, Wang J, Wei Y, Ma J, Kang H, Qi P, Deng M, Zheng Y, Chen G (2022) Exome sequencing from bulked segregant analysis identifies a gene for all-stage resistance to stripe rust on chromosome 1AL in Chinese wheat landrace “Xiaohemai.” Plant Dis 106:1209–1215. https://doi.org/10.1094/PDIS-08-21-1618-RE
Jin H, Wen W, Liu J, Zhai S, Zhang Y, Yan J, Liu Z, Xia X, He Z (2016) Genome-wide QTL mapping for wheat processing quality parameters in a Gaocheng 8901/Zhoumai 16 recombinant inbred line population. Front Plant Sci 7:1032. https://doi.org/10.3389/fpls.2016.01032
Jin H, Zhang H, Zhao X, Long L, Guan F, Wang Y, Huang L, Zhang X, Wang Y, Li H, Li W, Pu Z, Zhang Y, Xu Q, Jiang Q, Wei Y, Ma J, Qi P, Deng M, Kang H, Zheng Y, Chen G, Jiang Y (2023) Identification of a suppressor for the wheat stripe rust resistance gene Yr81 in Chinese wheat landrace Dahongpao. Theor Appl Genet 136:67. https://doi.org/10.1007/s00122-023-04347-5
Klindworth DL, Williams ND, Maan SS (2002) Chromosomal location of genetic male sterility genes in four mutants of hexaploid wheat. Crop Sci 42:1447–1450. https://doi.org/10.2135/cropsci2002.1447
Lei D, Jian A, Huang X, Liu X, Chen L, Bai W, Cheng S, He X, Xiong Y, Yu X, Wang C, Zheng H, You S, Wang Q, Lu J, Hu Y, Xie Z, Jiang L, Zhang X, Ren Y, Lei C, Cheng Z, Lin Q, Wu C, Zhu S, Zhao Z, Wan J (2023) Anther-specific expression of OsRIP1 causes dominant male sterility in rice. Plant Biotechnol J 21:1932–1934. https://doi.org/10.1111/pbi.14140
Liu Z, Li S, Li W, Liu Q, Zhang L, Song X (2020) Comparative transcriptome analysis indicates that a core transcriptional network mediates isonuclear alloplasmic male sterility in wheat (Triticum aestivum L.). BMC Plant Biol 20:10. https://doi.org/10.1186/s12870-019-2196-x
Longin CF, Mühleisen J, Maurer HP, Zhang H, Gowda M, Reif JC (2012) Hybrid breeding in autogamous cereals. Theor Appl Genet 125:1087–1096. https://doi.org/10.1007/s00122-012-1967-7
Ma Q, Chen C, Zeng Z, Zou Z, Li H, Zhou Q, Chen X, Sun K, Li X (2018) Transcriptomic analysis between self- and cross-pollinated pistils of tea plants (Camellia sinensis). BMC Genomics 19:289. https://doi.org/10.1186/s12864-018-4674-1
Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436. https://doi.org/10.1126/science.7902614
Moon J, Skibbe D, Timofejeva L, Wang CJ, Kelliher T, Kremling K, Walbot V, Cande WZ (2013) Regulation of cell divisions and differentiation by MALE STERILITY32 is required for anther development in maize. Plant J 76:592–602. https://doi.org/10.1111/tpj.12318
Mu Y, Gong W, Qie Y, Liu X, Li L, Sun N, Liu W, Guo J, Han R, Yu Z, Xiao L, Su F, Zhang W, Wang J, Han G, Ma P (2022) Identification of the powdery mildew resistance gene in wheat breeding line Yannong 99102–06188 via bulked segregant exome capture sequencing. Front Plant Sci 13:1005627. https://doi.org/10.3389/fpls.2022.1005627
Ni F, Qi J, Hao Q, Lyu B, Luo MC, Wang Y, Chen F, Wang S, Zhang C, Epstein L, Zhao X, Wang H, Zhang X, Chen C, Sun L, Fu D (2017) Wheat Ms2 encodes for an orphan protein that confers male sterility in grass species. Nat Commun 8:15121. https://doi.org/10.1038/ncomms15121
Niu F, Bu Y, Yang X, Wu Y, He M, Zhang L, Song X (2023) Rfd1, a restorer to the Aegilops juvenalis cytoplasm, functions in fertility restoration of wheat cytoplasmic male sterility. J Exp Bot 74:1432–1447. https://doi.org/10.1093/jxb/erac484
Pallotta MA, Warner P, Kouidri A, Tucker EJ, Baes M, Suchecki R, Watson-Haigh N, Okada T, Garcia M, Sandhu A, Singh M, Wolters P, Albertsen MC, Cigan AM, Baumann U, Whitford R (2019) Wheat ms5 male-sterility is induced by recessive homoeologous Aand D genome non-specific lipid transfer proteins. Plant J 99:673–685. https://doi.org/10.1111/tpj.14350
Peng G, Liu Z, Zhuang C, Zhou H (2023) Environment-sensitive genic male sterility in rice and other plants. Plant Cell Environ 46:1120–1142. https://doi.org/10.1111/pce.14503
Perez-Prat E, van LookerenCampagne MM (2002) Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci 7:199–203. https://doi.org/10.1016/s1360-1385(02)02252-5
Qin R, Ma T, Cai Y, Shi X, Cheng J, Dong J, Wang C, Li S, Pan G, Guan Y, Zhang L, Yang S, Xu H, Zhao C, Sun H, Li X, Wu Y, Li J, Cui F (2023) Characterization and fine mapping analysis of a major stable QTL qKnps-4A for kernel number per spike in wheat. Theor Appl Genet 136:211. https://doi.org/10.1007/s00122-023-04456-1
Rudrabhatla P, Reddy MM, Rajasekharan R (2006) Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Mol Biol 60:293–319. https://doi.org/10.1007/s11103-005-4109-7
Sharma A, Komatsu S (2002) Involvement of Ca2+-dependent protein kinase component downstream to the gibberellin-binding phosphoprotein, Rubis CO activase, in rice. Biochem Biophys Res Commun 290:690–695. https://doi.org/10.1006/bbrc.2001.6269
Song J, Li L, Liu B, Dong Y, Dong Y, Li F, Liu S, Luo X, Sun M, Ni Z, Fei S, Xia X, Ni Z, He Z, Cao S (2023) Fine mapping of reduced height locus RHT26 in common wheat. Theor Appl Genet 136:62. https://doi.org/10.1007/s00122-023-04331-z
Tang H, Dong H, Guo X, Cheng M, Li M, Chen Q, Yuan Z, Pu Z, Wang J (2023) Identification of candidate gene for the defective kernel phenotype using bulked segregant RNA and exome capture sequencing methods in wheat. Front Plant Sci 14:1173861. https://doi.org/10.3389/fpls.2023.1173861
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677. https://doi.org/10.1038/nature01014
Tucker EJ, Baumann U, Kouidri A, Suchecki R, Baes M, Garcia M, Okada T, Dong C, Wu Y, Sandhu A, Singh M, Langridge P, Wolters P, Albertsen MC, Cigan AM, Whitford R (2017) Molecular identification of the wheat male fertility gene Ms1 and its prospects for hybrid breeding. Nat Commun 8:869. https://doi.org/10.1038/s41467-017-00945-2
Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoprotein of Brassica. Nature 345:743–746. https://doi.org/10.1038/345743a0
Wang Z, Li J, Chen S, Heng Y, Chen Z, Yang J, Zhou K, Pei J, He H, Deng XW, Ma L (2017) Poaceae-specific MS1 encodes a phospholipid-binding protein for male fertility in bread wheat. Proc Natl Acad Sci U S A 114:12614–12619. https://doi.org/10.1073/pnas.1715570114
Wu J, Wang Q, Xu L, Chen X, Li B, Mu J, Zeng Q, Huang L, Han D, Kang Z (2018) Combining single nucleotide polymorphism genotyping array with bulked segregant analysis to map a gene controlling adult plant resistance to stripe rust in wheat line 03031–1-5 H62. Phytopathology 108:103–113. https://doi.org/10.1094/PHYTO-04-17-0153-R
Xing QH, Ru ZG, Zhou CJ, Xue X, Liang CY, Yang DE, Jin DM, Wang B (2003) Genetic analysis, molecular tagging and mapping of the thermo-sensitive genic male-sterile gene (wtms1) in wheat. Theor Appl Genet 107:1500–1504. https://doi.org/10.1007/s00122-003-1385-y
Xu J, Wang B, Wu Y, Du P, Wang J, Wang M, Yi C, Gu M, Liang G (2011) Fine mapping and candidate gene analysis of ptgms2-1, the photoperiod-thermo-sensitive genic male sterile gene in rice (Oryza sativa L.). Theor Appl Genet 122:365–372. https://doi.org/10.1007/s00122-010-1452-0
Xu D, Shi J, Rautengarten C, Yang L, Qian X, Uzair M, Zhu L, Luo Q, An G, Waßmann F, Schreiber L, Heazlewood JL, Scheller HV, Hu J, Zhang D, Liang W (2017) Defective pollen wall 2 (DPW2) encodes an acyl transferase required for rice pollen development. Plant Physiol 173:240–255. https://doi.org/10.1104/pp.16.00095
Xu C, Xu Y, Wang Z, Zhang X, Wu Y, Lu X, Sun H, Wang L, Zhang Q, Zhang Q, Li X, Xiao J, Li X, Zhao M, Ouyang Y, Huang X, Zhang Q (2023) Spontaneous movement of a retrotransposon generated genic dominant male sterility providing a useful tool for rice breeding. Natl Sci Rev 10:210. https://doi.org/10.1093/nsr/nwad210
Yang L, Zhao D, Meng Z, Xu K, Yan J, Xia X, Cao S, Tian Y, He Z, 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
Ye M, Wan H, Yang W, Liu Z, Wang Q, Yang N, Long H, Deng G, Yang Y, Feng H, Zhou Y, Yang C, Li J, Zhang H (2023) Precisely mapping a major QTL for grain weight on chromosome 5B of the founder parent Chuanmai42 in the wheat-growing region of southwestern China. Theor Appl Genet 136:146. https://doi.org/10.1007/s00122-023-04383-1
Yuan S, Bai J, Guo H, Duan W, Zhang L (2020) QTL mapping of male sterility-related traits in a photoperiod and temperature-sensitive genic male sterile wheat line BS366. Plant Breeding 139:498–507. https://doi.org/10.1111/pbr.12811
Zhai S, Liu J, Xu D, Wen W, Yan J, Zhang P, Wan Y, Cao S, Hao Y, Xia X, Ma W, He Z (2018) A genome-wide association study reveals a rich genetic architecture of flour color-related traits in bread wheat. Front Plant Sci 9:1136. https://doi.org/10.3389/fpls.2018.01136
Zhang C, Zhao H, Liu Y, Li Q, Liu X, Tan H, Yuan C, Dong Y (2010a) Isolation and characterization of a novel glycogen synthase kinase-3 gene, GmGSK, in Glycine max L. that enhances abiotic stress tolerance in Saccharomyces cerevisiae. Biotechnol Lett 32:861–866. https://doi.org/10.1007/s10529-010-0220-1
Zhang LP, Tian ZM, Zhao CP, Wang LH, Shan FH, Zhang FT, Yuan SH (2010b) QTL mapping for photoperiod-temperature sensitive genic male sterility of BS20 in common wheat. J Agri Biotech 18:437–444. https://doi.org/10.1080/00949651003724790
Zhang P, Zhao Z, Zheng M, Liu Y, Niu Q, Liu X, Shi Z, Yi H, Yu T, Rong T, Cao M (2023) Fine mapping and candidate gene analysis of a novel fertility restorer gene for C-type cytoplasmic male sterility in maize (Zea mays L.). Theor Appl Genet 136:234. https://doi.org/10.1007/s00122-023-04480-1
Zhao L, Yang Y, Hu P, Qiao Q, Lv G, Li J, Liu L, Wei J, Ren Y, Dong Z, Chen F (2023) Genetic mapping and analysis of candidate leaf color genes in common winter wheat (Triticum aestivum L.). Mol Breed 43:48. https://doi.org/10.1007/s11032-023-01395-z
Zhou S, Zhang J, Che Y, Liu W, Lu Y, Yang X, Li X, Jia J, Liu X, Li L (2018) Construction of Agropyron Gaertn. genetic linkage maps using a wheat 660K SNP array reveals a homoeologous relationship with the wheat genome. Plant Biotechnol J 16:818–827. https://doi.org/10.1111/pbi.12831
Acknowledgements
The authors gratefully thank MolBreeding Biotech Ltd. for their help with GenoBaits® Wheat 100K Panel and BSE-Seq analysis. And the authors gratefully thank China Golden Marker Biotech Co., Ltd. for their help with wheat 660K SNP array genotyping.
Funding
This study was sponsored by the National Natural Science Foundation for Young Scientists of China (32001534); Beijing Municipal Natural Science Foundation (6232010); Outstanding Scientist Cultivation Program of BAAFS (JKZX202210); National Natural Science Foundation of China (32272108); Foundation for Youths of BAAFS (QNJJ202212).
Author information
Authors and Affiliations
Contributions
LPZ, XYS and CPZ conceived and designed the study. FQN and ZHL performed the experiments, analyzed the data and wrote the article with contributions from all of the authors. FTZ and SHY provided experimental materials. YML, HZ and HSZ participated in field trials. JFB and YJL revised and polished this manuscript. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
We declare that these experiments complied with the ethical standards in China.
Additional information
Communicated by Mark E. Sorrells.
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
Niu, F., Liu, Z., Zhang, F. et al. Identification and validation of major-effect quantitative trait locus QMS-5B associated with male sterility in photo-thermo-sensitive genic male sterile wheat. Theor Appl Genet 136, 257 (2023). https://doi.org/10.1007/s00122-023-04500-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00122-023-04500-0