Abstract
Key message
Major QTL for grain zinc and iron concentrations were identified on the long arm of chromosomes 2D and 6D. Gene-based KASP markers were developed for putative candidate genes TaIPK1-2D and TaNAS10-6D.
Abstract
Micronutrient malnutrition is one of the most common public health problems in the world. Biofortification, the most attractive and sustainable solution to surmount malnutrition requires the development of micronutrient enriched new crop cultivars. In this study, two recombinant inbred line (RIL) populations, ZM175/XY60 and ZM175/LX987, were used to identify QTL for grain zinc concentration (GZnC), grain iron concentration (GFeC) and thousand grain weight (TGW). Eight QTL for GZnC, six QTL for GFeC and five QTL for TGW were detected. Three QTL on chromosomes 2DL and 4BS and chromosome 6A showed pleiotropic effects on all three traits. The 4BS and 6A QTL also increased plant height and might be Rht-B1a and Rht25a, respectively. The 2DL locus within a suppressed recombination region was identified in both RIL populations and the favorable allele simultaneously increasing GZnC, GFeC and TGW was contributed by XY60 and LX987. A QTL on chromosome 6DL associated only with GZnC was detected in ZM175/XY60 and was validated in JD8/AK58 RILs using kompetitive allele-specific PCR (KASP) marker K_AX-110119937. Both the 2DL and 6DL QTL were new loci for GZnC. Based on gene annotations, sequence variations and expression profiles, the phytic acid biosynthesis gene TaIPK1-2D and nicotianamine synthase gene TaNAS10-6D were predicted as candidate genes. Their gene-based KASP markers were developed and validated in a cultivar panel of 343 wheat accessions. This study investigated the genetic basis of GZnC and GFeC and provided valuable candidate genes and markers for breeding Zn- and Fe-enriched wheat.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aggarwal S, Kumar A, Bhati KK, Kaur G, Shukla V, Tiwari S, Pandey AK (2018) RNAi-mediated downregulation of inositol pentakisphosphate linase (IPK1) in wheat grains decreases phytic acid levels and increases Fe and Zn accumulation. Front Plant Sci 9:259. https://doi.org/10.3389/fpls.2018.00259
Ali MW, Borrill P (2020) Applying genomic resources to accelerate wheat biofortification. Heredity 125:386–395. https://doi.org/10.1038/s41437-020-0326-8
Bonneau J, Baumann U, Beasley J, Li Y, Johnson AA (2016) Identification and molecular characterization of the nicotianamine synthase gene family in bread wheat. Plant Biotechnol J 14:2228–2239. https://doi.org/10.1111/pbi.12577
Bouis HE, Hotz C, McClafferty B, Meenakshi JV, Pfeiffer WH (2011) Biofortification: a new tool to reduce micronutrient malnutrition. Food Nutr Bull 32:S31–S40. https://doi.org/10.1079/9781780642994.020
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
Cakmak I (2007) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17. https://doi.org/10.1007/s11104-007-9466-3
Cakmak I, Pfeiffer WH, McClafferty B (2010) Biofortification of durum wheat with zinc and iron. Cereal Chem 87:10–20. https://doi.org/10.1094/CCHEM-87-1-0010
Crespo-Herrera LA, Velu G, Singh RP (2016) Quantitative trait loci mapping reveals pleiotropic effect for grain iron and zinc concentrations in wheat. Ann Appl Bio 169:27–35. https://doi.org/10.1111/aab.12276
Cui F, Zhao C, Ding A, Li J, Wang L, Li X, Bao Y, Li J, Wang H (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
Cui F, Fan X, Chen M, Zhang N, Zhao C, Zhang W, Han J, Ji J, Zhao X, Yang L, Zhao Z, Tong Y, Wang T, Li J (2016) QTL detection for wheat grain size and quality and the responses of these traits to low nitrogen stress. Theor Appl Genet 129:469–484. https://doi.org/10.1007/s00122-015-2641-7
Distelfeld A, Cakmak I, Peleg Z, Ozturk L, Yazici AM, Budak H, Saranga Y, Fahima T (2007) Multiple QTL-effects of wheat Gpc-B1 locus on grain protein and micronutrient concentrations. Physiol Plantarum 129:635–643. https://doi.org/10.1111/j.1399-3054.2006.00841.x
Fan MS, Zhao FJ, Fairweather-Tait SJ, Poulton PR, Dunham SJ, McGrath SP (2008) Evidence of decreasing mineral density in wheat grain over the last 160 years. J Trace Elem Med Biol 22:315–324. https://doi.org/10.1016/j.jtemb.2008.07.002
FAO, IFAD, UNICEF, WFP, WHO (2022) The state of food security and nutrition in the world 2022. Repurposing food and agricultural policies to make healthy diets more affordable. Rome, FAO. https://doi.org/10.4060/cc0639en
Ford BA, Foo E, Sharwood R, Karafiatova M, Vrana J, MacMillan C, Nichols DS, Steuernagel B, Uauy C, Dolezel J, Chandler PM, Spielmeyer W (2018) Rht18 semidwarfism in wheat is due to increased GA2-oxidaseA9 expression and reduced GA content. Plant Physiol 177:168–180. https://doi.org/10.1104/pp.18.00023
Guo Z, Yang Q, Huang F, Zheng H, Sang Z, Xu Y, Zhang C, Wu K, Tao J, Prasanna BM, Olsen MS, Wang Y, Zhang J, Xu Y (2021) Development of high-resolution multiple-SNP arrays for genetic analyses and molecular breeding through genotyping by target sequencing and liquid chip. Plant Commun 2:100230. https://doi.org/10.1016/j.xplc.2021.100230
Gupta PK, Balyan HS, Sharma S, Kumar R (2020a) Biofortification and bioavailability of Zn, Fe and Se in wheat: present status and future prospects. Theor Appl Genet 134:1–35. https://doi.org/10.1007/s00122-020-03709-7
Gupta PK, Balyan HS, Sharma S, Kumar R (2020b) Genetics of yield, abiotic stress tolerance and biofortification in wheat (Triticum aestivum L.). Theor Appl Genet 133:1569–1602. https://doi.org/10.1007/s00122-020-03583-3
Hao Y, Velu G, Peña RJ, Singh S, Singh RP (2014) Genetic loci associated with high grain zinc concentration and pleiotropic effect on grain weight in wheat (Triticum aestivum L.). Mol Breed 34:1893–1902. https://doi.org/10.1007/s11032-014-0147-7
Hao C, Jiao C, Hou J, Li T, Liu H, Wang Y, Zheng J, Liu H, Bi Z, Xu F, Zhao J, Ma L, Wang Y, Majeed U, Liu X, Appels R, Maccaferri M, Tuberosa R, Lu H, Zhang X (2020) Resequencing of 145 landmark cultivars reveals asymmetric sub-genome selection and strong founder genotype effects on wheat breeding in China. Mol Plant 13:1733–1751. https://doi.org/10.1016/j.molp.2020.09.001
Haque M, Martinek P, Watanabe N, Kuboyama T (2011) Genetic mapping of gibberellic acid-sensitive genes for semi-dwarfism in durum wheat. Cereal Res Commun 39:171–178. https://doi.org/10.1556/crc.39.2011.2.1
He Z, Chen X, Wang D, Zhang Y, Xiao Y, Li F, Zhang Y, Li S, Xia X, Zhang Y, Zhuang Q (2015) Characterization of wheat cultivar Zhongmai 175 with high yielding potential, high water and fertilizer use efficiency, and broad adaptability. Sci Agric Sin 48:3394–3403. https://doi.org/10.3864/j.issn.0578-1752.2015.17.007(inChinese)
Heidari B, Sayed-Tabatabaei BE, Saeidi G, Kearsey M, Suenaga K (2011) Mapping QTL for grain yield, yield components, and spike features in a doubled haploid population of bread wheat. Genome 54:517–527. https://doi.org/10.1139/g11-017
Heidari B, Padash S, Dadkhodaie A (2016) Variations in micronutrients, bread quality and agronomic traits of wheat landrace varieties and commercial cultivars. Aust J Crop Sci 10:377–384. https://doi.org/10.21475/ajcs.2016.10.03.p7231
Holland J, Nyquist W, Cervantes-Martínez C (2003) Estimating and interpreting heritability for plant breeding: an update. Plant Breed Rev 22:11–112. https://doi.org/10.1002/9780470650202.ch2
Hu M, Zhao X, Liu Q, Hong X, Zhang W, Zhang Y, Sun L, Li H, Tong Y (2018) Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnol J 16:1858–1867. https://doi.org/10.1111/pbi.12921
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
Jobson EM, Martin JM, Schneider TM, Giroux MJ (2018) The impact of the Rht-B1b, Rht-D1b, and Rht-8 wheat semidwarfing genes on flour milling, baking, and micronutrients. Cereal Chem 95:770–778. https://doi.org/10.1002/cche.10091
Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374. https://doi.org/10.1534/genetics.106.066811
Li Z, Li B, Tong Y (2008) The contribution of distant hybridization with decaploid Agropyron elongatum to wheat improvement in China. J Genet Genomics 35:451–456. https://doi.org/10.1016/S1673-8527(08)60062-4
Li X, Zhao X, He X, Zhao G, Li B, Liu D, Zhang A, Zhang X, Tong Y, Li Z (2011) Haplotype analysis of the genes encoding glutamine synthetase plastic isoforms and their association with nitrogen-use- and yield-related traits in bread wheat. New Phytol 189:449–458. https://doi.org/10.1111/j.1469-8137.2010.03490.x
Li H, Zhou Y, Xin W, Wei Y, Zhang J, Guo L (2019) Wheat breeding in northern China: achievements and technical advances. Crop J 7:718–729. https://doi.org/10.1016/j.cj.2019.09.003
Liu H, Wang ZH, Li F, Li K, Yang N, Yang Y, Huang D, Liang D, Zhao H, Mao H, Liu J, Qiu W (2014a) Grain iron and zinc concentrations of wheat and their relationships to yield in major wheat production areas in China. Field Crop Res 156:151–160. https://doi.org/10.1016/j.fcr.2013.11.011
Liu G, Jia L, Lu L, Qin D, Zhang J, Guan P, Ni Z, Yao Y, Sun Q, Peng H (2014b) Mapping QTLs of yield-related traits using RIL population derived from common wheat and Tibetan semi-wild wheat. Theor Appl Genet 127:2415–2432. https://doi.org/10.1007/s00122-014-2387-7
Liu J, Wu B, Singh RP, Velu G (2019) QTL mapping for micronutrients concentration and yield component traits in a hexaploid wheat mapping population. J Cereal Sci 88:57–64. https://doi.org/10.1016/j.jcs.2019.05.008
Luo Q, Zheng Q, Hu P, Liu L, Yang G, Li H, Li B, Li Z (2020) Mapping QTL for agronomic traits under two levels of salt stress in a new constructed RIL wheat population. Theor Appl Genet 134:171–189. https://doi.org/10.1007/s00122-020-03689-8
Luo Q, Hu P, Yang G, Li H, Liu L, Wang Z, Li B, Li Z, Zheng Q (2021) Mapping QTL for seedling morphological and physiological traits under normal and salt treatments in a RIL wheat population. Theor Appl Genet 134:2991–3011. https://doi.org/10.1007/s00122-021-03872-5
Monasterio I, Graham RD (2000) Breeding for trace minerals in wheat. Food Nutr Bull 21:392–396. https://doi.org/10.1177/1564826500021004
Murphy KM, Reeves PG, Jones SS (2008) Relationship between yield and mineral nutrient concentrations in historical and modern spring wheat cultivars. Euphytica 163:381–390. https://doi.org/10.1007/s10681-008-9681-x
Ortiz-Monasterio JI, Palacios-Rojas N, Meng E, Pixley K, Trethowan R, Peña RJ (2007) Enhancing the mineral and vitamin content of wheat and maize through plant breeding. J Cereal Sci 46:293–307. https://doi.org/10.1016/j.jcs.2007.06.005
Paltridge NG, Milham PJ, Ortiz-Monasterio JI, Velu G, Yasmin Z, Palmer LJ, Guild GE, Stangoulis JCR (2012) Energy-dispersive X-ray fluorescence spectrometry as a tool for zinc, iron and selenium analysis in whole grain wheat. Plant Soil 361:261–269. https://doi.org/10.1007/s11104-012-1423-0
Ramírez-González RH, Uauy C, Caccamo M (2015) PolyMarker: a fast polyploid primer design pipeline. Bioinformatics 31:2038–2039. https://doi.org/10.1093/bioinformatics/btv069
Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Uauy C (2018) The transcriptional landscape of polyploid wheat. Science 361:eaar6089. https://doi.org/10.1126/science.aar6089
Shariatipour N, Heidari B, Richards CM (2021a) Meta-analysis of QTLome for grain zinc and iron contents in wheat (Triticum aestivum L.). Euphytica 217:86. https://doi.org/10.1007/s10681-021-02818-8
Shariatipour N, Heidari B, Tahmasebi A, Richards C (2021b) Comparative genomic analysis of quantitative trait loci associated with micronutrient contents, grain quality, and agronomic traits in wheat (Triticum aestivum L.). Front Plant Sci 12:709817. https://doi.org/10.3389/fpls.2021.709817
Shi W, Hao C, Zhang Y, Cheng J, Zhang Z, Liu J, Yi X, Cheng X, Sun D, Xu Y, Zhang X, Cheng S, Guo P, Guo J (2017) A combined association mapping and linkage analysis of grain number per spike in common wheat (Triticum aestivum L.). Front Plant Sci 8:1412. https://doi.org/10.3389/fpls.2017.01412
Su Q, Zhang X, Zhang W, Zhang N, Song L, Liu L, Xue X, Liu G, Liu J, Meng D, Zhi L, Ji J, Zhao X, Yang C, Tong Y, Liu Z, Li J (2018) QTL detection for grain size and weight in bread wheat (Triticum aestivum L.) uing a high-density SNP and SSR-based linkage map. Front Plant Sci 9:1484. https://doi.org/10.3389/fpls.2018.01484
Tahmasebi S, Heidari B, Pakniyat H, McIntyre CL (2016) Mapping QTLs associated with agronomic and physiological traits under drought and terminal-heat stress conditions in wheat (Triticum aestivum L.). Genome. https://doi.org/10.1139/gen-2016-0017
Tian X, Xia X, Xu D, Liu Y, Xie L, Hassan MA, Song J, Li F, Wang D, Zhang Y, Hao Y, Li G, Chu C, He Z, Cao S (2022) Rht24b, an ancient variation of TaGA2ox-A9, reduces plant height without yield penalty in wheat. New Phytol 233:738–750. https://doi.org/10.1111/nph.17808
Tong J, Sun M, Wang Y, Zhang Y, Rasheed A, Li M, Xia X, He Z, Hao Y (2020) Dissection of molecular processes and genetic architecture underlying iron and zinc homeostasis for biofortification: from model plants to common wheat. Int J Mol Sci 21:9280. https://doi.org/10.3390/ijms21239280
Tong J, Zhao C, Sun M, Fu L, Song J, Liu D, Zhang Y, Zheng J, Pu Z, Liu L, Rasheed A, Li M, Xia X, He Z, Hao Y (2022) High resolution genome wide association studies reveal rich genetic architectures of grain zinc and iron in common wheat (Triticum aestivum L.). Front Plant Sci 13:840614. https://doi.org/10.3389/fpls.2022.840614
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301. https://doi.org/10.1126/science.1133649
Velu G, Ortiz-Monasterio I, Cakmak I, Hao Y, Singh RP (2014) Biofortification strategies to increase grain zinc and iron concentrations in wheat. J Cereal Sci 59:365–372. https://doi.org/10.1016/j.jcs.2013.09.001
Velu G, Singh RP, Huerta J, Guzman C (2017) Genetic impact of Rht dwarfing genes on grain micronutrients concentration in wheat. Field Crop Res 214:373–377. https://doi.org/10.1016/j.fcr.2017.09.030
Velu G, Crespo-Herrera L, Guzman C, Huerta J, Singh PT, RP, (2019) Assessing genetic diversity to breed competitive biofortified wheat with enhanced grain Zn and Fe concentrations. Front Plant Sci 9:1971. https://doi.org/10.3389/fpls.2018.01971
Wang Y, Xu X, Hao Y, Zhang Y, Liu Y, Pu Z, Tian Y, Xu D, Xia X, He Z, Zhang Y (2021) QTL mapping for grain zinc and iron concentrations in bread wheat. Front Nutr 8:680391. https://doi.org/10.3389/fnut.2021.680391
Welch RM (2002) The impact of mineral nutrients in food crops on global human health. Plant Soil 247:83–90. https://doi.org/10.1023/A:1021140122921
Welch RM, Graham RD (1999) A new paradigm for world agriculture: meeting human needs productive, sustainable, nutritious. Field Crop Res 60:1–10. https://doi.org/10.1016/S0378-4290(98)00129-4
Xu Y, Wang R, Tong Y, Zhao H, Xie Q, Liu D, Zhang A, Li B, Xu H, An D (2014) Mapping QTLs for yield and nitrogen-related traits in wheat: influence of nitrogen and phosphorus fertilization on QTL expression. Theor Appl Genet 127:59–72. https://doi.org/10.1007/s00122-013-2201-y
Xu X, Zhu Z, Jia A, Wang F, Wang J, Zhang Y, Fu C, Fu L, Bai G, Xia X, Hao Y, He Z (2019) Mapping of QTL for partial resistance to powdery mildew in two Chinese common wheat cultivars. Euphytica 216:1–12. https://doi.org/10.1007/s10681-019-2537-8
Zhang J, Li C, Zhang W, Zhang X, Mo Y, Tranquilli GE, Vanzetti LS, Dubcovsky J (2023) Wheat plant height locus RHT25 encodes a PLATZ transcription factor that interacts with DELLA (RHT1). Proc Natl Acad Sci 120:e2300203120. https://doi.org/10.1073/pnas.2300203120
Acknowledgments
We thank Prof. R. A. McIntosh, Plant Breeding Institute, University of Sydney, for review of the draft manuscript. This study was financially supported by the National Key Research and Development Program of China (2021YFF1000204 and 2020YFE0202300), the National Natural Science Foundation of China (31961143007), the Agricultural Science and Technology Innovation Program (CAAS-ZDRW202109) and Fundamental Research Funds for Central Non-Profit of Institute of Crop Sciences, CAAS.
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YH and QZ designed the experiments; MS and YH wrote the draft manuscript; MS performed the experiments and data analysis; QL performed genotypic data analysis and QTL mapping; JT, YW, ZP and JZ participated in phenotyping; JT, YW, JS, YZ, LL and AZ participated in field trials; and YH, AR, ML, SC, XX and ZH reviewed and revised the manuscript.
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Sun, M., Luo, Q., Zheng, Q. et al. Molecular characterization of stable QTL and putative candidate genes for grain zinc and iron concentrations in two related wheat populations. Theor Appl Genet 136, 217 (2023). https://doi.org/10.1007/s00122-023-04467-y
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DOI: https://doi.org/10.1007/s00122-023-04467-y