Abstract
Background
Biomass yield is an important trait for wheat breeding programs. Enhancing the yield of the aerial components of wheat cultivars will be an integral part of future wheat improvement. Aluminum (Al) toxicity is one of the main factors limiting wheat growth and production in acid soils, which occur on up to 50% of the arable lands of the world especially in tropical and subtropical regions.
Objective
Our objective was to identify quantitative trait loci (QTL) of plant growth characteristics and yield in wheat.
Methods
A recombinant inbred line (RIL) population consisting of 167 lines, derived from a cross between SeriM82 and Babax were evaluated under two Al treatments (+ Al, 800 µM of Al; −Al, 0 µM of Al) in the field based on an alpha lattice design with two replications for two consecutive crop seasons.
Results
A total of 40 QTLs including nine putative and 31 suggestive QTLs were found for all traits using the composite interval mapping (CIM) method. By mixed model-based composite interval mapping (MCIM) method, 42 additive QTLs and nine pairs of epistatic effects were detected for studied traits, of which 20 additive and six pairs of epistatic QTLs showed significant QTL × environment interactions. Most of the detected QTLs across environments were stable, and the highest number of stable QTLs was related to A genome. Co-localization of QTL was found on linkage groups (LGs) 2B, 4B, 6A-a, and 7A (CIM method) and 2A-d, and 6A-a (MCIM method).
Conclusion
These results have implications for selection strategies in biomass yield and for increasing the yield of the aerial part of wheat following further evaluations in various genetic backgrounds and environments.
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References
Acuna-Galindo MA, Mason RE, Subramanian NK, Hays DB (2015) Meta-analysis of wheat QTL regions associated with adaptation to drought and heat stress. Crop Sci 55(2):477–492. https://doi.org/10.2135/cropsci2013.11.0793
Assanga SO, Fuentealba M, Zhang G, Tan C, Dhakal S, Rudd JC et al (2017) Mapping of quantitative trait loci for grain yield and its components in a US popular winter wheat TAM 111 using 90K SNPs. PLoS One 12(12):e0189669. https://doi.org/10.1371/journal.pone.0189669
Bona L, Wright RJ, Baligar VC, Matuz J (1993) Screening wheat and other small grains for acid soil tolerance. Landsc Urban Plan 27(2–4):175–178. https://doi.org/10.1016/0169-2046(93)90046-G
Bhusal N, Sarial AK, Sharma P, Sareen S (2017) Mapping QTLs for grain yield components in wheat under heat stress. PLoS One 12(12):e0189594
Cai S, Bai GH, Zhang D (2008) Quantitative trait loci for aluminum resistance in Chinese wheat landrace FSW. Theor Appl Genet 117(1):49–56. https://doi.org/10.1007/s00122-008-0751-1
Caires EF, Garbuio FJ, Churka S, Barth G, Correa JCL (2008) Effects of soil acidity amelioration by surface liming on notill corn, soybean, and wheat root growth and yield. Eur J Agron 28(1):57–64. https://doi.org/10.1016/j.eja.2007.05.002
Dai J, Bai G, Zhang D, Hong D (2013) Validation of quantitative trait loci for aluminum tolerance in Chinese wheat landrace FSW. Euphytica 192(2):171–179. https://doi.org/10.1007/s10681-012-0807-9
Dargahi H, Tanya P, Somta P, Abe J, Srinives P (2014) Mapping quantitative trait loci for yield-related traits in soybean (Glycine max L.). Breed Sci 64(4):282–290. https://doi.org/10.1270/jsbbs.64.282
El-Feki WM, Byrne PF, Reid SD, Haley SD (2018) Mapping quantitative trait loci for agronomic traits in winter wheat under different soil moisture levels. Agron J 8:133. https://doi.org/10.3390/agronomy8080133
Farokhzadeh S, Fakheri BA, Mahdi Nezhad N, Tahmasebi S, Mirsoleimani A, Heidari B (2019) Mapping QTLs associated with grain yield and yield-related traits under aluminum stress in bread wheat. Crop Pasture Sci. https://doi.org/10.1139/gen-2016-0017
Foy CD (1988) Plant adaptation to acid, aluminum-toxic soils. Commun Soil Sci Plant Anal 19:959–987. https://doi.org/10.1080/00103628809367988
Froese PS, Carter AH (2016) Single nucleotide polymorphisms in the wheat genome associated with tolerance of acidic soils and aluminum toxicity. Crop Sci 56(4):1662–1677. https://doi.org/10.2135/cropsci2015.10.0629
Gabrielle B, Gagnaire N (2008) Life-cycle assessment of straw use in bio-ethanol production: A case study based on biophysical modelling. Biomass Bioenergy 32(5): 431–441. https://doi.org/10.1016/j.biombioe.2007.10.017
Garcia-Oliveira AL, Poschenrieder C, Barcelo J, Martins-Lopes P (2015) Breeding for Al tolerance by unravelling genetic diversity in bread wheat. Aluminum stress adaptation in plants. Springer International Publishing, Berlin, pp 125–153
Garcia-Oliveira AL, Benito C, Guedes-Pinto H, Martins-Lopes P (2018) Molecular cloning of TaMATE2 homoeologues potentially related to aluminium tolerance in bread wheat (Triticum aestivum L.). Plant Biol 20(5):817–824. https://doi.org/10.1111/plb.12864
Golabadi M, Arzani A, Mirmohammadi Maibody SAM, Tabatabaei BES, Mohammadi SA (2011) Identification of micro satellite markers linked with yield components under drought stress at terminal growth stages in durum wheat. Euphytica 177(2):207–221. https://doi.org/10.1007/s10681-010-0242-8
Gonzalez A, Martin I, Ayerbe L (2007) Response of barley genotypes to terminal soil moisture stress: phenology, growth, and yield. Aust J Agric Res 58(1):29–37. https://doi.org/10.1071/AR06026
Goulding KWT (2016) Soil acIDification and the importance of liming agricultural soils with particular reference to the United Kingdom. Soil Use Manag 32(3):390–399. https://doi.org/10.1111/sum.12270
Huang X, Kempf H, Ganal MW, Roder MS (2004) Advanced backcross QTL analysis in progenies derived from a cross between a German elite winter wheat variety and a synthetic wheat (Triticum aestivum L.). Theor Appl Genet 109(5):933–943. https://doi.org/10.1007/s00122-004-1708-7
Jaiswal SK, Naamala J, Dakora FD (2018) Nature and mechanisms of aluminium toxicity, tolerance and amelioration in symbiotic legumes and rhizobia. Biol Fert Soils 54(3):309–318. https://doi.org/10.1007/s00374-018-1262-0
Jaskowiak J, Tkaczyk O, Slota M, Kwasniewska J, Szarejko I (2018) Analysis of aluminum toxicity in Hordeum vulgare roots with an emphasis on DNA integrity and cell cycle. PLoS One 13(2):e0193156. https://doi.org/10.1371/journal.pone.0193156
Kirigwi FM, Ginkel M, Brown-Guedira G, Gill BS, Paulsen GM, Fritz AK (2007) Markers associated with a QTL for grain yield in wheat under drought. Mol Breed 20(4):401–413. https://doi.org/10.1007/s11032-007-9100-3
Kumar N, Kulwal PL, Balyan HS, Gupta PK (2007) QTL mapping for yield and yield contributing traits in two mapping populations of bread wheat. Mol Breed 19(2):163–177. https://doi.org/10.1016/S1875-2780(11)60041-2
Lal R (2005) World crop residues production and implications of its use as a biofuel. Environ Int 31(4):575–584. https://doi.org/10.1016/j.envint.2004.09.005
Li ZK, Jiang XL, Peng T, Shi CL, Han SX, Tian B et al (2014) Mapping quantitative trait loci with additive effects and additive × additive epistatic interactions for biomass yield, grain yield, and straw yield using a doubled haploid population of wheat (Triticum aestivum L.). Genet Mol Res 13(1):1412–1424. https://doi.org/10.4238/2014.February.28.14
Ling H-Q, Zhao S, Liu D, Wang J, Sun H, Zhang C et al (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496(7443):87–90. https://doi.org/10.1038/nature11997
Lopes MS, Reynolds MP, McIntyre CL, Mathews KL, Kamali MRJ, Mossad M et al (2013) QTL for yield and associated traits in the SeriM82/Babax population grown across several environments in Mexico, in the West Asia, North Africa, and South Asia regions. Theor Appl Genet 126(4):971–984. https://doi.org/10.1007/s00122-012-2030-4
Ma HX, Bai GH, Lu WZ (2006) Quantitative trait loci for aluminum resistance in wheat cultivar Chinese Spring. Plant Soil 283(1–2):239–249. https://doi.org/10.1007/s11104-006-0008-1
Marza F, Bai GH, Carver BF, Zhou WC (2006) Quantitative trait loci for yield and related traits in the wheat population Ning7840 × Clark. Theor Appl Genet 112(4):688–698. https://doi.org/10.1007/s00122-005-0172-3
Mason RE, Mondal S, Beecher FW, Pacheco A, Jampala B, Ibrahah AMH et al (2010) QTL associated with heat susceptibility index in wheat (Triticum aestivum L.) under short-term reproductive stage heat stress. Euphytica 174(3):423–436. https://doi.org/10.1007/s10681-010-0151-x
Masoudi B, Mardi M, Hervan EM, Bihamta MR, Naghavi MR, Nakhoda B, Amini A (2015) QTL mapping of salt tolerance traits with different effects at the seedling stage of bread wheat. Plant Mol Bio Reporter 33(6):1790–1803. https://doi.org/10.1007/s11105-015-0874-x
Mathews KL, Malosetti M, Chapman S, McIntyre L, Reynolds M, Shorter R, van Eeuwijk F (2008) Multi-environment QTL mixed models for drought stress adaptation in wheat. Theor Appl Genet 117(7):1077–1091. https://doi.org/10.1007/s00122-008-0846-8
McIntosh RA, Devos KM, Dubcovsky J, Morris CF, Rogers WJ (2003) Catalogue of gene symbols for wheat (Online). http://wheat.pw.usda.gov/ggpages/wgc/2003/GeneSymbol.html
McIntyre CL, Mathews KL, Rattey A, Drenth J, Ghaderi M, Reynolds M et al (2010) Molecular detection of genomic regions associated with grain yield and yield-related components in an elite bread wheat cross evaluated under irrigated and rainfed conditions. Theor Appl Genet 120(3):527–541. https://doi.org/10.1007/s00122-009-1173-4
Monpara BA (2011) Grain filling period as a measure of yield improvement in bread wheat. Crop Improv 38(1):1–5
Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253(1):201–218. https://doi.org/10.1023/A:1024553303144
Navakode S, Weidner A, Lohwasser U, Roder MS, Borner A (2009) Molecular mapping of quantitative trait loci (QTLs) controlling aluminium tolerance in bread wheat. Euphytica 166(2):283–290. https://doi.org/10.1007/s10681-008-9845-8
Navakode S, Neumann K, Kobiljski B, Lohwasser U, Borner A (2014) Genome wide association mapping to identify aluminium tolerance loci in bread wheat. Euphytica 198(3):401–411. https://doi.org/10.1007/s10681-014-1114-4
Olivares-Villegas JJ, Reynolds MP, McDonald GK (2007) Drought-adaptive attributes in the Seri/Babax hexaploid wheat population. Funct Plant Biol 34(3):189–203. https://doi.org/10.1071/FP06148
Paliwal R, Roder MS, Kumar U, Srivastava JP, Joshi AK (2012) QTL mapping of terminal heat tolerance in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 125(3):561–575. https://doi.org/10.1007/s00122-012-1853-3
Payne R, Welham S, Harding S (2012) A guide to REML in GenStat. 15th International VSN, Hempstead H (eds), U.K. Available at: http://www.vsni.co.uk/software/genstat
Peleg ZVI, Fahima T, Krugman T, Abbo S, Yakir DAN, Korol AB, Saranga Y (2009) Genomic dissection of drought resistance in durum wheat × wild emmer wheat recombinant in breed line population. Plant Cell Environ 32(7):758–779. https://doi.org/10.1111/j.1365-3040.2009.01956.x
Pereira JF (2018) Initial root length in wheat is highly correlated with acid soil tolerance in the field. Sci Agric 75:79–83. https://doi.org/10.1590/1678-992X-2016-0422
Pinto RS, Reynolds MP, Mathews KL, McIntyre CL, Olivares-Villegas JJ, Chapman SC (2010) Heat and drought adaptive QTL in a wheat population designed to minimize confounding agronomic effects. Theor Appl Genet 121(6):1001–1021. https://doi.org/10.1007/s00122-010-1351-4
Polle E, Konzak CF (1985) A single scale for determining Al tolerance levels in cereals. Agron Abstr, 67
Pushpendra KG, Harindra SB, Pawan LK, Neeraj K, Ajay K, Reyazul RM, Amita M, Jitendra K (2007) QTL analysis for some quantitative traits in bread wheat. J Zhejiang Univ Sci B 8(11):807–814. https://doi.org/10.1631/jzus.2007.B0807
Quarrie SA, Steed A, Calestani C, Semikhodskii A et al (2005) A high-density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring × SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110(5):865–880. https://doi.org/10.1007/s00122-004-1902-7
Rahman MA, Lee SH, Ji HC, Kabir AH, Jones CS, Lee KW (2018) Importance of mineral nutrition for mitigating aluminum toxicity in plants on acidic soils: Current Status and Opportunities. Int J Mol Sci 19:3073. https://doi.org/10.3390/ijms19103073
Raman H, Ryan PR, Raman R, Stodart BJ, Zhang K et al (2008) Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). Theor Appl Genet 116(3):343–354. https://doi.org/10.1007/s00122-007-0672-4
Raman H, Stodart B, Ryan PR, Delhaize E, Emebiri L, Raman R, Coombes N, Milgate A (2010) Genome-wide association analyses of common wheat (Triticum aestivum L.) germplasm identifies multiple loci for aluminium resistance. Genome 53(11):957–966. https://doi.org/10.1139/G10-058
Rattey A, Shorter R, Chapman S, Dreccer F, van Herwaarden A (2009) Variation for and relationships among biomass and grain yield component traits conferring improved yield and grain weight in an elite wheat population grown in variable yield environments. Crop Pasture Sci 60(8):717–729. https://doi.org/10.1071/CP08460
Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149:340–351. https://doi.org/10.1104/pp.108.129155
Ryan PR, Dong D, Teuber F, Wendler N, Muhling KH, Liu J, Xu M, Salvador Moreno N, You J, Maurer H-P, Horst WJ, Delhaize E (2018) Assessing how the aluminum-resistance traits in wheat and rye transfer to hexaploid and octoploid triticale. Front Plant Sci 9:1334. https://doi.org/10.3389/fpls.2018.01334
Song QJ, Marek LF, Shoemaker RC, Lark KG et al (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109(1):122–128. https://doi.org/10.1007/s00122-004-1602-3
Shannon MC (1997) Adaptation of plants to salinity. Adv Agron 60:75–120. https://doi.org/10.1016/S0065-2113(08)60601-X
Sharma AD, Sharma H, Lightfoot DA (2011) The genetic control of tolerance to aluminum toxicity in the ‘Essex’ by ‘Forrest’ recombinant inbred line population. Theor Appl Genet 122(4):687–694. https://doi.org/10.1007/s00122-010-1478-3
Sharma RC (1992) Duration of the vegetative and reproductive period in relation to yield performance of spring wheat. Eur J Agron 1(3):133–137. https://doi.org/10.1016/S1161-0301(14)80062-2
Shi Sh, Azam FI, Li H, Chang X, Li B (2017) Mapping QTL for stay-green and agronomic traits in wheat under diverse water regimes. Euphytica 213:246
Smith A, Cullis B, Thompson R (2001) Analyzing variety by environment data using multiplicative mixed models and adjustments for spatial field trend. Biometrics 57(4):1138–1147. https://doi.org/10.1111/j.0006-341X.2001.01138.x
Sohrabi Chah Hassan F, Solouki M, Fakheri BA, Mahdi Nezhad N, Masoudi B (2018) Mapping QTLs for physiological and biochemical traits related to grain yield under control and terminal heat stress conditions in bread wheat (Triticum aestivum L.). Physiol Mol Biol Plants 24(6):1231–1243. https://doi.org/10.1007/s12298-018-0590-8
Tahmasebi S, Heidari B, Pakniyat H, McIntyre CL (2016) Mapping QTLs associated with agronomic and physiological traits under terminal drought and heat stress conditions in wheat (Triticum aestivum L.). Genome 60(1):26–45. https://doi.org/10.1139/gen-2016-0017
Tang C, Rengel Z, Diatloff E, Gazey C (2003) Responses of wheat and barley to liming on a sandy soil with subsoil acidity. Field Crops Res 80(3):235–244. https://doi.org/10.1016/S0378-4290(02)00192-2
Tao Y, Niu Y, Wang Y, Chen T, Naveed SA, Zhang J et al (2018) Genome-wIDe association mapping of aluminum toxicity tolerance and fine mapping of a candIDate gene for Nrat1 in rice. PLoS One 13(6):e0198589. https://doi.org/10.1371/journal.pone.0198589
Tiwari C, Walwork H, Kumar U, Dhari R, Arun B, Mishra VK et al (2013) Molecular mapping of high-temperature tolerance in bread wheat adapted to the Eastern Gangetic Plain region of India. Field Crops Res 154:201–210. https://doi.org/10.1016/j.fcr.2013.08.004
Tovkach A, Ryan PR, Richardson AE, Lewis DC, Rathjen TM, Ramesh S, Tyerman SD, Delhaize E (2013) Transposon-mediated alteration of TaMATE1B expression in wheat confers constitutive citrate efflux from root apices. Plant Physiol 161(2):880–892
Valle SR, Carrasco J, Pinochet D, Calderini DF (2009) Grain yield, above-ground and root biomass of Al-tolerant and Al-sensitive wheat cultivars under different soil aluminum concentrations at field conditions. Plant Soil 318(1–2):299–310. https://doi.org/10.1007/s11104-008-9841-8
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78. https://doi.org/10.1093/jhered/93.1.77
Wang S, Basten CJ, Zeng ZB (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, N.C. Available from http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
Wang S, Zhang X, Chen F, Cui D (2015) A single-nucleotide polymorphism of TaGS5 gene revealed its association with kernel weight in Chinese bread wheat. Front Plant Sci 6:1166. https://doi.org/10.3389/fpls.2015.01166
Wu QH, Chen YX, Zhou SH, Fu L, Chen JJ et al (2015) High density genetic linkage map construction and QTL mapping of grain shape and size in the wheat population Yanda1817 × Beinong6. PLoS One 10(2):e0118144. https://doi.org/10.1371/journal.pone.0118144
Xu Y, Li S, Li L, Zhang X, Xu H, An D (2013) Mapping QTLs for salt tolerance with additive, epistatic and QTL × treatment interaction effects at seedling stage in wheat. Plant Breed.https://doi.org/10.1111/pbr.12048
Yang J, Hu CC, Hu H, Yu RD, Xia Z, Ye XZ, Zhu J (2008) QTL Network: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24(5):721–723. https://doi.org/10.1093/bioinformatics/btm494
Yang D, Liu Y, Cheng H, Chang L, Chen J, Chai S, Li M (2016) Genetic dissection of flag leaf morphology in wheat (Triticum aestivum L.) under diverse water regimes. BMC Genet 17(1):94. https://doi.org/10.1186/s12863-016-0399-9
Zhai H, Feng Z, Li J, Liu X, Xiao S, Ni Z, Sun Q (2016) QTL analysis of spike morphological traits and plant height in winter wheat (Triticum aestivum L.) using a high-density SNP and SSR-based linkage map. Front Plant Sci 7:1617. https://doi.org/10.3389/fpls.2016.01617
Zhang J, Chen J, Chu C, Zhao W, Wheeler J, Souza EJ, Zemetra RS (2014) Genetic dissection of QTL associated with grain yield in diverse environments. AGRON J 4:556–578. https://doi.org/10.3390/agronomy4040556
Acknowledgements
The authors are grateful to Darab Agriculture and Natural Resources Research and Education Center for providing the seeds of the SB population and the support in field trials and also Faculty of Agriculture and Natural Resources of Darab to provide laboratory facilities.
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B.A.F, S.T, N.M.N and A.M designed the research and edited the manuscript. Thanks to S.T for the help in statistical analysis. Thanks to C.L.M for providing the marker data of SeriM82/Babax population and offering constructive suggestions to improve the manuscript. S.F. performed the experiments, analyzed the data, and wrote the primary draft of the manuscript.
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Farokhzadeh, S., Fakheri, B.A., Nezhad, N.M. et al. Genetic control of some plant growth characteristics of bread wheat (Triticum aestivum L.) under aluminum stress. Genes Genom 42, 245–261 (2020). https://doi.org/10.1007/s13258-019-00895-7
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DOI: https://doi.org/10.1007/s13258-019-00895-7