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      The use of weighted multiple linear regression to estimate QTL × QTL × QTL interaction effects of winter wheat ( Triticum aestivum L.) doubled-haploid lines

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          Abstract

          Knowledge of the magnitude of gene effects and their interactions, their nature, and contribution to determining quantitative traits is very important in conducting an effective breeding program. In traditional breeding, information on the parameter related to additive gene effect and additive-additive interaction (epistasis) and higher-order additive interactions would be useful. Although commonly overlooked in studies, higher-order interactions have a significant impact on phenotypic traits. Failure to account for the effect of triplet interactions in quantitative genetics can significantly underestimate additive QTL effects. Understanding the genetic architecture of quantitative traits is a major challenge in the post-genomic era, especially for quantitative trait locus (QTL) effects, QTL–QTL interactions, and QTL–QTL–QTL interactions. This paper proposes using weighted multiple linear regression to estimate the effects of triple interaction (additive–additive–additive) quantitative trait loci (QTL–QTL–QTL). The material for the study consisted of 126 doubled haploid lines of winter wheat (Mandub × Begra cross). The lines were analyzed for 18 traits, including percentage of necrosis leaf area, percentage of leaf area covered by pycnidia, heading data, and height. The number of genes (the number of effective factors) was lower than the number of QTLs for nine traits, higher for four traits and equal for five traits. The number of triples for unweighted regression ranged from 0 to 9, while for weighted regression, it ranged from 0 to 13. The total aaa gu effect ranged from − 14.74 to 15.61, while aaa gw ranged from − 23.39 to 21.65. The number of detected threes using weighted regression was higher for two traits and lower for four traits. Forty-nine statistically significant threes of the additive-by-additive-by-additive interaction effects were observed. The QTL most frequently occurring in threes was 4407404 (9 times). The use of weighted regression improved (in absolute value) the assessment of QTL–QTL–QTL interaction effects compared to the assessment based on unweighted regression. The coefficients of determination for the weighted regression model were higher, ranging from 0.8 to 15.5%, than for the unweighted regression. Based on the results, it can be concluded that the QTL–QTL–QTL triple interaction had a significant effect on the expression of quantitative traits. The use of weighted multiple linear regression proved to be a useful statistical tool for estimating additive-additive-additive ( aaa) interaction effects. The weighted regression also provided results closer to phenotypic evaluations than estimator values obtained using unweighted regression, which is closer to the true values.

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          Most cited references64

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          Epistasis and quantitative traits: using model organisms to study gene-gene interactions.

          The role of epistasis in the genetic architecture of quantitative traits is controversial, despite the biological plausibility that nonlinear molecular interactions underpin the genotype-phenotype map. This controversy arises because most genetic variation for quantitative traits is additive. However, additive variance is consistent with pervasive epistasis. In this Review, I discuss experimental designs to detect the contribution of epistasis to quantitative trait phenotypes in model organisms. These studies indicate that epistasis is common, and that additivity can be an emergent property of underlying genetic interaction networks. Epistasis causes hidden quantitative genetic variation in natural populations and could be responsible for the small additive effects, missing heritability and the lack of replication that are typically observed for human complex traits.
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            The landscape of genetic complexity across 5,700 gene expression traits in yeast.

            Many studies have identified quantitative trait loci (QTLs) that contribute to continuous variation in heritable traits of interest. However, general principles regarding the distribution of QTL numbers, effect sizes, and combined effects of multiple QTLs remain to be elucidated. Here, we characterize complex genetics underlying inheritance of thousands of transcript levels in a cross between two strains of Saccharomyces cerevisiae. Most detected QTLs have weak effects, with a median variance explained of 27% for highly heritable transcripts. Despite the high statistical power of the study, no QTLs were detected for 40% of highly heritable transcripts, indicating extensive genetic complexity. Modeling of QTL detection showed that only 3% of highly heritable transcripts are consistent with single-locus inheritance, 17-18% are consistent with control by one or two loci, and half require more than five loci under additive models. Strikingly, analysis of parent and progeny trait distributions showed that a majority of transcripts exhibit transgressive segregation. Sixteen percent of highly heritable transcripts exhibit evidence of interacting loci. Our results will aid design of future QTL mapping studies and may shed light on the evolution of quantitative traits.
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              Principles for the buffering of genetic variation.

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                Author and article information

                Contributors
                jan.bocianowski@up.poznan.pl
                Journal
                J Appl Genet
                J Appl Genet
                Journal of Applied Genetics
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1234-1983
                2190-3883
                25 October 2023
                25 October 2023
                2023
                : 64
                : 4
                : 679-693
                Affiliations
                [1 ]Department of Mathematical and Statistical Methods, Poznań University of Life Sciences, ( https://ror.org/03tth1e03) Wojska Polskiego 28, 60-637 Poznań, Poland
                [2 ]Plant Breeding and Acclimatization Institute – National Research Institute, Department of Applied Biology, ( https://ror.org/05qgkbq61) Radzików 05-870 Błonie, Poland
                Author notes

                Communicated by Izabela Pawłowicz

                Author information
                http://orcid.org/0000-0002-9753-9277
                http://orcid.org/0000-0003-1067-6867
                http://orcid.org/0000-0003-2076-7586
                http://orcid.org/0000-0002-0102-0084
                Article
                795
                10.1007/s13353-023-00795-3
                10632291
                37878169
                fcfbc57a-6c59-43aa-bf5a-5a3e01d25572
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 31 July 2023
                : 25 September 2023
                : 4 October 2023
                Categories
                Plant Genetics • Original Paper
                Custom metadata
                © Institute of Plant Genetics Polish Academy of Sciences 2023

                Genetics
                three-way epistasis,weighted regression,doubled haploid lines,resistance,triticum aestivum

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