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      Genome-wide association mapping in a diverse spring barley collection reveals the presence of QTL hotspots and candidate genes for root and shoot architecture traits at seedling stage

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          Abstract

          Background

          Adaptation to drought-prone environments requires robust root architecture. Genotypes with a more vigorous root system have the potential to better adapt to soils with limited moisture content. However, root architecture is complex at both, phenotypic and genetic level. Customized mapping panels in combination with efficient screenings methods can resolve the underlying genetic factors of root traits.

          Results

          A mapping panel of 233 spring barley genotypes was evaluated for root and shoot architecture traits under non-stress and osmotic stress. A genome-wide association study elucidated 65 involved genomic regions. Among them were 34 root-specific loci, eleven hotspots with associations to up to eight traits and twelve stress-specific loci. A list of candidate genes was established based on educated guess. Selected genes were tested for associated polymorphisms. By this, 14 genes were identified as promising candidates, ten remained suggestive and 15 were rejected. The data support the important role of flowering time genes, including HvPpd-H1, HvCry2, HvCO4 and HvPRR73. Moreover, seven root-related genes, HERK2, HvARF04, HvEXPB1, PIN5, PIN7, PME5 and WOX5 are confirmed as promising candidates. For the QTL with the highest allelic effect for root thickness and plant biomass a homologue of the Arabidopsis Trx-m3 was revealed as the most promising candidate.

          Conclusions

          This study provides a catalogue of hotspots for seedling growth, root and stress-specific genomic regions along with candidate genes for future potential incorporation in breeding attempts for enhanced yield potential, particularly in drought-prone environments. Root architecture is under polygenic control. The co-localization of well-known major genes for barley development and flowering time with QTL hotspots highlights their importance for seedling growth. Association analysis revealed the involvement of HvPpd-H1 in the development of the root system. The co-localization of root QTL with HERK2, HvARF04, HvEXPB1, PIN5, PIN7, PME5 and WOX5 represents a starting point to explore the roles of these genes in barley . Accordingly, the genes HvHOX2, HsfA2b, HvHAK2, and Dhn9, known to be involved in abiotic stress response, were located within stress-specific QTL regions and await future validation.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-019-1828-5) contains supplementary material, which is available to authorized users.

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          Most cited references126

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          Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions.

          The genetic improvement of drought resistance is essential for stable and adequate crop production in drought-prone areas. Here we demonstrate that alteration of root system architecture improves drought avoidance through the cloning and characterization of DEEPER ROOTING 1 (DRO1), a rice quantitative trait locus controlling root growth angle. DRO1 is negatively regulated by auxin and is involved in cell elongation in the root tip that causes asymmetric root growth and downward bending of the root in response to gravity. Higher expression of DRO1 increases the root growth angle, whereby roots grow in a more downward direction. Introducing DRO1 into a shallow-rooting rice cultivar by backcrossing enabled the resulting line to avoid drought by increasing deep rooting, which maintained high yield performance under drought conditions relative to the recipient cultivar. Our experiments suggest that control of root system architecture will contribute to drought avoidance in crops.
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              Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.

              Cytokinins are hormones that regulate cell division and development. As a result of a lack of specific mutants and biochemical tools, it has not been possible to study the consequences of cytokinin deficiency. Cytokinin-deficient plants are expected to yield information about processes in which cytokinins are limiting and that, therefore, they might regulate. We have engineered transgenic Arabidopsis plants that overexpress individually six different members of the cytokinin oxidase/dehydrogenase (AtCKX) gene family and have undertaken a detailed phenotypic analysis. Transgenic plants had increased cytokinin breakdown (30 to 45% of wild-type cytokinin content) and reduced expression of the cytokinin reporter gene ARR5:GUS (beta-glucuronidase). Cytokinin deficiency resulted in diminished activity of the vegetative and floral shoot apical meristems and leaf primordia, indicating an absolute requirement for the hormone. By contrast, cytokinins are negative regulators of root growth and lateral root formation. We show that the increased growth of the primary root is linked to an enhanced meristematic cell number, suggesting that cytokinins control the exit of cells from the root meristem. Different AtCKX-green fluorescent protein fusion proteins were localized to the vacuoles or the endoplasmic reticulum and possibly to the extracellular space, indicating that subcellular compartmentation plays an important role in cytokinin biology. Analyses of promoter:GUS fusion genes showed differential expression of AtCKX genes during plant development, the activity being confined predominantly to zones of active growth. Our results are consistent with the hypothesis that cytokinins have central, but opposite, regulatory functions in root and shoot meristems and indicate that a fine-tuned control of catabolism plays an important role in ensuring the proper regulation of cytokinin functions.
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                Author and article information

                Contributors
                abdelghani@MUTAH.EDU.JO
                Rajiv.Sharma@hutton.ac.uk
                wabila2003@yahoo.com
                sidram.dhanagond@gmail.com
                Owais@mutah.edu.jo
                mduwayri@yahoo.com
                sadam.dalaeen@bau.edu.jo
                christian.klukas@basf.com
                chendijun2012@gmail.com
                thomasl@iastate.edu
                vonwiren@ipk-gatersleben.de
                graner@ipk-gatersleben.de
                benjamin.kilian@croptrust.org
                neumannk@ipk-gatersleben.de
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                23 May 2019
                23 May 2019
                2019
                : 19
                : 216
                Affiliations
                [1 ]GRID grid.440897.6, Department of Plant Production, Faculty of Agriculture, , Mutah University, ; Mutah, Karak, 61710 Jordan
                [2 ]ISNI 0000 0001 0943 9907, GRID grid.418934.3, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), ; Corrensstrasse 3, 06466 Seeland, Germany
                [3 ]ISNI 0000 0004 0397 2876, GRID grid.8241.f, Division of Plant Science, , University of Dundee at JHI, Invergowrie, ; Dundee, DD2 5DA UK
                [4 ]ISNI 0000 0001 2174 4509, GRID grid.9670.8, Department of Horticulture and Agronomy, Faculty of Agriculture, , University of Jordan, ; Amman, Jordan
                [5 ]ISNI 0000 0004 0623 1491, GRID grid.443749.9, Al-Shoubak University College, , Al-Balqa’ Applied University, ; Al-, Salt, 19117 Jordan
                [6 ]ISNI 0000 0001 1551 0781, GRID grid.3319.8, Digitalization in Research & Development (ROM), , BASF SE, ; 67056 Ludwigshafen, Germany
                [7 ]ISNI 0000 0001 2248 7639, GRID grid.7468.d, Department for Plant Cell and Molecular Biology, , Institute for Biology, Humboldt University Berlin, ; 10115 Berlin, Germany
                [8 ]ISNI 0000 0004 1936 7312, GRID grid.34421.30, Department of Agronomy, , Agronomy Hall, Iowa State University, ; Ames, IA 50011 USA
                [9 ]ISNI 0000 0001 0679 2801, GRID grid.9018.0, Martin-Luther-University Halle-Wittenberg, ; Betty-Heimann-Str. 3, 06120 Halle/Saale, Germany
                [10 ]Global Crop Diversity Trust, Platz der Vereinten Nationen 7, 53113 Bonn, Germany
                Author information
                http://orcid.org/0000-0001-7451-7086
                Article
                1828
                10.1186/s12870-019-1828-5
                6533710
                31122195
                239ad57c-59ee-4ed1-ad44-738ebe5728a7
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 6 December 2018
                : 13 May 2019
                Funding
                Funded by: Deutsche Forschungsgemeinschaft (DFG)
                Award ID: KI 1465/8-1
                Award ID: KI 1465/9-1
                Award Recipient :
                Funded by: Deutscher Akademischer Austauschdienst (DAAD)
                Award ID: A/14/05106
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002347, Bundesministerium für Bildung und Forschung;
                Award ID: 0315969D
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Plant science & Botany
                barley,candidate genes,genome-wide association study,osmotic stress,root architecture

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