Genetic and physical mapping of anther extrusion in elite European winter wheat

RESEARCH ARTICLE Genetic and physical mapping of anther extrusion in elite European winter wheat Quddoos H. Muqaddasi1*, Klaus Pillen2, Jörg Plieske3, Martin W. Ganal3, Marion S. Röder1 1 Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Stadt Seeland OT Gatersleben, Germany, 2 Institute of Agricultural and Nutritional Sciences, Martin-Luther-University Halle-Wittenberg, Halle, Germany, 3 TraitGenetics GmbH, Stadt Seeland OT Gatersleben, Germany * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Muqaddasi QH, Pillen K, Plieske J, Ganal MW, Röder MS (2017) Genetic and physical mapping of anther extrusion in elite European winter wheat. PLoS ONE 12(11): e0187744. https://doi.org/10.1371/journal.pone.0187744 Editor: Harsh Raman, New South Wales Department of Primary Industries, AUSTRALIA Received: June 21, 2017 Accepted: October 25, 2017 Published: November 9, 2017 Copyright: © 2017 Muqaddasi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Abstract The production and cultivation of hybrid wheat is a possible strategy to close the yield gap in wheat. Efficient hybrid wheat seed production largely depends on high rates of cross-pollination which can be ensured through high anther extrusion (AE) by male parental lines. Here, we report the AE capacity and elucidate its genetics in 514 elite European winter wheat varieties via genome-wide association studies (GWAS). We observed a wide range of variation among genotypes and a high heritability (0.80) for AE. The whole panel was genotyped with the 35k Affymetrix and 90k iSELECT single nucleotide polymorphism (SNP) arrays plus Ppd-D1, Rht-B1 and Rht-D1 candidate markers. GWAS revealed 51 markertrait associations (MTAs) on chromosomes 1A, 1B, 2A, 4D and 5B, with Rht-D1 (4D) being the most significant marker. Division of whole panel according to the Rht-D1 genotype resulted in 212 and 294 varieties harboring Rht-D1a and Rht-D1b allele, respectively. The presence of Rht-D1a compared to Rht-D1b (mutant) allele had a large phenotypic influence on AE resulting in its ~17% increase. GWAS performed on the sub-panels detected novel MTAs on chromosomes 2D, 3B and 6A with increased phenotypic variance imparted by individual markers. Our study shows that AE is a highly quantitative trait and wild type Rht-D1a allele greatly improves AE. Moreover, demarcating the quantitative trait loci regions based on intra-chromosomal linkage disequilibrium revealed AE’s candidate genes/genomic regions. Understanding the genetics of AE in elite European wheat and utilizing the linked markers in breeding programs can help to enhance cross-pollination for better exploitation of heterosis. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: The genotyping data were generated in the project VALID funded by BMBF (project number 0315947). This research is supported by the program Grants4Traits from Bayer Crop Science (BCS). Both funders provided support in the form of contributions to salaries (BMBF for JP; BCS for QHM) and research materials, but did not have any additional role in study design, data collection and analysis, decision to publish, or Introduction Harnessing the advantages of heterosis has emerged as an important strategy for improving and stabilizing yield in many crops. Heterosis, a phenomenon where a hybrid offspring exhibits superior performance compared to the parents, has been in the focus of both plant breeders and geneticists [1]. While hybrid cultivars are widely used in out-crossing species such as maize, rapeseed and rye [2], heterotic advantages in wheat have so far not been optimally PLOS ONE | https://doi.org/10.1371/journal.pone.0187744 November 9, 2017 1 / 17 Anther extrusion for hybrid wheat breeding preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section. Competing interests: JP and MWG are employed by the company TraitGenetics GmbH. QHM was partially supported by the program Grants4Traits from Bayer Crop Science. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. This does not alter our adherence to PLOS ONE policies on sharing data and materials. realized. Much of this owes to the strict inbreeding nature of wheat. Wheat flowers having male and female organs in the same floret often does not open during flowering, forming the basis of self-pollination or cleistogamy in wheat. Industrial scale production of hybrid wheat seed demands a high level of pollen shedding outside the florets by male parents for efficient cross-fertilization of the female parents. Sufficient opening of florets at flowering time is therefore crucial to help anthers extrude, dehisce and shed pollen outside the floret. The subject of hybrid wheat breeding has a long history [3] with a modest success [4]. A special emphasis has been given to the importance of anther extrusion (AE) for generating pools of efficient pollinators [5–8] and a more recent surge in hybrid wheat breeding also highlights the importance of high AE by male parental lines to improve cross-pollination and subsequent seed set on female parents [4, 9–13]. AE, a phenomenon in which anthers at yellow stage come out of the florets at flowering time [14], therefore, is a major contributing trait for hybrid wheat seed production. To prevent self-pollination and to achieve male sterility in female parents, the most common system for industrial scale hybrid wheat production is the use of chemical hybridization agents (CHAs) [4]. The application of CHAs renders the stamens of the female parent unfertile (male sterile). Male sterile female parents are subsequently pollinated via cross-pollination from male parental lines. Recent positional cloning of a cleistogamous gene (cleistogamy 1) in barley showed that it inhibited the flower opening by reducing the size of the lodicules [15]. Cly1 encoded a transcription factor containing two AP2 domains and a putative microRNA (miR172) targeting site. Cleavage of mRNA directed by miR172 was detectable only in a non-cleistogamous background [15]. Orthologous genes to the barley cleistogamous gene Cly1 were detected in wheat in the subtelomeric regions of the long arms of the group 2 chromosomes [16]. These genes were designated as TaAP2-A, -B and–D, and had a high transcript abundance in the lodicules. Like the barley genes, the TaAP2 mRNAs were cleaved at their miR172 sites. However, resequencing of the TaAP2 genes showed a high degree of conservation for these genes even across different ploidy levels and no functional variants at the key miRNA172 target (...truncated)