Theoretical and Applied Genetics https://doi.org/10.1007/s00122-020-03602-3 ORIGINAL ARTICLE Identifcation of two novel Hessian fy resistance genes H35 and H36 in a hard winter wheat line SD06165 Lanfei Zhao1,2 · Nader Ragab Abdelsalam2,3 · Yunfeng Xu2 · Ming‑Shun Chen4 · Yi Feng2,5 · Lingrang Kong1 · Guihua Bai4,2 Received: 31 January 2020 / Accepted: 1 May 2020 © This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2020 Abstract Key message Two new Hessian fy resistance QTLs (H35 and H36) and tightly linked SNP markers were identifed in a US hard winter wheat SD06165. Abstract Hessian fy (HF), Mayetiola destructor (Say), is one of the most destructive pests in wheat (Triticum aestivum L.) worldwide. Growing resistant cultivars is the most efective approach to minimize Hessian fy damage. To identify new quantitative trait loci (QTLs) for HF resistance, a recombinant inbred line population was developed by crossing HF resistant wheat line SD06165 to a susceptible line OK05312. The population was genotyped with 1709 single-nucleotide polymorphisms (SNPs) generated from genotyping-by-sequencing and phenotyped for HF resistance in greenhouses. Two novel QTLs for HF resistance were identifed from SD06165. The major QTL, designated as H35, was closely linked to SNP marker SDOKSNP7679 on chromosome 3BS that explained 23.8% and 36.0% of the phenotypic variations; the minor QTL, designated as H36, was fanked by SNP markers SDOKSNP1618 and SDOKSNP8089 on chromosome 7AS and explained 8.5% and 13.1% of the phenotypic variation in the two experiments. Signifcant interaction was detected between the two QTLs. Seventeen SNPs that tightly link to H35 and eight SNPs that tightly link to H36 were converted to kompetitive allele specifc polymerase chain reaction markers for selecting these QTLs in breeding programs. Introduction Hessian fy (HF), Mayetiola destructor (Say), is a destructive Communicated by Aimin Zhang. pest of wheat (Triticumestivum) worldwide. HF originated from the Fertile Crescent in West Asia along with wheat, its Electronic supplementary material The online version of this primary host (Harris et al. 2003). HF can be transported with article (https ://doi.org/10.1007/s0012 2-020-03602 -3) contains supplementary material, which is available to authorized users. wheat across regions (Barnes 1956; Fitch 1846). Today, HF can be found in North Africa, South Europe, North America, * Guihua Bai Southwest Asia and other wheat growing regions worldwide [email protected] (Ando et al. 2018; Berzonsky et al. 2003; El Bouhssini et al. 1 State Key Laboratory of Crop Biology, Shandong Key 2013). In the USA, HF was the frst invasive insect to cause Laboratory of Crop Biology, College of Agronomy, economic havoc, especially in the Great Plains and southeast Shandong Agriculture University, Taian 271018, Shandong, region of the USA. (Hao et al. 2013; Morton et al. 2011; China Pauly 2002). HF can cause signifcant reduction in spike 2 Department of Agronomy, Kansas State University, 2004 number per plant, grain number and weight, eventually grain Throckmorton Hall, Manhattan, KS 66506, USA yield of wheat (Smiley et al. 2004; Schwarting et al. 2016). 3 Agricultural Botany Department, Faculty of Agriculture, Hessian fy is a member in the Cecidomyiidae family Saba Basha, Alexandria University, Alexandria 21531, Egypt (Mamaev 1975; Gagné 1994) and is sexually reproduced 4 Hard Winter Wheat Genetics Research Unit, USDA, 4008 with a short life cycle of 30 days. A female insect can lay Throckmorton Hall, Manhattan, KS 66506, USA 100–400 eggs on the adaxial surfaces of wheat tender leaves 5 College of Agronomy, Northwest A&F University, in a short time (approximately 3 h). Eggs will hatch within Yangling 712100, China Vol.:(0123456789)1 3 Theoretical and Applied Genetics 3–4 days at 20 °C. Newly hatched larvae migrate along the chromosome 2B (Amri et al. 1990), H31 on the terminus leaf-blade, enter wheat stem via the whorl, and continue to of chromosome arm 5BS (Williams et al. 2003), H34 and move to the base of the nearest node where their feeding QHara.icd-6B on chromosome 6B (Bassi et al. 2019; Li causes abnormal sheath and leaf growth, stunt plant, and et al. 2013). eventual seedling death (Anderson and Harris 2006). A sin- To date, 16 biotypes of HF have been reported, includ- gle wheat seedling can have up to 50 larvae, and infestation ing biotypes A to O and GP (the Great Plains biotype) in wheat can cause signifcant reduction in wheat grain yield based on their responses to the wheat resistant cultivars (Smiley et al. 2004; Schwarting et al. 2016). carrying genes H3, H5, H6 and a combination of H7H8 Currently, the most efective approach to HF control is (Gallun 1977; Ratclife and Hatchett 1997). The biotype integrated pest management (IPM) that mainly consists of GP is still the prevalent biotype of HF in the US Great cultural, chemical, biological and genetic controls (Buntin Plains, although it is the least virulent biotype among et al. 1992). The genetic control to use host-plant resistance these biotypes reported in the USA. (Chen et al. 2009; to the insect is the most important foundation of a successful Garcés-Carrera et al. 2014; Sardesai et al. 2005). IPM strategy. Growing resistant wheat cultivars is widely The relationship between wheat and HF fts a classical accepted as the most efective and environmentally friendly gene-for-gene genetic model, so deploying a single resist- approach to reduce HF damage worldwide (Berzonsky et al. ance gene in wheat cultivar may quickly lose its efective- 2003). ness due to the selection pressure that leads HF to adapt Wheat resistance to HF was frst reported in 1785 (Painter to the corresponding resistance gene (Foster et al. 1991; 1951). To date, a total of 35 HF resistance genes (H1-H34 Ratclife et al. 1994, 1996). Therefore, improving the and Hdic) from wheat and its wild relatives have been of- durability of HF resistance is an ultimate goal of wheat cially named (Bassi et al. 2019; Hao et al. 2013; Li et al. breeding programs worldwide. One approach is to pyramid 2013). All the HF resistance genes are dominant or partially multiple resistance genes in wheat cultivars to extend the dominant except that h4 was reported as a recessive gene duration of resistance; another way is to search for novel (Bassi et al. 2019). Among these resistance genes, nine were resistance genes to be used in wheat breeding programs. identifed from common wheat including H1, H2, H3, h4, Molecular markers closely linked to these resistance genes H5, H7, H8, H12 and H34; six were from Aegilops tauschii are essential for gene pyramiding. In addition, previously including H13, H22, H23, H24, H26 and H32; 15 were some genes have been localized to chromosomes using from durum wheat including H6, H9, H10, H11, H14, H15, monosomic analysis, which is difcult to locate a gene H16, H17, H18, H19, H20, H28, H29, H31 and H33; two to a short chromosome interval, sometimes results in an (H21 and H25) were from rye (Secale cereale); and three incorrect chromosomal location (Gallun and Patterson were from Ae. ventricosa (H27), Ae. triuncialis (H30) and 1977). Due to limited markers available and lack of refer- a cultivated primitive emmer wheat (Triticum turgidum ssp. ence genome sequence in early studies, some genes were dicoccum) (Hdic) (Bassi et al. 2019; Kong et al. 2005, 2008; mapped incorrectly to chromosomes even using DNA McIntosh et al. 1973; Sardesai et al. 2005). More recently, markers. For example, H26 was previously localized on two new major QTLs for HF resistance were identifed by chromosome 4D, but later it was remapped to chromosome association mapping, including QH.icd-2A transferred from 3D using a high-density map (Wang et al. 2006). Using a T. dicoccum and QHara.icd-6B transferred from T. ararati- high-density single-nucleotide polymorphism (SNP) map, cum (Bassi et al. 2019). H34 was identifed on chromosome 6B (Li et al. 2013) Many of these resistance genes have been mapped to and another HF resistance gene was mapped on the short various wheat chromosomes. Gallun and Patterson (1977) arm of chromosome 1A (Li et al. 2015). More recently, was the frst to locate H6 on chromosome 5A using mono- H7 and H8 have been reassigned to chromosomes 6A and somic analysis (Gallun and Patterson 1977). Later, Steb- 2B, respectively, using a SNP map (Liu et al. 2020). Fur- bins et al. (Stebbins et al. 1982) found that H6 closely thermore, those SNPs closely linked to a gene can be con- linked to H3, H9 and H10. Using molecular markers, H3, verted into kompetitive allele specifc PCR (KASP) assays H5, H6, H9, H10, H11, H12, H14, H15, H16, H17, H19, for marker-assisted selection (MAS) in wheat breeding H28, H29 and Hdic were further mapped to a HF resist- programs (Tan et al. 2017). ance gene cluster in the distal gene-rich region of short ‘SD06165’ is a hard-red winter (HRW) wheat line arm of wheat chromosome 1A (Kong et al. 2005, 2008; from South Dakota that showed stable resistance to Hes- Liu et al. 2005). H13, H22, H23, H24, H26 and H32 from sian fy biotype GP. In this study, a RIL population from Aegilops tauschii were located on the wheat chromosomes SD06165 × OK05312 was genotyped using SNP markers 1D, 3D, 4D and 6D (Cox and Hatchett 1994; Gill et al. generated by genotyping-by-sequencing (GBS) and phe- 1987; Raupp et al. 1993; Sardesai et al. 2005). Only four notyped for HF resistance in greenhouse experiments to genes were mapped in the B genome of wheat with H20 on identify HF resistance QTL in SD06165.