Genetic analysis and molecular mapping of a stripe rust resistance gene in wheat–Leymus mollis translocation line M8926-2

Highlights

• M8926-2 is highly resistant to the prevalent Chinese Puccinia striiformis f. sp. tritici (Pst) races.

• A single dominant gene YrM8926 confers all-stage resistance to CYR32 in M8926-2.

• YrM8926 was located on wheat chromosome 2DS by seven simple sequence repeat (SSR) markers.

Abstract

Stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is one of the most widespread and destructive diseases of wheat crop worldwide. Growing resistant cultivars is the preferred method of controlling diseases, but only a few effective genes are available. M8926-2, a translocation line developed from interspecific hybridization between Leymus mollis and a common wheat genotype 7182, is highly resistant to the prevalent Chinese Pst races. In order to identify gene(s) for stripe rust resistance, M8926-2 was crossed with susceptible genotype Mingxian 169, and seedlings of parents and F₁, F₂, and F_2:3 progenies were tested with the most prevalent Pst race CYR32 under controlled greenhouse conditions. M8926-2 has a single dominant gene, designated as YrM8926, conferring all-stage resistance to CYR32. Genetic mapping was used to identify molecular markers linked to YrM8926. A linkage group of seven simple sequence repeat (SSR) markers was constructed for YrM8926 using 191 F_2-2 population plants and the gene was located on wheat chromosome 2DS. The wheat-L. mollis translocation line background of M8926-2 and disease assessments indicated that YrM8926 is originally derived from L. mollis. The stripe rust resistance gene and closely linked molecular markers should be useful for pyramiding with other genes to develop wheat cultivars with high-level and long-term resistance to stripe rust.

Introduction

Stripe rust (or yellow rust), caused by Puccinia striiformis Westend. f. sp. tritici Erikss. (Pst), is one of the most devastating diseases of wheat worldwide (Chen, 2005, Wan et al., 2004). It leads to significant economic losses because of reduced production and/or high costs for chemical control (Wellings, 2007). In China, particularly in the northwestern and southwestern regions, stripe rust has caused significant economic losses over the last 60 years (Li and Zeng, 2002, Wan et al., 2007). Survey data from the last 10 years shows that the average annual area affected by stripe rust is approximately 4 million hectares. They also showed that stripe rust affected 6.6, 4.9, and 4.1 million hectares in 2002, 2003, and 2009, respectively (Kang et al., 2010).

Breeding for and growing resistant cultivars is the most effective and economical approach toward controlling the disease, and pyramiding of effective resistance genes has provided long-term control (Chen, 2005, Wellings, 2007). To date, >70 stripe rust resistance genes with official Yr designations have been reported in wheat, and many other genes and quantitative trait loci (QTL) have been temporarily named (Cheng et al., 2014, McIntosh et al., 2013). Most of these genes have race-specific resistance, and are usually short-lived because of rapid virulence changes in pathogen populations. For example, stripe rust resistance gene Yr9 from rye has been widely used in wheat-breeding programs in China since the early 1970s (He et al., 2001), with more than 80% of the released cultivars containing Yr9 by the late 1980s (Wan et al., 2004, Wan et al., 2007). Pst race CYR29 with virulence to Yr9, detected in 1985, overcame resistance in most wheat cultivars carrying Yr9, resulting in the nationwide stripe rust epidemic that caused a yield loss of 1.8 million metric tons in 1990 (Wan et al., 2004). A similar situation occurred for stripe rust resistance in Fan 6 with resistance from Hybrid 46 (Yr4b, YrH46) (Wan et al., 2004). Wheat cultivars derived from Fan 6 were widely grown on 1.5–2.0 million hectares annually in southwestern China. Fan 6 and its derivatives have been highly resistant to stripe rust for 20 years (Niu and Wu, 1997), but became susceptible to the new Pst races CYR31 and CYR32, leading to another nationwide stripe rust epidemic that caused 1.3 million metric tons of yield loss in 2002 (Wan et al., 2004). In recent years, Yr26 (= Yr24) has been widely used in wheat-breeding programs in China for developing stripe rust-resistant cultivars (Han et al., 2010), and Yr26/Yr24 varieties have been grown on >3.4 million hectares in China. However, a new Pst race V26 with virulence to Yr26/Yr24 and Yr10 was detected in China in 2009 (Liu et al., 2010), whose frequency increased from 4.3% in 2011 to 14.5% in 2013 (National Wheat Rust Research Group, unpublished data). To date, few Yr genes have been shown to be effective against all current Chinese and world populations of Pst, with the notable exceptions of Yr5 and Yr15 (Sharma-Poudyal et al., 2013). As such, there is an urgent need to identify new stripe rust resistance genes in order to diversify and pyramid genes to achieve effective and long-term resistance for sustainable control of stripe rust.

Most stripe rust resistance genes are derived from common wheat (Triticum aestivum) and one replacement of highly diverse landraces by high-yielding, pure-line varieties in many parts of the world has narrowed the genetic basis for disease resistance in the wheat gene pool (Kuraparthy et al., 2007). Fortunately, in addition to common wheat, wild relatives of wheat have gained importance as sources for stripe rust resistance in wheat breeding. Among the officially designated Yr genes, Yr5, Yr8, Yr9, Yr15, Yr17, Yr19, Yr28, Yr35, Yr36, Yr37, Yr38, Yr40, Yr42, Yr49, Yr53, Yr64, and Yr65 have been identified from wild relatives of common wheat (Cheng et al., 2014, McIntosh et al., 2008, Xu et al., 2013). Among them, Yr5 and Yr15 are still resistant to the most prevalent Chinese Pst races, CYR32 and CYR33.

Leymus mollis (Trin.) Hara., a perennial allotetraploid (2n = 4x = 28) belonging to Hordinae, Poaceae, exhibits superior agronomic characteristics such as strong stems, large spikes, multiple spikelets, tolerance of abiotic stresses (e.g., drought, cold, salts, and infertile soils), and resistance to fungal and bacterial diseases. Thus, it serves as a valuable wild relative of wheat (Kishii et al., 2003). Hybridizations between wheat and L. mollis have been conducted successfully in several countries, including Russia, Iceland, Sweden, and China, and many wheat–L. mollis hexaploid or octoploid derivatives have been produced (Zhao et al., 2013). However, few reports are available on wheat–L. mollis translocation lines resistant to wheat stripe rust. Guo et al. (2002) reported that L. mollis confers stripe rust resistance gene(s) that can be transmitted via a Triticum–Leymus hybrid. Using a simple sequence repeat (SSR) and expressed sequence tags (EST) marker, Bao et al. (2012) mapped a stripe rust resistance gene YrSh0096 on wheat chromosome 4AL in the wheat line Shannong 0096 derived from a wheat–L. mollis octoploid and bread wheat cultivar Yannong15.

M8926-2, a wheat–L. mollis translocation line (2n = 42) derived from a cross between L. mollis line and common wheat line 7182 (Jing et al., 2001, Wang et al., 2004), exhibits high resistance to the prevalent Chinese Pst races in both the seedling and adult-plant stages. Therefore, the objectives of this study were to characterize and map the stripe rust resistance gene(s) in wheat–L. mollis translocation line M8926-2, and to identify closely linked markers for resistance breeding.