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Review

Advances in the Mining of Disease Resistance Genes from Aegilops tauschii and the Utilization in Wheat

by
Hongyun Kou
1,
Zhenbo Zhang
1,
Yu Yang
2,
Changfeng Wei
2,
Lili Xu
2 and
Guangqiang Zhang
1,2,3,*
1
State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an 271018, China
2
College of Agriculture and Bioengineering, Heze University, Heze 274015, China
3
Shandong Shofine Seed Technology Co., Ltd., Jining 272400, China
*
Author to whom correspondence should be addressed.
Plants 2023, 12(4), 880; https://doi.org/10.3390/plants12040880
Submission received: 17 October 2022 / Revised: 1 December 2022 / Accepted: 7 December 2022 / Published: 15 February 2023
(This article belongs to the Special Issue Genetic and Genomic Resources for Wheat Improvement)
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Abstract

:
Aegilops tauschii is one of the malignant weeds that affect wheat production and is also the wild species ancestor of the D genome of hexaploid wheat (Triticum aestivum, AABBDD). It contains many disease resistance genes that have been lost in the long-term evolution of wheat and is an important genetic resource for the mining and utilization of wheat disease resistance genes. In recent years, the genome sequence of Aegilops tauschii has been preliminarily completed, which has laid a good foundation for the further exploration of wheat disease resistance genes in Aegilops tauschii. There are many studies on disease resistance genes in Aegilops tauschii; in order to provide better help for the disease resistance breeding of wheat, this paper analyzes and reviews the relationship between Aegilops tauschii and wheat, the research progress of Aegilops tauschii, the discovery of disease resistance genes from Aegilops tauschii, and the application of disease resistance genes from Aegilops tauschii to modern wheat breeding, providing a reference for the further exploration and utilization of Aegilops tauschii in wheat disease resistance breeding.

1. Introduction

As one of the major crops, wheat is the main grain for about one third of the world’s population, and its yield is of great significance for alleviating global hunger [1]. According to the FAO, pests and diseases cause 20–40% of global food crop losses and losses of USD 220 billion in agricultural trade every year [2]. In the long-term natural selection and artificial selection, wheat has lost many excellent disease resistance genes [3,4], resulting in a single genetic background of wheat.
Aegilops tauschii belongs to the genus Aegilops in the Triticeae family of Poaceae [5]. It is an annual weed in wheat fields and is also a relative plant of wheat and the donor species of the D genome during the evolution of common hexaploid wheat [6,7]. Compared with the D genome of wheat, Aegilops tauschii has a richer genetic diversity and contains many stress resistance, disease resistance, and insect resistance genes, among many other excellent genes, which are an important breeding resource for wheat breeders to improve wheat traits as well as disease resistance and stress resistance [8,9,10,11]. Therefore, fully exploring and utilizing the excellent disease resistance genes in Aegilops tauschii are of great value for wheat disease resistance breeding.

2. The Relationship between Aegilops tauschii and Wheat

Aegilops tauschii (DD, 2n = 14), which originates from West Asia, is mainly distributed in the Middle East, Europe, West Asia, and other places [12,13]. In China, Aegilops tauschii is mainly distributed in Xinjiang and the Yellow River Basin (including Shaanxi and Henan Provinces) [14,15]. There are two main lines of introducing Aegilops tauschii into the Yellow River Basin of China: first, Middle East→Russia→Xinjiang, China→Yellow River Basin into China; second, it was directly imported from the Middle East via the ancient Silk Road without passing through Xinjiang [16] (Figure 1a,b). As the donor of the D genome of wheat, Aegilops tauschii has a wider distribution area and higher genetic diversity than common hexaploid wheat. The addition of the D genome makes hexaploid wheat more adaptable to continental climates, which has laid a solid foundation for the large-scale cultivation of wheat [17].
Wheat originated in the fertile crescent of the Middle East. The first domesticated wild wheat was Triticum monococcum, followed by cultivated emmer wheat (Triticum turgidum); finally, the common wheat (Triticum aestivum) was formed through natural hybridization between cultivated emmer wheat and Aegilops tauschii along the Caspian Sea coast [18]. As for how wheat evolved from diploid wheat to the present allohexaploid wheat, there are two theories: one is formation by direct homoploid hybridization. Marcussen et al. found that approximately 6.5 million years ago, the wheat lineage (Triticum and Aegilops) began to differentiate from a common ancestor into the A and B genome lineages. About 5.5 million years ago, the first hybridization occurred between the A and B genome lineages and led to the origin of the D genome lineage. Furthermore, the second hybridization between the A genome donor Triticum urartu (AA) and a related species (BB) of Aegilops speltodies occurred approximately 0.8 million years ago, resulting in allotetraploid emmer wheat (Triticum turgidum; AABB), which then acclimated to cultivated tetraploid wheat, being crossed again with the D genome donor Aegilops tauschii (DD) about 0.4 million years ago to form hexaploid wheat; finally, it was acclimated to Triticum aestivum (AABBDD) [19]. In addition, Li et al. re-evaluated the homoploid hybrid origin of Aegilops tauschii. Based on the whole chloroplast genome sequence, they analyzed the neighbor joining tree of the Triticum–Aegilops complex and found that the chloroplast topology reveals that Aegilops tauschii is cladistically nested between the A and remaining S * and M genomes. They gave two possible explanations, i.e., the chloroplast capture model and the ancestry capture model. Therefore, they clearly pointed to a more complex history of Aegilops tauschii than that proposed by Marcussen et al. [19], one that may have involved multiple rounds of both recent and ancient hybridizations [20]. Then, Aegilops tauschii hybridized with tetraploid wheat to form hexaploid wheat. According to Alison et al., wheat was introduced into China in at least two ways. The first is that wheat came from the northwest of West Asia, moving through Eurasia, southern Siberia, and Mongolia to the middle and lower reaches of the Yellow River; the second is that wheat came from West Asia, potentially moving through the Afghanistan or Central Asian oases and northern Xinjiang into China’s Yellow River Basin, rather than the Eurasian steppe [21] (Figure 1c,d). China is the secondary origin center of wheat, mainly including three wheat subspecies: Yunnan wheat (Triticum aestivum ssp. yunnanense King), Tibet semi-wild wheat (Triticum aestivum ssp. tibetanum Shao), and Xinjiang wheat (Triticum aestivum ssp. Petropavlovsk yi) [22].
Since the domestication of wheat, yield improvement has always been the focus of wheat research. By improving cultivation measures and breeding techniques, the yield per unit area of wheat has been greatly increased [23,24,25,26,27,28,29,30,31,32]. Among them, enhancing wheat disease resistance has always been an important part of improving wheat yield. Aegilops tauschii contains abundant beneficial genes for disease resistance, insect resistance, cold resistance, and high quality, which is of great significance for improving wheat yield.
By analyzing the relationship between the two species, it has been proved that Aegilops tauschii is an important germplasm resource of wheat. During the long-term evolution process of wheat, the genetic diversity of the D genome has gradually narrowed, resulting in few available genetic resources. However, as the donor of the D genome of wheat, Aegilops tauschii carries abundant excellent genes, and the genetic material between them can be exchanged and recombined, which provides a valuable genetic resource pool for wheat breeding. Since both of these wheat species originated in West Asia, we can further enrich wheat germplasm resources by exploring wild wheat and Aegilops tauschii from West Asia.

3. The Research Progress of Aegilops tauschii

At present, the research on Aegilops tauschii mainly includes the construction of the Aegilops tauschii gene map, the utilization of distant wheat germplasm resources, and the control of malignant weeds in crop fields.
(1) Construction of Aegilops tauschii gene map: Jia et al. [33] used AL8/78 as the research material to construct the Aegilops tauschii gene map and sequenced the entire genome of AL8/78 with Illumina high-throughput sequencing technology to obtain the whole genome sketch of Aegilops tauschii. Luo et al. [34] sequenced the BAC library of AL8/78 using the snapshot method, developed an SNP chip, and constructed a physical map containing 7185 markers, which laid the foundation for the analysis of Aegilops tauschii. Luo et al. [35] generated a reference-quality genome sequence for Aegilops tauschii strangelata accession AL8/78 by using ordered clone genome sequencing, whole-genome shotgun sequencing, and BioNano optical genome mapping, which is closely related to the wheat D genome. Zhao et al. [36] used new sequencing assembly technology to assemble AL8/78 and obtain new genomic data. Previous studies on the construction of the Aegilops tauschii gene map, on the one hand, provided data support for fragment location and cloning of Aegilops tauschii itself; on the other hand, they provided technical support for genetic improvement of wheat breeding and made important contributions to the research and utilization of Aegilops tauschii resources.
(2) Utilization of distant wheat germplasm resources: Previous studies on the germplasm resources of Aegilops tauschii mainly focused on the exploration and utilization of disease resistance genes, insect resistance genes, high-yield genes, etc. The development of disease resistance genes is the focus of wheat germplasm resources. There is a lot of research in this area. The second part of this paper mainly introduces the research in this area in detail. At present, there are eight permanently named cereal cyst nematode resistance genes, namely, Cre1–Cre8, and only two genes, Cre3 and Cre4, were derived from Aegilops tauschii [37,38]. Later, Lage et al. [39] found a gene resistant to wheat aphids on the genome of Aegilops tauschii. In the study of high-yield genes, Wan et al. [40] found a major QTL for leaf sheath hairiness (LSH) on Aegilops tauschii 4DS, and the allele of this QTL locus was significantly positively correlated with the increase in grain yield, grain weight, and grain weight per spike. Delorean et al. [41] sequenced 273 accessions spanning the known diversity of Aegilops tauschii. They found that Aegilops tauschii is a reservoir for unique Glu-D1 alleles and provides a genomic resource for improving wheat quality.
(3) Control of malignant weeds in crop fields: In the current production, the herbicide mesosulfuron–methyl is mainly used to control Aegilops tauschii in wheat fields, and it is often used in combination with the safener mefenpyr–diethyl [42]. However, Yuan et al. [43] found that the tolerance of Aegilops tauschii to mesosulfuron–methyl was significantly increased in the presence of mefenpyr–diethyl by performing a bioassay, and they proposed that seed dressing with mefenpyr–diethyl could replace spraying to improve the resistance of wheat to mesosulfuron–methyl and enhance the control effect on Aegilops tauschii.

4. Discovery of Disease Resistance Genes from Aegilops tauschii

As an important resource of wheat resistance genes, Aegilops tauschii provides stripe rust resistance genes, leaf rust resistance genes, powdery mildew resistance genes, brown spot resistance genes, etc.

4.1. Discovery of Rust Resistance Genes from Aegilops tauschii

Rust is one of the main diseases of wheat, including three types: stripe rust, leaf rust, and stem rust [44].

4.1.1. Discovery of Stripe Rust Resistance Genes from Aegilops tauschii

Wheat stripe rust is a common disease of wheat, caused by Puccinia striiformis f. sp. tritici (Pst), which is characterized by a high prevalence and frequency, a wide incidence range, and serious damage [45]. It is estimated that the annual loss of wheat production caused by stripe rust worldwide is over 5 million tons, with an estimated market value of USD 1 billion [46]. On the one hand, the pathogen of stripe rust invades wheat and absorbs wheat nutrients and water, affecting plant growth; on the other hand, it causes a reduction in the wheat leaf area, affecting photosynthesis, and reducing wheat yield. Using wheat stripe rust resistance genes to control wheat stripe rust is the most effective and environmentally friendly way to counter this disease [47]. At present, there are 84 permanently named stripe rust resistance genes in wheat, namely, Yr1–Yr84, and only 8 genes, Yr5, Yr7, Yr15, Yr18, Yr27, Yr28, Yr36, and Yr46, have been cloned [17,48,49,50,51,52,53,54]. Among them, only the Yr28 gene is derived from Aegilops tauschii (Table 1).
Yr28 was first discovered and named by Singh et al. [55], and it was located on the short arm of the 4D chromosome and had resistance to multiple stripe rust races, showing all-stage resistance (ASR) in Aegilops tauschii. Liu et al. [56] and Huang et al. [57] found the dominant stripe rust resistance gene YrAS2388 in Aegilops tauschii and located it on chromosome 4DS. In 2013, Liu et al. [58] found the existence of YrAS2388 in the subspecies Aegilops tauschii subsp. Strangulata near the Caspian Sea. In 2019, Zhang et al. [17] cloned the YrAs2388 gene using traditional map-based cloning technology, confirmed that the YrAs2388 gene is the internationally named Yr28 gene, and introduced this gene into hexaploid wheat using synthetic wheat. Yr28 encodes a typical NBS-LRR structural protein (NLR4DS-1). Compared with the susceptible haplotype of Yr28, the resistant haplotype has two repeated 3′ untranslated regions (3′UTR1 and 3′UTR2), and there are five transcript variants in the domain of the gene (two alternative splicing variants are associated with 3’UTR1, and the other three alternative splicing variants are associated with 3’UTR2), which makes Aegilops tauschii and synthetic wheat containing the Yr28 gene resistant to stripe rust, but Yr28 only shows adult plant resistance (APR) in synthetic wheat. Athiyannan et al. [59] found a full-growth period resistance gene, YrAet672, from Aegilops tauschii CPI110672 and successfully cloned it through map-based cloning. It was proved that the gene was identical to the coding region sequence of YrAS2388, only being different in the 5’UTR and 3’UTR regions, and was an allele of YrAS2388 and Yr28. The study also found that the hexaploid wheat genome can inhibit the expression of YrAet672, where there may be some modification or inhibition of the gene.

4.1.2. Discovery of Leaf Rust Resistance Gene from Aegilops tauschii

Wheat leaf rust is a fungal disease caused by Puccinia triticina (Pt), which has the characteristics of multiple infection and strong harmfulness [60]. When wheat is infected with leaf rust, the yield decreases by 5–15%, and the yield loss even reaches 40% in pandemic years [61]. Wheat leaf rust fungus mainly affects the normal growth and development of wheat by infecting wheat leaves, especially photosynthesis, and then affects grain filling, resulting in a reduction in the 1000-grain weight [62]. Up to now, 82 wheat leaf rust resistance genes have been identified, namely, Lr1–Lr82 [63,64], although only seven genes, Lr1, Lr10, Lr13, Lr21, Lr22a, Lr34, Lr42, and Lr67, have been cloned [65,66]. At present, the leaf rust resistance genes from Aegilops tauschii include Lr21, Lr22a, Lr32, Lr39, and Lr42 [67,68,69,70,71] (Table 1).
The Lr21 gene was found in synthetic wheat RL5406 by Rowland and Kerber in 1974 and is located on chromosome 1DS. The gene was derived from Aegilops tauschii on the coast of the Caspian Sea [67] and is an all-stage resistance gene. In 2003, Li and Gill found that RGA-like could be used to mark all known members of the Lr21 leaf rust resistance gene family in Aegilops tauschii and wheat, and the Lr21 gene was successfully cloned using the diploid/polyploid shuttle localization strategy [72,73]. Scofield et al. [74] analyzed the resistance mechanism of Lr21 using virus-induced gene silencing and found that Lr21 encodes a leucine-rich repeat resistance gene product at the nucleotide binding site, which may contribute to wheat resistance. To further elucidate the origin of the Lr21 gene, Huang et al. [75] identified and analyzed three basic non-functional Lr21 haplotypes, H1, H2, and H3, by analyzing the Lr21 and Lr21 allele sequences of 24 wheat cultivars and 25 Aegilops tauschii and found that Lr21 is a chimera of H1 and H2 in wheat. The next year, Fu et al. [76] re-sequenced the wheat leaf rust resistance locus Lr21 of 95 wheat varieties released in Canada, revealed 13 SNPs, 4 insertions and deletions, 10 haplotypes, and 4 major haplotype groups, and developed a new SCAR marker to identify resistant haplotypes and haplotype groups. In North America, Kolmer and Anderson found that the physiological races TFBJQ and TFBGQ were toxic to wheat varieties containing Lr21 [77]. Kumari et al. [78] developed a KASPar marker for the Lr21 gene and tested it on 384 American wheat lines, finding that the marker could effectively distinguish resistant and susceptible genotypes and could be applied to molecular-marker-assisted breeding of disease-resistant wheat varieties through gene pyramiding. Naz et al. [79] studied the evolution and functional differentiation of Lr21 in diploid and hexaploid wheat by using population genetics and high-resolution comparative genomics and found that there were at least two independent polyploidization events in wheat evolution. At the same time, a unique Lr21-tbk allele and its neofunctionalization were discovered in hexaploid wheat, and the seedling resistance and adult plant resistance were related to the development-dependent variation in Lr21 expression, which helps us to further understand the evolution of Lr21 and its role in broad-spectrum resistance to leaf rust in wheat.
Lr22a was discovered by Dyck and Kerber in synthetic wheat derived from common wheat and Aegilops tauschii and mapped on chromosome 2DS [68]. Pretorius found that in adult-plant-resistant wheat line RL6044, Lr22a was not expressed at the seedling stage but at the adult stage, indicating that Lr22a endowed this line with adult plant resistance (APR) [80]. The next year, Pretorius found that Lr22a was a partially recessive monogenic inheritance [81]. In order to select varieties containing the Lr22a gene among different wheat lines, Hiebert et al. [82] found that a GWM marker is close to Lr22a and could be used as a microsatellite marker of the Lr22a gene, and it is useful under different genetic background conditions. Based on TACCA (targeted chromosome-based cloning via long-range assembly), Thind et al. [83] cloned the broad-spectrum leaf rust resistance gene Lr22a using molecular marker information and ethyl methane sulfonate (EMS) mutants and found that Lr22a encodes an intracellular immune receptor homologous to the RPM1 protein of Arabidopsis thaliana. Although Lr22a has broad-spectrum resistance and has been successfully cloned, it has not been widely used in production. Sharma et al. [84] identified and isolated SNPs using the Lr22a coding sequence and developed four competitive allele-specific polymerase chain reaction (KASP) markers, which can reliably detect the presence or absence of Lr22a and will contribute to the application of Lr22a in breeding.
Lr32 is a whole-growth period resistance gene, which was first discovered by Kerber et al. and later located on the 3DS chromosome. Thomas found that the Lr32 gene has two simple sequence repeat (SSR) loci, wmc43 and barc135, which can be used as superposition markers between Lr32 and other widely effective leaf rust resistance genes [69,85,86].
Lr39 was first discovered by Pretorius and located on 2DS by Raupp through microsatellite marker analysis, and it is a full-growth stage disease resistance gene [70,87]. Li et al. [88] revealed 36 differentially expressed genes (DEGs) for wheat leaf rust resistance mediated by Lr39/41 through suppression subtractive hybridization and microarray analysis and quantitatively analyzed the expression levels of eight selected DEGs at different stages of Lr39/41-mediated resistance.
Lr42 is a partially dominant gene, which was discovered and reported by Cox et al. together with the Lr41 and Lr43 genes; Sun et al. located it on chromosome 1DS [71,89]. Harsimardeep et al. [90] found that Lr42 was dominant in Aegilops tauschii, fine-mapped the gene to the 3.16 Mb genomic region on chromosome 1DS of Chinese Spring and the 3.5 Mb genomic region on chromosome 1 of the Aegilops tauschii reference genome, and developed two co-dominant allele-specific polymorphism (KASP) markers (SNP113325 and TC387992) on the flanking region of Lr42 for assisted breeding selection. Liu et al. [91] identified the sequence polymorphism of the differentially expressed gene (TaRPM1) encoding the hypothetical NB-ARC protein in the Lr42 candidate region through RNA sequencing of the Lr42 allelic variation near-isogenic line and developed a diagnostic DNA marker for Lr42. The marker is designed based on deletion mutations and single-nucleotide polymorphisms (SNPs) in the gene and has the advantages of a low cost and easy determination. In 2022, Lin et al. identified three candidate genes of Lr42 using the batch-isolated RNA-Seq (BSR-Seq) mapping strategy. Among them, the gene AET1Gv20040300 has obvious sequence differences in disease-resistant and susceptible varieties. The down-regulation of the Lr42 gene caused by virus-induced gene silencing (VIGS) and the mutation of the Lr42 C700Y amino acid caused by mutagenesis were carried out on this gene. It was found that both caused the loss of resistance of the Aegilops tauschii line TA2450, and the candidate gene AET1Gv20040300 was finally determined as Lr42 and successfully cloned [92].

4.1.3. Discovery of Stem Rust Resistance Genes from Aegilops tauschii

Wheat stem rust, caused by Puccinia graminis Pers. f. sp. tritici, is one of the most devastating fungal diseases in wheat production. The disease can lead to wheat production reductions of up to 75%, and some areas even experience no production [93]. Stem rust mainly destroys the tissues of wheat stems and leaves. Its spores can penetrate the leaves, invade the host from the stomata, reduce the photosynthetic area of the host, destroy the guiding tissues of the stems, and hinder nutrient transport [94]. At present, 62 wheat stem rust resistance genes have been officially named, namely, Sr1–Sr62 [95,96,97,98], of which Sr13, Sr21, Sr22, Sr33, Sr35, Sr45, Sr46, Sr50, and Sr62 have been cloned [98,99,100,101,102,103,104,105]. At present, there are three genes, Sr33, Sr45, and Sr46, found to be resistant to stem rust in Aegilops tauschii [106,107,108] (Table 1). Furthermore, some stem rust resistance genes are still under investigation and not formally named, such as the SrTA10187 and SrTA10171 genes located on chromosomes 6DS and 7DS, respectively [109]. Wiersma et al. finely mapped SrTA10187 to the 1.1cM region and developed PCR-based SNP and STS markers using genotyping-by-sequencing tags and SNP sequences available in online databases [110].
Sr33 is an adult plant resistance gene; Kerber and Dyck first discovered it, and then Jones et al. located it on the 1DS chromosome arm of wheat through the double-terminal and normal chromosome 1D recombination substitution line. This gene is derived from Aegilops tauschii [111,112]. Han et al. discovered the co-dominant markers Xbarc152 and Xcfd15, located on both sides of Sr33 [113]. Sambasivam successfully cloned Sr33 and found that it encodes a coiled-coil, nucleotide-binding, leucine-rich repeat protein, which is closely related to its ability to confer stem rust resistance in wheat [100]. Through bioinformatics analysis, Ivaschuk et al. found that sequences S5DMA6 and E9P785 were the closest homologues of the Sr33 gene product RGA1e protein [114]. Md Hatta et al. found that Sr33 functions not only in wheat but also in barley to resist stem rust [115].
Sr45 comes from Aegilops tauschii; it was discovered by Marais et al. and is closely linked to Sr33 and localized on chromosome 1DS [116]. It is an adult plant disease resistance gene [117]. Therefore, to develop a marker for the identification of Sr45 in the tight linkage of centromere-Sr45-Sr33-Lr21-telomere, Periyannan et al. fine-mapped the Sr45 region in a large mapping population generated by the hybridization of CS1D5406 (the disomic substitution line on chromosome 1D of RL5406 replaced Chinese Spring 1D) with Chinese Spring and amplified a fragment linked to Sr45 using an AFLP marker sequence to mark Sr45-carrying haplotypes [107]. Steuernagel used MutRenSeq technology to clone the stem rust resistance gene Sr45 by combining chemical mutagenesis with exon capture and sequencing [102]. Md Hatta et al. found that Sr45, like Sr33, could confer stem rust resistance in both wheat and barley [115].
Sr46 was discovered by Evans but not published in relevant papers; however, it was then included in the “Catalogue of Gene Symbols for Wheat” by McIntosh [108,117]. Yu et al. located Sr46 on 2DS. The gene is significantly affected by temperature and is an adult plant resistance gene. In the meantime, Yu et al. found that two closely linked markers, Xgwm210 and Xwmc111, could be used for marker-assisted selection of Sr46 in wheat breeding [108]. Arora et al. combined association genetics with R gene enrichment sequencing (AgRenSeq) to successfully clone the stem rust resistance gene Sr46 [105]. Aegilops tauschii germplasms RL5271 and CPI110672 were resistant to wheat stem rust. Athiyannan et al. identified RL5271 and found that SrRL5271 was the dominant resistance gene in RL5271, while CPI110672 resistance was separated in Sr672.1 and Sr672.2. They also found that SrRL5271 and Sr672.1 have the same sequence and are the alleles of Sr46, except that an amino acid sequence (N763K) is different from Sr46, although the other amino acid sequences are identical [118].

4.2. Discovery of Powdery Mildew Resistance Genes from Aegilops tauschii

Wheat powdery mildew is a widespread wheat disease in the world, which is caused by Blumeria graminis f. sp. Tritici (Bgt). The yield reduction caused by powdery mildew accounts for about 5% of the yield reduction caused by wheat pests and diseases, which seriously affects the yield improvement and quality improvement of wheat [119]. Wheat powdery mildew is a type of living parasitic fungus. When conidia make contact with living tissues such as the leaves and stems of wheat, they will be immersed in host cells to form white flocculent small mildew spots, which weakens plant photosynthesis and enhances transpiration and respiration, resulting in reduced plant dry matter accumulation and reduced yield [120]. Thus far, a total of 68 wheat powdery mildew resistance genes have been officially named, namely, Pm1–Pm68, and Pm1a, Pm2, Pm3b, Pm4, Pm5e, Pm8, Pm17, Pm21, Pm24, Pm38, Pm41, Pm46, and Pm60 have been cloned [49,50,121,122,123,124,125,126,127,128,129,130,131]. Meanwhile, researchers have found 140 QTLs for powdery mildew resistance, distributed in 21 chromosomes of wheat, among which 4 QTLs have been confirmed and widely used in some regions or units [132]. Thus far, the powdery mildew resistance genes discovered and officially named from Aegilops tauschii include Pm2a, Pm19, Pm34, Pm35, and Pm58 [133,134,135,136,137] (Table 1).
Pm2a, a powdery mildew resistance gene, was discovered by Pugsley and Carter in 1953 and later officially named Pm2, with whole-growth resistance [133,138]. In 1970, researchers found that Pm2a was located near the centromere of wheat chromosome 5DS [139]. Lutz et al. [140] obtained 40 materials containing the Pm2 gene from 400 Aegilops tauschii materials. Sáchez-Martín et al. [123] cloned the wheat powdery mildew resistance gene Pm2a using the MutChromSeq (mutant chromosome sequencing) strategy. Since powdery mildew and disease resistance genes are consistent with the gene-for-gene hypothesis, there are corresponding avirulence genes in the pathogen, which react with disease resistance genes to stimulate a wheat disease resistance response [141]. Praz et al. [142] cloned the avirulence gene BgtE-5845 corresponding to Pm2 by combining genetic mapping and association analysis, namely AvrPm2, and speculated that AvrPm2 may have dual functions: first, it has the function of recognizing and stimulating the host immune response with Pm2 in incompatible interactions; second, it participates in the formation of haustoria in the affinity interaction and inhibits the function of the host cell defense response. Manser et al. [143] further studied AvrPm2 and found two other haplotypes of AvrPm2, AVRPM2-H1 and AVRPM2-H2, in powdery mildew strains USA7 and USA2, and only AVRPM2-H1 could be specifically recognized by Pm2a.
Pm19 is a new powdery mildew resistance gene discovered by Lutz et al. [134] in their progeny by crossing two powdery mildew resistance wheat lines with susceptible durum wheat, and it is located on chromosome 7D.
Pm34 was discovered by Miranda et al. [135] using the F (2) derivative line of NC97BGTD7×Saluda, and it is a new wheat powdery mildew resistance gene; the authors then marked the gene on the long arm of chromosome 5D with microsatellite markers and officially named it Pm34.
Pm35 is a single gene controlling powdery mildew resistance identified by Miranda et al. [136] through genetic analysis of the F (2) derivative line of NCD3×Saluda. Miranda then located the gene on chromosome 5DL with microsatellite markers, and the gene was independent from Pm34, being officially named Pm35.
Pm58 was derived from Aegilops tauschii TA1662 near the Caspian Sea. Wiersma et al. used 96 BC2F4 introgression lines to position Pm58 within an interval of 8.6 Mb on chromosome 2DS and obtained two high-generation lines carrying the Pm58 gene and excellent agronomic traits the following year [137,144]. These two lines are highly resistant to powdery mildew, but the yield is lower than that of common wheat. In 2022, Xue et al. [145] fine-mapped the Pm58 gene into a 141.3 Kb Xsts20220-Xkasp61553 region and developed a co-segregated KASP marker, Xkasp68500, that could be used for Pm58-assisted selection breeding.

4.3. Discovery of Other Disease Resistance Genes from Aegilops tauschii

Besides stripe rust resistance genes, leaf rust resistance genes, and powdery mildew resistance genes, Aegilops tauschii also contains septoria tritici blotch resistance genes and brown spot resistance genes. Stb5 is a septoria tritici blotch resistance gene, which was discovered by Arraiano et al. in Synthetic 6x (derived from a hybrid of Triticum dicoccoides and Triticum tauschii) and located on the 7D short arm, endowing the plant with resistance at the whole-growth stage [146,147] (Table 1). Tsr3, a brown spot resistance gene, from tetraploid wheat and Aegilops tauschii synthetic wheat lines (CS/XX41, CS/XX45, and CS/XX110) was identified by Tadesse et al. (Table 1). The Tsr3 gene is a recessive gene. Tadesse et al. used SSR markers to carry out linkage analysis and found that Tsn3a of XX41, Tsn3b of XX45, and Tsn3c of XX110 were clustered near Xgwm2a, located on the short arm of chromosome 3D [148].
Table
Table 1. Officially named disease resistance genes in Aegilops tauschii.
Table 1. Officially named disease resistance genes in Aegilops tauschii.
ClassificationGeneTypesChromosomeClonedReference
stripe rust resistance genesYr28ASR4DSYes[55]
leaf rust resistance genesLr21ASR1DSYes[67]
Lr22aAPR2DSYes[68]
Lr32ASR3DSNo[69]
Lr39ASR2DSNo[70]
Lr42ASR1DSYes[71]
stem rust resistance genesSr33ASR1DSYes[111]
Sr45APR1DSYes[116]
Sr46APR2DSYes[108]
powdery mildew resistance genesPm2aASR5DSYes[133]
Pm19ND7DNo[134]
Pm34ND5DLNo[135]
Pm35ND5DLNo[136]
Pm58ND2DSNo[137]
septoria tritici blotch resistance genesStb5ASR7DSNo[146]
brown spot resistance genesTsr3ND3DNo[148]
ND: not detected; ASR: all-stage resistance; APR: adult plant resistance.

5. Application of Disease-Resistant Genes from Aegilops tauschii in Wheat Breeding

The utilization of disease resistance genes in Aegilops tauschii is of great significance for expanding wheat disease resistance. Synthetic hexaploid wheat (SHW) is an artificially created hexaploid wheat that can simultaneously introduce genetic variations from tetraploid wheat and Aegilops tauschii, and it has been widely used to expand the genetic diversity of common wheat [149]. The method mainly includes two main steps: First, a hybrid F1 with an ABD genome is produced by direct hybridization of tetraploid wheat with Aegilops tauschii, and then a synthetic hexaploid wheat with an AABBDD genome is obtained through chromosome doubling [149]. Second, the genetic variation in Aegilops tauschii and tetraploid wheat is introduced into common wheat varieties by using the artificial synthetic hexaploid wheat as a bridge and common wheat as a backcross or topcross [107].

5.1. Application of Rust Resistance Genes from Aegilops tauschii in Wheat Breeding

5.1.1. Application of Stripe Rust Resistance Genes from Aegilops tauschii in Wheat Breeding

Yr28 is the first stripe rust resistance gene cloned from Aegilops tauschii. Through map-based cloning results, previous researchers designed resistance co-segregation molecular markers, conducted auxiliary selection, and bred a new variety, Shumai 1675 [17]. The main cultivation processes were as follows: (1) introducing disease resistance genes into synthetic hexaploid wheat; (2) establishing a breeding population; (3) F2 small group mixed selection; (4) F3 small population for molecular marker selection to prevent target gene loss; (5) F5 line focused on the selection of yield-related traits, and molecular marker selection of disease resistance genes [150]. After the above processes, the yield of F5 and its selected line Shumai 1675 increased significantly and showed stripe rust resistance.

5.1.2. Application of Leaf Rust Resistance Genes from Aegilops tauschii in Wheat Breeding

Lr21 is the first powdery mildew resistance gene found and successfully cloned from Aegilops tauschii. Thus far, the application of the Lr21 gene in wheat breeding is low. Mebrate et al. [151] used 31 Pt races to detect 36 wheat cultivars from Ethiopia and Germany and found that Sirbo and Granny contained Lr21. Gebrewahid et al. [152] identified 83 wheat varieties and 36 lines with known leaf rust resistance (Lr) genes from three provinces in China. There were 41 cultivars containing leaf rust resistance (Lr) genes, but only Wanmai 47 contained Lr21. Khakimova et al. [153] studied 36 synthetic hexaploid wheat varieties from Russia and identified 11 materials containing Lr21. Zhang et al. [154] identified and analyzed 46 Chinese landraces and found that only Baiheshang contained Lr21.
Lr22a has broad-spectrum resistance to wheat leaf rust, but it has not been widely used in production due to differences in varieties from different regions. Khakimova et al. [153] studied 36 synthetic hexaploid wheat varieties from Russia and found that three of them contained Lr22a. Huang et al. identified and analyzed 36 wheat production varieties in Gansu Province and found that the varieties Huining 15, Lantian 37, and Longjian 113 showed resistance to all Lr22a non-toxic races, indicating that these three materials may contain Lr22a [155]. However, Atia et al. [156] identified and analyzed 50 wheat varieties in Egypt and successfully identified 21 Lr genes, and all wheat varieties contained Lr22a.
Although Lr32 has not been cloned successfully, it was found that the disease-resistant wheat varieties contained this gene in actual production identification. Zhao et al. identified 23 Chinese wheat microcore collections, and the five core germplasms of Tongjiaba wheat, Honghua wheat, Kefeng 3, Atlas66, and Golden wheat contained the Lr32 gene [157]. Hanaa et al. [158] identified leaf rust resistance in 10 Egyptian spring wheat varieties at the seedling stage and found that Sids12 and Sakha93 contained Lr32. Bahar et al. [159] used SSR markers of 13 resistance genes to identify 57 wheat lines and found that all 57 lines contained Lr32. Atia et al. [156] identified and analyzed 50 wheat varieties in Egypt and successfully identified 21 Lr genes, and all wheat varieties contained Lr32.
Lr39 is a powdery mildew resistance gene of wheat at the seedling stage, and it has certain development value [160]. Hanaa et al. [158] identified leaf rust resistance in 10 Egyptian spring wheat varieties at the seedling stage and found that Miser1 and Miser2 contained Lr39. Atia et al. [156] identified and analyzed 50 wheat varieties in Egypt and successfully identified 21 Lr genes, and 42 wheat varieties contained Lr39. Wang et al. identified the leaf rust resistance of 71 important wheat production varieties in Henan Province and found that four cultivars contained Lr39 [161].
As early as 1991, Lr42 was transferred from Aegilops tauschii to common wheat through hybridization by the Wheat Germplasm Resources Center (WGRC) of Kansas State University in the United States, and the KS91WGRC11 wheat line was developed [162]. Subsequently, the International Maize and Wheat Improvement Center (CIMMYT) widely applied the disease resistance genes in this line to breeding materials. Through the identification and analysis of 103 wheat varieties (lines) of CIMMYT and 35 control varieties containing known leaf rust resistance genes, Han et al. found that 11 CIMMYT wheat varieties may contain Lr42 [163]. Liu et al. tested 66 wheat varieties approved by Qinghai Province and found that 23 varieties contained Lr42, accounting for 34.85% [164]. Among 52,943 CIMMYT lines or varieties sequenced by GBS, 5121 pedigrees contained Lr42 [92].

5.1.3. Application of Stem Rust Resistance Genes from Aegilops tauschii in Wheat Breeding

Sr33 is an important gene for resistance to the physiological race Ug99 of stem rust, and its wide application is of great significance to reduce the harm of stem rust. Ma et al. conducted SSR detection on 58 spring wheat varieties resistant to Ug99 introduced at home and abroad and 18 main wheat varieties in Heilongjiang Province and found that only one spring wheat variety material resistant to Ug99 and three main wheat varieties in Heilongjiang Province contained the Sr33 gene [165].
Periyannan et al. [107] found that Sr45 was effective against Puccinia graminis f. sp. tritici races prevalent in small populations in Australia and South Africa and the Ug99 race group, but the related detection was lower.
Kokhmetova and Atishova found that only the Sr46 gene existed in the 338-K1-1//ANB/BUC/3/GS50A/4/422/5/BAYRAKTAR line when detecting 88 cultivars of spring soft wheat in Kazakhstan [166].

5.2. Application of Powdery Mildew Resistance Genes from Aegilops tauschii in Wheat Breeding

Pm2a, as a successfully cloned gene from Aegilops tauschii, is of great significance in wheat breeding for powdery mildew resistance. Švec et al. [167] identified the Pm2 gene in 32 Polish wheat varieties. Agnieszka et al. [168] identified seven wheat varieties from Europe by establishing a multiplex PCR reaction and found that all wheat varieties contained the Pm2 gene. Jimai 22 has been approved and widely promoted in Shandong Province and the northern part of Huanghuai; as of the summer harvest in 2020, the cumulative promotion area was 20 million hm2. Liangxing 66 has been promoted and planted in Shandong, central and southern Hebei, southern Shanxi, and Anyang, Henan, to the north of the Huanghuai winter wheat region [169]. Through genetic analysis and molecular marker detection, the above two varieties were found to carry the wheat powdery mildew resistance gene Pm2 [170]. With the increase in the utilization frequency of Pm2 in production, the frequency of the corresponding virulent species variation is also rising, resulting in an increasing risk of overcoming Pm2 resistance.
With the acceleration of variety replacement, the varieties containing Pm19 in actual production have gradually increased. Li et al. [171] identified 23 white powdery mildew-resistant materials and found that only one material contained Pm19. According to the identification results, Pm19 was considered to have low resistance and should be used in combination with other resistance genes. Shi et al. [172] identified 61 reserve varieties of powdery mildew in China and found that 21 wheat varieties contained powdery mildew resistance genes, and four of them contained Pm19.
Although Pm34 has not been cloned, it has been identified to contain this gene in wheat in actual production. Li et al. [173] identified 42 Yunnan wheat varieties using 20 wheat powdery mildew strains with different toxicity profiles and found that four varieties contained Pm34. Wang et al. [174] analyzed 305 wheat germplasm resources at home and abroad and found that 95 wheat varieties contained Pm34, accounting for 31.15%, including Lumai 5, Yanzhan 4110, Fengsheng 3, Jimai 22, CA9719, and Azulon.
El-Shamy et al. [175] used 12 Egyptian wheat varieties to identify the virulence of 52 powdery mildew strains and found that wheat varieties containing the Pm35 gene had higher disease resistance. However, in actual production, there are few wheat varieties containing Pm35. Through toxicity monitoring and annual dynamic change analysis of wheat powdery mildew populations in Shaanxi Province, China, Liu et al. found that NCD3 wheat varieties containing Pm35 had higher disease resistance [176]. Yan et al. identified 371 wheat materials from Hebei Province and found that only Pubing 01 contained the Pm35 gene [177].
Due to the late discovery and cloning of Pm58, only the germplasm lines U6714-A-011 (Reg.No.GP-1023, PI682090) and U6714-B-056 (Reg.No.GP-1022, PI 682089) of the new powdery mildew resistance gene Pm58 cultivated by Michigan State University using TA1662 and KS05HW14 are currently available, but the wheat yields of these two germplasm lines need to be improved [144].

5.3. Application of Other Disease-Resistant Genes from Aegilops tauschii in Wheat Breeding

Because the genetic research on wheat septoria tritici blotch resistance genes are relatively slow, Stb5, as the only localized gene of wheat septoria tritici blotch in Aegilops tauschii, has not been widely studied and utilized in production [178].
Tsr3 is one of the four genes for wheat brown spot disease resistance officially mapped in Aegilops tauschii [179]. The research on Tsr3 is less than that on wheat resistance to wheat septoria tritici blotch, and relevant production research reports have not been found yet.

6. Expectations

With the completion of the wheat gene map construction, breeders, on the one hand, have stepped up their research on the genes of common wheat itself; on the other hand, they have also excavated and utilized wheat-related plants. Aegilops tauschii, as a relative plant of wheat and an ancestor species of the wheat D genome, has a wider genetic diversity than that of the wheat D genome. Compared with the wheat A and B genomes, the D genome has the lowest degree of excavation. At present, the gene map of Aegilops tauschii has been basically constructed, and a reference-quality genome sequence for Aegilops tauschii has been available since 2017. It is of great significance to supplement wheat’s genetic resources and improve its genetic diversity by fully excavating and utilizing the disease resistance genes in it.
According to previous studies, we found that there is still a huge gap from the successful gene mapping or cloning of genes in Aegilops tauschii to the application of genes to actual production. The utilization of wheat disease resistance genes in Aegilops tauschii should be promoted from the following aspects: (1) Intensify the excavation of wheat disease resistance genes in Aegilops tauschii. Through the previous studies on stripe rust, leaf rust, and stem rust, it is found that there are still few disease resistance genes discovered in Aegilops tauschii. Understanding how to explore more disease resistance genes from Aegilops tauschii will still be a key topic for a long time in the future. We should innovate the research methods of gene discovery and accelerate the discovery of excellent resistance genes in Aegilops tauschii through association map analysis, map-based cloning, MutChromSeq, long reads, CRISPRs, and other modern methods. (2) Clone the discovered wheat resistance genes. It can be seen from the previous description that although many wheat disease resistance genes have been discovered and mapped in Aegilops tauschii, there are still few genes successfully cloned, and the disease resistance mechanism still needs to be further studied. Because the traditional map-based cloning technology is very time-consuming and entails a huge, laborious workload, and because it often takes many years to successfully clone genes, understanding how to clone disease-resistant genes quickly and efficiently is still a difficult challenge for the future. (3) Accelerate the application of cloned genes in wheat resistance breeding production. Previous studies have shown that only a few of the cloned disease resistance genes in Aegilops tauschii have been successfully applied to breeding production, while the most widely used disease resistance genes in actual production are still the first few genes cloned. With the large-scale application of single disease-resistant genes and the continuous emergence of new pathogenic races, many production varieties will rapidly lose disease resistance after several years of planting. In production, polygene polymerization breeding should be adopted to broaden the variety of disease resistance genes and reduce the loss of disease resistance genes as much as possible. Moreover, there may be genetic encumbrance among the resistance genes. Therefore, understanding how to successfully break this genetic encumbrance, speed up the transfer of cloned genes into the wheat genome, and cultivate new disease-resistant lines is still the top priority in the application of disease resistance genes from Aegilops tauschii in wheat breeding.

Author Contributions

H.K. wrote a draft of the article with the help of G.Z. All the authors contributed to the conception and design of the article and revised it critically. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (32201737), the Natural Science Foundation of Shandong Province (ZR2021QC197), and the 2021 Youth Innovation Talent Introduction and Education Program of Shandong Province Universities.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Plants 12 00880 g001 550
Figure 1. Road map of the introduction of Aegilops tauschii and wheat into China. The route of Aegilops tauschii introduced into China: (a) Middle East→Russia→Xinjiang, China→Yellow River Basin; (b) the ancient Silk Road in the Middle East; (c) northwest of West Asia→Eurasia→southern Siberia and Mongolia→Middle and Lower Yellow River Region; (d) Afghanistan or Central Asia Oasis →Northern Xinjiang→Yellow River Basin.
Figure 1. Road map of the introduction of Aegilops tauschii and wheat into China. The route of Aegilops tauschii introduced into China: (a) Middle East→Russia→Xinjiang, China→Yellow River Basin; (b) the ancient Silk Road in the Middle East; (c) northwest of West Asia→Eurasia→southern Siberia and Mongolia→Middle and Lower Yellow River Region; (d) Afghanistan or Central Asia Oasis →Northern Xinjiang→Yellow River Basin.
Plants 12 00880 g001
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Kou, H.; Zhang, Z.; Yang, Y.; Wei, C.; Xu, L.; Zhang, G. Advances in the Mining of Disease Resistance Genes from Aegilops tauschii and the Utilization in Wheat. Plants 2023, 12, 880. https://doi.org/10.3390/plants12040880

AMA Style

Kou H, Zhang Z, Yang Y, Wei C, Xu L, Zhang G. Advances in the Mining of Disease Resistance Genes from Aegilops tauschii and the Utilization in Wheat. Plants. 2023; 12(4):880. https://doi.org/10.3390/plants12040880

Chicago/Turabian Style

Kou, Hongyun, Zhenbo Zhang, Yu Yang, Changfeng Wei, Lili Xu, and Guangqiang Zhang. 2023. "Advances in the Mining of Disease Resistance Genes from Aegilops tauschii and the Utilization in Wheat" Plants 12, no. 4: 880. https://doi.org/10.3390/plants12040880

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