Abstract
Plants have the capability to protect themselves from attacks by several types of fungal pathogens. Several powdery mildew resistance genes have been reported at different loci, and most of them have been originated from progenitors of wheat or wild accessions. Powdery mildew resistance is deliberated to be quantitative traits (QTLs), also considered as complex traits, because they are measured by several genes and are affected by fungal pathogens. Numerous researchers have been studied such traits in the past periods for the development of genetic markers, which could be used in several wheat breeding studies mainly encompassing simple sequence repeat, restriction fragment length polymorphism, random amplified polymorphic DNA, single nucleotide polymorphism, and amplified fragment length polymorphism. The discovery of molecular markers and related technologies, such as marker-assisted selection (MAS), has led to the appearance of a new genetic background in plant breeding. MAS would be exceedingly valuable in the cases of polygenic or quantitative disease resistance, in which the individual quantitative trait loci (QTL) would have minute effects on disease development. This review elaborately describes the availability of many molecular markers that recognize the locus of gene mapping for an understanding of the genetic background of disease resistance.
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Introduction
Cultivation of disease-resistant cultivars/varieties is an efficient factor in both experimental and commercial breeding, and disease control performed by the management of resistance genes might enhance the stability of the variety. Such resistance durability might be exceedingly beneficial to farmers as it leads to increase in yield, reduces the costs, and is environmentally friendly (Shah et al. 2017a). So far, 82 PM resistance genes have been formally cataloged on 54 loci (McIntosh et al. 2017), but most of them are race specific and are easily overcome by new Bgt isolates (Li et al. 2014). Among them, the Pm3 resistance alleles have been well categorized (Yahiaoui et al. 2004; 2006); likewise, four other genes named as Pm1, Pm3, Pm4, and Pm5 have more than one allele contributing to the resistance to powdery mildew (Yahiaoui et al. 2006). The A-genome progenitor is Triticum urartu (Ling et al. 2013). Wheat gene pool of the diploid ‘‘A’’ genome progenitor containing three closely related species, for instance, Triticum monococcum, Triticum boeoticum, and T. urartu, has valuable variability for several economically significant genes, coding resistance to powdery mildew (Singh et al. 2007; Hussien et al. 1997). Similarly, several other genes including Pm4a, Pm4b, Pm5a, Pm6, Pm16, Pm26, Pm27, Pm30, Pm31, and Pm33 have been introduced from tetraploid wheat (McIntosh et al. 2007); two new alleles of Pm1 have been introgressed from two different accessions of T. monococcum, conferring defense response to powdery mildew. Several molecular markers, including RAPD, RFLP, AFLP, expressed sequence tags (EST), and STS, have been found to be associated with more than 29 powdery mildew resistance genes on wheat chromosomes (McIntosh et al. 2007; Alam et al. 2011). Some of the above reported markers have been effectively applied in gene map-based cloning (Yahiaoui et al. 2004), MAS and gene pyramiding against powdery mildew (Liu et al. 2001). Molecular markers might help selection in the early developmental stages and might be assessed for high yield with high heritability and they can easily be found by the genetic linkage of the desirable gene group on the chromosome associated with disease resistance (Hua et al. 2009).
Sources of resistance to powdery mildew in wheat
In a report published by Marone et al. (2013), several resistance genes were transferred from diploid and tetraploid relatives of wheat, such as Triticum carthlicum Nevski (Pm6 and Pm33), Triticum timopheevii (Pm27, Pm37, PmNCAG11, and MlAG12), Triticum turgidum var. dicoccoides (MlIW170, Pm42, MlAB10, MlZec1, Pm41, Pm16, Ml3D232, PmAS846, Pm36, PmG3M, PmG16, and MlIW72), T. monococcum (Pm4d, Pm2026, NCA6Pm, Mlm2033, and PmNCA4), T. boeoticum (Boiss) (PmTb7A.1, PmTb7A.2, and Mlm80), T. urartu (Tum.) (PmU) and several Aegilops spp. (PmY212, Pm35, PmY201, Pm34, and Pm12) or from related genera, such as Elytrigia (Pm40), Secale (PmHNK54 and PmTm4), and Thinopyrum intermedium (Host) (Pm43). The confluence in the same region of QTL and the genes that derive from diverse species is the most exemplified instance along the chromosomes of the wheat genome, which leads to the hypothesis that diverse sources of resistance might have contributed to these regions. Chromosome 1A was characterized in Triticum militinae, which contains the marker Xpsp2999 (47.2 cM) (Jakobson et al. 2012), where a gene-rich region resulting MQTL4 was recognized on chromosome 2A. This region appears to have been subjected to multiple events of introgression from wild species as genes and QTL that derive from different sources were mapped (T. monococcum, Triticum aestivum, Triticum dicoccum, T. timopheevii, and T. carthilicum). There are other convergence regions in which different origins of resistance have contributed to the same chromosomal region on chromosomes 2B (T. carthlicum, T. aestivum, and Triticum dicoccoides), 5B (T. dicoccoides, T. aestivum), 5A (T. aestivum, T. monococcum, and T. militinae), and 6B (T. aestivum, T. timopheevi, and T. dicoccoides, Aegilops speltoides) (Marone et al. 2013).
So far, approximately 82 designated powdery mildew-resistant genes have been identified at 54 loci (Pm1-Pm54), including Pm1a-Pm1e at Pm1, Pm3a-Pm3g at Pm3, Pm4a-Pm4d at Pm4, Pm5e-Pm5, Pm8, Pm17, and Pm24a-Pm24b at Pm24 (Table 1, Hao et al. 2015). Another published report Zeller et al. (1993) stated that Pm3d, Pm3e, and Pm3f were identified on short arm of wheat chromosome 1A. In other report, The et al. (1979) stated that Pm4a and Pm4b have been recognized on long arm of T. dicoccum and T. carthlicum chromosome 2A, respectively. Reportedly, most of the designated host defense genes have been originated from T. aestivum and wild plants. For example, the sources of resistance genes including Pm1b and Pm25 were introduced to common wheat from T. monococcum; Pm16, Pm26, and Pm30 genes were introduced from T. turgidum sub sp. dicoccoides; Pm6 and Pm27 genes from T. timopheevii; Pm4a and Pm5a genes from T. turgidum sp. Dicoccum; Pm4b gene was introduced from T. turgidum subsp. Carthlicum; Pm5c was introduced from T. aestivum subspp. sphaerococcu; Pm7, Pm8, Pm17, and Pm20 genes were transferred from Secale cereale; Pm2 and Pm19 genes were introduced from Aegilops tauschii, Pm21 gene was transferred from Dasypyrum villosum; Pm12 and Pm32 genes were transferred from A. speltoides; and Pm29 gene was introduced from Aegilops ovate to wheat plant as described by Hsam et al. (2003). Resistance gene Pm10 to powdery mildew was recognized on wheat chromosome 1D (Tosa et al. 1987). Similarly, resistance genes Pm11, Pm14, and Pm15 to powdery mildew were recognized on small arm of wheat chromosome 6B (Table 1, Tosa and Sakai 1990; Tosa et al. 1988). Extensive molecular studies for the identification of the sources of host resistance to virulent pathogens are needed to allow effective utilization of disease resistance in wheat breeding populations for commercial use (Ma et al. 2014). Li et al. (2011) and Song et al. (2012) evaluated a large number of powdery mildew isolates in China and reported that some wheat cultivars have resistance genes to powdery mildew genes: PmYm66 linked to Ksum193 and PmHNK54 flanked by Barc5 and Gwm312 that were identified on chromosome arm 2AL in Yumai 66 and Zheng 9754, respectively (Xu et al. 2011). Powdery mildew resistance gene PmTm4 is flanked by Gwm611 and EST92 in Tangmai 4 on chromosomal arm 7BL (Tie-Zhu et al. 2008), where Pm2 was the first powdery mildew gene found on chromosomal arm 5DS and was designated as Pm2a, while the new allele Pm2b at the same locus was already reported earlier (Ma et al. 2015). The another powdery mildew resistance gene, Pm48, was observed to be located in the multi-allelic Pm2 region of the chromosome of the German cultivar Tabasco (Gao et al. 2012), which is consistent with the findings of (Mcintosh et al. 2011) who reported that it was initially designated as Pm46 and then formally re-designated as Pm48. The commonly used wheat resistance line Lankao 906, introduced from a cross between wheat and rye (Mzalenod Beer) and Xuanxi (Baofeng), was found to carry a recessive powdery mildew resistance gene located on wheat chromosome 2AL that was temporarily named PmLK906 (Niu et al. 2008). Likewise, one more temporarily named gene (TacsAetPR5) was recognized on chromosomal arm 2AL at Pm4 locus in cultivar Lankao 906 and was designated as PmLK906. Similarly, other temporary genes (PmPS5A) were introduced from T. carthlicum to common wheat (Zhu et al. 2005), and PmYm66 was introduced from common wheat (Yumai 66) (Tie-Zhu et al. 2008). Nine powdery mildew resistance genes were mapped on chromosome 2B, and four of them were designated as MlZec1, PmY39, MIAB10, and MlIw170. PmY39 was converged by hybridization between the population of Am9 and Laizhou 953. Resistance gene Pm38 was identified on wheat chromosome 7DS (Spielmeyer et al. 2005), whereas Pm39 was recognized on wheat chromosome 1BL (Table 1, Lillemo et al. 2008). Likewise, resistance gene Pm51 was identified on chromosome 2BL in wild plant Dasypyrum villosum (Zhan et al. 2014), whereas Pm57 was recognized on chromosome 2BL in Ae. searsii (Table 1, Liu et al. 2017).
Adult plant resistance
Race-specific resistance is easily recognized in the field by its qualitative monogenic inheritance and is easy to integrate into the genome of receptive plant cells. Unfortunately, this type of resistance is easily influenced by emergence of new races. The traits related to quantitative trait loci (QTL), for example, adult plant resistance (APR), are widespread in plant breeding due to their stability over a wide geographic range and time. Plant defense responses may be induced at the different stages of host development, varying with plant age or tissue ripeness, and are extremely closely associated with plant and pathogen interactions (Shah et al. 2017c; Develey-Rivière and Galiana 2007). For instance, Cowger et al. (2012) reported that APR to powdery mildew in numerous widely cultivated cultivars has an effective durability of more than four decades. Slow fungus infections and multiplication of fungal pathogens have been observed at adult plant stages (Shaner 2003). CIMMYT wheat (T. aestivum L.) lines Francolin#1 and Quaiu#3 displayed effective and stable adult plant resistance to Chinese Blumeria graminis f. sp. tritici isolates in the field (Ren et al. 2017). Other researchers, Hsam et al. (2003) found that Pm5 gene acts as a source of APR to wheat powdery mildew. Das and Griffey (1994) identified 14 chromosomes involved in the expression of APR in monosomic wheat varieties (Chinese Spring and Caribo). They also investigated the winter wheat cultivars Knox 62, Massey, and Redcoat and concluded that two to three genes with moderate to high heritability controlled APR. Similarly, the resistance to fungal development was observed on seven chromosomes at the adult plant stage of the wheat cultivar Knox 62. For example, chromosomes 5A, 7A, 4B, and 5D displayed a higher association with the resistance to fungal infections at the adult plant stage (Lan et al. 2009). In addition, powdery mildew resistance gene (MlRE) was reported to have a significant defense response to pathogen infections during the adult stage of the winter wheat cultivar RE714 because of dominant residual effects (Chantret et al. 1999). Ren et al. (2017) detected six QTL conferring APR to powdery mildew across environments, including QPm.heau-1BL (Pm39), QPm.heau-1DL, QPm.heau-2DL, QPm.heau-4BL, QPm.heau-5BL, and QPm.heau-6BS. QPm.heau-1DL is likely to be a novel QTL for resistance to powdery mildew. Besides Pm39, QPm.heau-2DL might be another co-located/pleotropic resistance gene in wheat, which maps to same position as Yr54.
Another published report revealed that Pm12, Pm16, and Pm20 genes confer most effective defense response against powdery mildew inoculation in adult plant stage (Wang et al. 2007). Based on phenotype variation only, it is hard to recognize plants with both race-specific resistance and APR to powdery mildew. However, some molecular markers associated with genes encompassing Pm1 (Hu et al. 1997); Pm2 and Pm3 (Ma et al. 1994); Pm4 (Hartl et al. 1999); Pm12 (Jia et al. 1996); Pm13 (Cenci et al. 1999); Pm21 (Qi et al. 1996) and Pm25 (Shi et al. 1998) have been reported with both race-specific resistance and APR to powdery mildew. With MAS, it is also probable to choose plants with both race-specific resistance, and APR to powdery mildew. Some molecular markers, such as SSR and SNP, were utilized for the identification of adult plant resistance genes against powdery mildew infection (Zhang et al. 2010). QTLs associated with the defense response were mapped at Pm4 locus (Muranty et al. 2009), which exhibited most influential defense response to powdery mildew infection during the adult plant stage. Zhao et al. (2013) and Purnhauser et al. (2011) identified markers that were tightly linked to Pm6 for APR. QTL associated with resistance against powdery mildew was mapped near the Pm1 locus (Chantret et al. 2001), and another QTL related to the Pm3a locus was identified for adult plant resistance (Liang et al. 2006). In addition, QTLs associated with Pm5 and Pm13 loci were mapped for APR (Chen et al. 2009). In their investigations, Muranty et al. (2009) and Lan et al. (2009) recognized and mapped QTLs for wheat adult plant resistance at or near the Pm35 and Pm43 loci, respectively.
Marker-assisted selection
Wheat molecular markers that are strongly linked to the resistance genes can be used for MAS to improve the efficacy of assortment in early generations (Gupta et al. 2010). For example, in wheat breeding programs, T. intermedium-derived barley yellow dwarf virus resistance gene Bdv2 has been transferred into commercial cultivars by using MAS (Zhang et al. 2004), but a small alien segment was found to be present. The alien-derived leaf rust resistance genes, e.g., Lr9, Lr24 and Lr47, have been introduced from Aegilops umbellulata, Thinopyrum ponticum, and A. speltoides, respectively, into other common wheat cultivars by the use of genetic markers (Nocente et al. 2007). As a result, these genes functioned as ‘perfect’ markers or were linked to wheat-derived markers.
Using the BC2F1 population of the cross KM2939/3*Shimai 15, seven molecular markers were recognized that were closely linked to the Pm2b resistance gene. Similarly, three RAPD markers associated with Pm25 could not detect the existence of Pm25 in some genetic circumstances because of the large genetic distances between the markers and Pm25 (Shi et al. 1998). Twenty years ago, it was challenging to identify all cultivars possessing Pm1 and Pm2a by the use of closely linked RFLP markers (Hartl et al. 1995), while a similar report from that time detected the presence of Pm2a using an STS marker that was converted from the corresponding RFLP marker linked to Pm2a (Mohler and Jahoor 1996). Later, Gupta et al. (2010) stated that for MAS it was essential to check the accessibility of the closely associated markers in various genetic backgrounds. Introducing Pm2b into various vulnerable cultivars by MAS has been performed for many years, and an advanced line has been attained, and several transgenic lines showed resistance to powdery mildew at both the seedling and adult stages (Gupta et al. 2010).
Molecular markers
The following molecular markers can be useful for the detection of disease resistance genes: (a) restriction fragment length polymorphisms (RFLPs); (b) simple-sequence repeats (SSRs); (c) amplified fragment length polymorphisms (AFLPs); and (d) single nucleotide polymorphism (SNP). The above reported markers provide a polymorphic detection platform; they are easily applicable for disease resistance detection in a population, while owing to co-dominant inheritance, these molecular markers are commonly used in molecular breeding for genetic mapping (Shah et al. 2017b). For example, using wheat cultivar Chancellor as a recurrent parent, Briggle and Sears (1966) developed NILs for the assembling of powdery mildew resistance genes, including Pm1, Pm2, Pm3, and Pm4a, which was confirmed by using RFLP markers. An RFLP marker (Whs179) was associated with the Pm3 locus and mapped at the distance of 1.9 cM (Hartl et al. 1993), and RFLP marker (BCD1434) was mapped at a distance of 1.3 cM from the Pm3b locus (Ma et al. 1994). Likewise, they also reported that the RFLP markers BCD1231-2A and CDO678-2A were associated with the Pm4a gene and mapped at a distance of 1.5 cM.
The RAPD marker OPF12650 was mapped at a distance of 5.4 cM from the Pm1 locus (Hu et al. 1997). Likewise, the Pm21 gene was recognized and mapped by using the RAPD marker OPH17-1900 on chromosome arm 6VS in common wheat (Qi et al. 1996). Two Dasypyrum villosum accessions, D.v#2 and No. 1026 from England and Russia, respectively, contain Pm21 on chromosome 6V#2S and PmV on chromosome 6V#4S (Li et al. 2017). These both genes confer high resistance to powdery mildew in wheat. Even though several molecular markers have been developed to detect Pm21 and PmV, only the MBH1 marker can simultaneously detect both Pm21 and PmV. It is noteworthy that Neu et al. (2002) converted the RAPD marker UBC638 into a dominant SCAR marker (STS638) and used for the identification of the Pm1 resistance locus on wheat chromosome. However, RAPDs technology was not used frequently due to the limited influence of the genetic background for powdery mildew resistance as well as due to the minor levels of polymorphism among the populations.
In this respect, simple-sequence repeats (SSR)-based markers are a convenient and commonly used technique as due to the detection of high levels of polymorphism among the populations. The microsatellite marker (PSP2999) was found to be linked with the Pm3 locus that conferring defense response to powdery mildew (Bougot et al. 2002). Later, Huang et al. (2003) mapped Pm5e on chromosome 7BL using SSR marker Xgwm1267. Another example is the study of Hua et al. (2009), in which the authors used two SSR markers (Xbarc7 and Xbarc55) that were strongly associated with Pm42 gene, with distances of 10.9 and 10.1 cM, respectively. Two genes (Pm42 and MlIW170) were identified by using two SSR markers, Xbarc7 and Xbarc55 (Liu et al. 2012), and these two genes can be related to the same gene clusters (Marone et al. 2013). Two reported genes including PmHNK54 and PmYm66 were detected by the SSR markers Gwm312 and Barc5 on chromosome 2AL in Zheng 9754 and Yumai 66, respectively (Xu et al. 2011). The defense responses of several wheat cultivars to powdery mildew were established in China (Song et al. 2012; Li et al. 2011). PmLX66, PmW14, and PmZ155 genes on chromosome 5DS in wheat (Liangxing 66) were found to be responsible for the defense against powdery mildew (Song et al. 2014; Huang et al. 2012; Sun et al. 2015). Successful transfer of PmTb7A.1 and PmTb7A.2 resistance genes is possible by using susceptible T. durum as a backcross linking species, and the obtained F1 can be crossed with hexaploid wheat for the transfer of the two powdery mildew resistance genes (PmTb7A.1 and PmTb7A.2) into breed wheat (Chhuneja et al. 2012).
For example, associations of Pm34 with Barc144 and Barc177 (Fig. 3, Miranda et al. 2006), of Pm-M53 with Gwm292 and Wmc289 (Li et al. 2011), and of Pm35 with Xcfd26 at a distance of 11.9 cM (Miranda et al. 2007) have been revealed on chromosome arm 5DL, which, according to the published maps, are positioned at the distances of approximately 92, 55, and 41 cM from Pm2b, respectively (Somers et al. 2004). Pm2a was found to be associated with Xcfd81 (SSR marker) with a genetic distance of 2.0 cM on chromosome 5DS in the wheat landrace Ulka and at a distance of 3.3 cM from Pm2b (Qiu et al. 2006). Temporarily designated powdery mildew resistance genes were identified on chromosome arm 5DS containing MlBrock, which is co-segregated with Cfd81 in the Brock cultivar (Li et al. 2009). Several genes, such as PmLX66, were mapped by Cfd81 and SCAR203 in the Chinese wheat cultivar/variety Liangxing 66 (Huang et al. 2012), PmD57-5D was identified and mapped by Mag6176 and Gwm205 in line D57 (Ma et al. 2011), PmX3986-2 was identified by Cfd81 and SCAR112 in an indigenous germplasm (Ma et al. 2014), and Pm46 was recognized by Mp510 and Gwm205 in the German cultivar/variety Tabasco (Gao et al. 2012). The resistance genes Mlbrock and PmD57-5D are same in comparison with Pm2a (Li et al. 2009; Ma et al. 2011), PmX3986-2, Pm46, and PmLX66 are at distances of 0.7, 1.8, and 4.1 cM, respectively, from Pm2b based on the maps published (Gao et al. 2012; Huang et al. 2012). To clarify the associations between the above-mentioned genes, wheat genotypes, including KM2939, Ulka/8*Cc (with Pm2a), Tabasco (with Pm46), Liangxing 66 (with PmLX66), and X3986-2 (with PmX3986-2) were verified by 27 Bgt isolates (Ma et al. 2015). Their inoculation results showed that KM2939 conferred a response pattern that is dissimilar from that of lines with Pm2a, PmLX66, Pm46, and PmX3986-2 (Ma et al. 2015). Hence, reportedly, Pm2b showed an association, which was different from that of Pm2a, Pm46, PmLX66, and PmX3986-2. It is noteworthy that they developed a near-isogenic line (NIL) using the susceptible wheat cultivar Shimai (recurrent parent) and applied 284 SSR markers across the population to measure the genetic polymorphism of selected lines to the backcross parent. According to the findings of a published report, the SSR marker Xgwm337 and the AFLP marker locus XE35M59-407 and XE34/M51-346 was found to be linked to Pm24 (Fig. 1, Huang et al. 2000) in Egyptian wheat cultivars, whereas two SSR markers (Xgwm332 and Xwmc790) were noted to be linked to Pm37 (Fig. 3, Perugini et al. 2008). Four other SSR markers (Xbarc7, Xbarc13, Xbarc55, and Xwmc441) were associated with the Pm5055 gene with the genetic distances of 23, 23, 23.9, and 10.6 cM, respectively (Saidou et al. 2016). On the other hand, PmAF7DS was mapped on the short arm of chromosome 7D with a distance to a 14.6 cM interval and was flanked by the SSR markers Xgwm350a and Xbarc184 on its distal and proximal sides (Reddy et al. 2016). Reportedly, two genes including PmTb7A.1 and PmTb7A.2 were established to be associated between wPt4553 and Xcfa2019 markers at a distance of 4.3 cM (Elkot et al. 2015).
Powdery mildew resistance loci were mapped with the utilization of high-density SNP markers in the RILs of Shanghai3/Catbird x Naxos and confirmed the consequences in a various genetic background; Soru#1 × Naxos (Susanne et al. 2017). They genotyped both populations with the Illumina iSelect 90 K wheat chip, and unified linkage maps developed by addition of previously genotyped DArT and SSR markers. In their reports, they identified a sum of 12 QTL with the novel linkage maps by utilizing SNP and DArT markers for powdery mildew resistance in the RILs of Shanghai3/Catbird x Naxos, of which eight were introduced from Naxos. A report published by Lu et al. (2012) stated that using SSR and DArT markers in the mapping population Shanghai3/Catbird x Naxos, discovered numerous important powdery mildew-resistant QTLs from Naxos. Similarly, they reported that several QTLs on chromosome 1AS and 2BL were more accurately mapped by utilizing SNP markers that facilitated finding of novel QTL on chromosome 1AL, 2AL, 5AL, and 5AS. Likewise, recently four powdery mildew resistance QTLs were recognized in the Soru#1 × Naxos population performed by Susanne et al. (2017), of which three had resistance to powdery mildew from Naxos. By using SNP-derived markers Bwm20, Bwm21, and Bwm25, Ma et al. (2016) flanked a temporarily designated gene (PmFG) at genetic distances of only 0.3, 0.3, and 0.5 cM, respectively, in the F2 population. Genetic analysis confirmed that a qualitative gene designated as PmFG, deliberated resistance to powdery mildew in FG-1 population at the seedling stage.
Numerous AFLP markers were found to be very nearly associated with Pm1c, and among them one AFLP marker XS19M22-325/200 was specific for Pm1c (Hartl et al. 1999), whereas in two wheat crosses segregating population, AFLP markers XE39M58-77 and XE34M53-439 on chromosome 7A for Pm22 (Fig. 2) and Pm1c (Fig. 1), respectively, specified that Pm22 gene, which had previously been consigned to chromosome 1D in the Italian wheat variety (Virest) (Peusha et al. 1996), was an allele of the complex Pm1 locus. Pm22 was therefore re-designated as Pm1e (Singrun et al. 2003). Two AFLP markers, XAG/AG-228 and XCA/CT-355, were linked to Pm17 with genetic distances of 2.4 and 1.5 cM, respectively (Fig. 1, Hsam et al. 2000). In double-haploid wheat population, Pm3g was mapped by using RFLP markers XGli-A5 at distance of 5.2 cM from Pm3g gene to the distal region of the short arm of chromosome 1AS (Sourdille et al. 1999), whereas using SSR marker Xgwm905, Pm3h was nearly linked on short arm of wheat chromosome 1A at distance of 3.7 cM from the gene (Fig. 1, Huang and Roder 2004). A report published by Liu et al. (1998) stated that fragment using STS primers developed from the sequence of the RFLP probe BCD1231 produced a particular band which was existing in all 11 tested 214 varieties/cultivars and lines encompassing the Pm4a and Pm4b alleles, whereas using microsatellite marker Xbarc122, Pm4b was nearly associated with wheat chromosome 2AL at distance of 2.0 cM from the gene (Hao et al. 2015). Pm6 has been extensively and effectively used in wheat powdery mildew resistance breeding as described by Bennett (1984). It was transferred to wheat from wild plant (T. timopheevii) by recombination between the B genome of hexaploid wheat and the G genome of T. timopheevii. RFLP marker xbcd135 was mapped at a distance of 1.6 ± 1.5 cM from Pm6, whereas two RFLP markers Xbcd307 and Xbcd266 were mapped at a distance of 1.6 ± 1.5 and 4.8 ± 2.6 cM from Pm6, respectively (Tao et al. 2000). Three SSR markers associated with Pm16 on short arm of wheat chromosome 5BS in F2 population (Chancellor’(susceptible) × ’70,281’(resistant)) (Chen et al. 2005), whereas Pm17 was nearly mapped with RFLP marker Xiag95 on short arm of Secale cereale chromosome 1RS (Hsam et al. 2000). Pm23 gene was recognized in the hexaploid wheat line from 81 to 7241 and originally assigned to wheat chromosome 5A and was repositioned on long arm of chromosome 2A with the help of microsatellite markers (Fig. 1, Hao et al. 2008). Three genes encompassing Pm12, Pm20, and Pm27 and one temporarily designated gene such as PmG3M were found to be recognized on chromosome 6B. Pm12 was accumulated into line #31 from A. speltoides, and was positioned on the chromosome 6BS-6SS.6SL (Jia et al. 1996). Likewise Pm27 was introduced from T. timopheevii to hexaploid wheat, and positioned on a translocation fragment close the centromeric region of chromosome 6B (Järve et al. 2000). Nevertheless, two other genes, e.g., PmG3M and Pm20, were assigned to the same deletion bin as PmA2K (Fig. 2, Jia et al. 1996). PmG3M was located at the distance of 23.3 cM to the marker Xbarc134 (Xie et al. 2012), while PmA2K was located to proximal to the marker at the distance of 1.2 cM; hence, the linkage distance between the two genes is about 24.5 cM. However, PmG3M was introduced from wild emmer T. dicoccoides, while PmA2K derived from hexaploid wheat. Pm26 gene was accumulated from wild emmer (T. turgidum) to common wheat and co-segregated with a polymorphic locus detected by the RFLP marker Xwg516, 49.4 cM from the terminal marker Xcdo456 (Rong et al. 2000). Linkage analysis exhibited that the Pm29 in Pova was particularly located on chromosome 7DL nearly associated with one RFLP and three SSR markers. Three microsatellite markers on the long arm of chromosome 6A were linked in a BC2F3 population, in which the SSR locus Xpsp3029-6A was closely linked (0.6 cM) to Pm31 (Fig. 2, Xie et al. 2003), whereas two RAPD markers, OPX061050 and OPAG04950 were found to be linked to Pm25 located on chromosome 1A (Shi et al. 1998). The SSR marker Xgwm159/500 were reported to be associated with the powdery mildew resistance gene Pm30 on short arm of wheat chromosome 5BS with a genetic distance of 5–6 cM (Fig. 3, Liu et al. 2002), whereas Pm36 came from T.turgidum in durum wheat and the genetic association of the five AFLP markers were linked with XP43M32(250) at the distance of 1.1 cM from Pm36 (Blanco et al. 2008).
Conclusions and future prospects
Phylogeny of mapmaking programs along with the improvement or development of high-density SNP chips also make it practicable to build integrated maps with various marker types, giving an even enhanced map resolution and making it probable to exchange formerly used DArT, SSR, and RFLP with SNP markers. The SNP markers are easygoing to use in genotyping with today’s technology platforms, for example, KASP (Semagn et al. 2014). Significant breakthrough in the genomic of wheat research was established in 2012 with the achievement of de novo sequencing of common wheat, Chinese Spring variety (CS42), enabling improvements in genomic research into the genus Triticum and giving visions into the polyploidization of wheat. A report published by Brenchley et al. (2012) stated that genome of wheat was sequenced by utilizing Roche 454 pyro-sequencing technology, e.g., GS FLX Titanium and GS FLX + Platforms.
One of the most important targets for a breeder is to develop a cultivar which is potentially resistance to disease infection. Substantial advancements have been made during the last two decades in detecting marker–trait associations and their use in MAS for wheat improvement. So far, most of the characters used for the development through MAS are simple and confer the disease defense response and these marker–trait associations will be the key object of attention in prospects wheat breeding efforts, including those by the use of MAS. The application and development of genetic markers will remain an effective approach in the classification or selection of target genes and the detection of their locus on the chromosome. In addition, the use of such markers of gene sequences will enable the recognition and distribution of innovative genes for the development of wheat disease resistance traits. The most efficient factor in the future achievements of wheat breeding will be the strategies and novelties that come through the utilization of molecular approaches and the plant breeders will easily gain targets and recognize effective germplasm for analysis by using advanced molecular technologies. These molecular technologies will support the further development, and it seems feasible that novelties in breeding approaches will be effective factors to the future role of MAS. There are several hurdles in wheat development due to the difficulties of working with three genomes; however, these challenges can be overcome, and improved genetic traits can be obtained by the utilization and development of strongly associated genetic markers for the recognition of new resistance genes to diseases. A large set of SNPs (132,000 SNPs) in A, B, and D genes will enhance future studies aimed at identifying QTLs and discovering associations of traits.
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Acknowledgements
This work was supported by Grants from The National Key Research and Development Program of China (2017YFD0100804), the Agriculture Research System (CARS-03), the Introduced talents team in Colleges and Universities in Anhui Province, and the Collaborative Innovation Center of Food Crops in Anhui Province.
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Shah, L., Rehman, S., Ali, A. et al. Genes responsible for powdery mildew resistance and improvement in wheat using molecular marker-assisted selection. J Plant Dis Prot 125, 145–158 (2018). https://doi.org/10.1007/s41348-017-0132-6
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DOI: https://doi.org/10.1007/s41348-017-0132-6