Molecular Pathogens 2024, Vol.15 http://microbescipublisher.com/index.php/mp © 2024 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher.
Molecular Pathogens 2024, Vol.15 http://microbescipublisher.com/index.php/mp © 2024 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher. Publisher MicroSci Publisher Editedby Editorial Team of Molecular Pathogens Email: edit@mp.microbescipublisher.com Website: http://microbescipublisher.com/index.php/mp Address: 11388 Stevenston Hwy, PO Box 96016, Richmond, V7A 5J5, British Columbia Canada Molecular Pathogens (ISSN 1925-1998) is an open access, peer reviewed journal published online by MicroSciPublisher. The journal is committed to publishing and disseminating all the latest and outstanding research articles, letters and reviews in all areas of molecular pathogens. The range of topics including isolation and identification of emerging pathogens viruses, pathogen-host interactions, genetics and evolution, genomics and gene regulation, proteomics and signal transduction, glycomics and signal recognition, virulence factors and vaccine design and other topical advisory subjects. All the articles published in Molecular Pathogens are Open Access, and are distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. MicroSci Publisher uses CrossCheck service to identify academic plagiarism through the world’s leading plagiarism prevention tool, iParadigms, and to protect the original authors’ copyrights. MicroSci Publisher is an international Open Access publisher specializing in microbiology, bacteriology, mycology, molecular and cellular biology and virology registered at the publishing platform that is operated by Sophia Publishing Group (SPG), founded in British Columbia of Canada.
Molecular Pathogens (online), 2024, Vol. 15 ISSN 1925-1998 http://microbescipublisher.com/index.php/mp © 2024 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher. Latest Content 2024, Vol.15, No.3 【Review Article】 Developing Durable Resistance to Wheat Diseases: Integration of Molecular Breeding Techniques 106-118 WeiWang DOI: 10.5376/mp.2024.15.0011 【Research Report】 The Role of Viruses in Sugarcane Yield Reduction: A Case Study onSugarcane Yellow Leaf Virus 119-128 Chunyang Zhan DOI: 10.5376/mp.2024.15.0012 【Feature Review】 Threats to Honeybee Populations: Pathogens, Pesticides, and Environmental Changes 129-141 JunLi DOI: 10.5376/mp.2024.15.0013 Collection and Functional Verification of Pine Disease Resistance Gene Resources 142-154 Minghui Zhao, Zonghui Liu, Xiazhen Huang DOI: 10.5376/mp.2024.15.0014 【Review and Progress】 Research Progress on Powdery Mildew in Cucurbitaceae Plants, A Systematic Review 155-169 Liangrong Jiang, Xianchao Xiao DOI: 10.5376/mp.2024.15.0015
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 106 Review Article Open Access Developing Durable Resistance to Wheat Diseases: Integration of Molecular Breeding Techniques WeiWang Institute of Life Science, Jiyang College of Zhejiang A&F University, Zhuji, 311800, Zhejiang, China Corresponding email: wei.wang@jicat.org Molecular Pathogens, 2024, Vol.15, No.3 doi: 10.5376/mp.2024.15.0011 Received: 28 Feb., 2024 Accepted: 15 Apr., 2024 Published: 10 May, 2024 Copyright © 2024 Wang, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Wang W., 2024, Developing durable resistance to wheat diseases: integration of molecular breeding techniques, Molecular Pathogens, 15(3): 106-118 (doi: 10.5376/mp.2024.15.0011) Abstract Wheat production is critically threatened by various diseases, necessitating the development of cultivars with durable resistance. This study explores the integration of molecular breeding techniques to enhance disease resistance in wheat. Advances in genetic breeding methods, including transgenic breeding, molecular marker-assisted selection, gene pyramiding, gene silencing, and gene editing, have significantly contributed to the development of wheat cultivars with multiple resistance traits. The continuous emergence of new pathogen races, particularly rust pathogens, underscores the need for innovative strategies combining genomic selection, genome editing, and phenotypic evaluations to develop high-quality, resistant wheat varieties. Additionally, the impact of climate change on disease prevalence necessitates the breeding of wheat varieties with multi-disease resistance that remains effective under varying environmental conditions. This study highlights the importance of integrating modern genomic tools and traditional breeding approaches to achieve sustainable wheat production with enhanced disease resistance. Keywords Molecular breeding; Disease resistance; Wheat cultivars; Genomic selection; Climate resilience 1 Introduction Wheat, a staple food crop globally, is constantly threatened by a variety of diseases caused by pathogens such as fungi, bacteria, and viruses. Among the most significant diseases are rusts (leaf rust, stem rust, and stripe rust), powdery mildew, and various blights and smuts. These diseases can lead to substantial yield losses, affecting global food security and economic stability (Johnson, 2004; Hafeez et al., 2021; Mapuranga et al., 2022). The continuous evolution of pathogen virulence poses a persistent challenge to wheat production, necessitating the development of effective and sustainable disease management strategies (Brown, 2015; Luo et al., 2023). Durable resistance refers to the ability of a plant to resist disease over a prolonged period and across various environmental conditions, despite the presence of the pathogen. This type of resistance is crucial for sustainable wheat production as it reduces the reliance on chemical controls, which can lead to environmental degradation and the development of resistant pathogen strains (Brown, 2015; Mapuranga et al., 2022). Durable resistance is often achieved through the integration of multiple resistance genes, which can provide broad-spectrum and long-lasting protection against a range of pathogens (Lowe et al., 2011; Jabran et al., 2023). The development of wheat cultivars with durable resistance is essential for ensuring food security and reducing the economic impact of wheat diseases (Hafeez et al., 2021; Kozub et al., 2022). This study provids a comprehensive overview of the recent advances in molecular breeding techniques for developing durable resistance to wheat diseases. It will discuss the various genetic and molecular approaches, including marker-assisted selection, gene pyramiding, and genome editing, that have been employed to enhance disease resistance in wheat. Additionally, the study will highlight the challenges and future prospects of integrating these techniques into wheat breeding programs to achieve sustainable disease management. By synthesizing current knowledge and identifying gaps in the literature, this study seeks to guide future research and breeding efforts towards the development of wheat cultivars with durable resistance to multiple diseases.
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 107 2 Overview of Wheat Diseases 2.1 Common diseases affecting wheat Wheat, a staple food crop globally, is susceptible to a variety of diseases that significantly impact its yield and quality. Among the most prevalent and damaging diseases are the rusts, including leaf rust (Puccinia triticina), stem rust (Puccinia graminis f. sp. tritici), and stripe rust (Puccinia striiformis) (Maré et al., 2020; Figlan et al., 2020; Mapuranga et al., 2022). These rust diseases are notorious for their ability to rapidly evolve and overcome resistance genes, posing a continuous threat to wheat production (Luo et al., 2021; Mapuranga et al., 2022). Another significant disease is Fusariumhead blight (FHB), caused by Fusariumspecies, which not only reduces yield but also contaminates the grain with mycotoxins, making it unsafe for consumption (Maré et al., 2020). Additionally, wheat is affected by other fungal diseases such as septoria, eyespot, and powdery mildew, which further complicate disease management strategies (Johnson, 2004; Summers and Brown, 2013). 2.2 Impact on wheat production The impact of these diseases on wheat production is profound. Rust diseases alone can cause yield losses of up to 70% in severe epidemics, leading to significant economic losses and food insecurity (Luo et al., 2021; Mapuranga et al., 2022). The continuous emergence of new pathogen races exacerbates this problem, as previously effective resistance genes become obsolete (Babu et al., 2020; Mapuranga et al., 2022). Fusarium head blight not only reduces yield but also affects grain quality due to mycotoxin contamination, which poses health risks to humans and animals (Maré et al., 2020). The economic burden of these diseases is substantial, as farmers often resort to chemical control methods, which increase production costs and can have adverse environmental effects (Figlan et al., 2020; Luo et al., 2023). Moreover, the reliance on fungicides can lead to the development of resistant pathogen strains, further complicating disease management (Luo et al., 2023). 2.3 Traditional control methods Traditional control methods for wheat diseases have primarily relied on the use of chemical fungicides and the development of resistant cultivars through conventional breeding techniques. Chemical control, while effective, is not sustainable in the long term due to the high costs, environmental impact, and the potential for pathogens to develop resistance (Figlan et al., 2020; Luo et al., 2023). Conventional breeding for disease resistance has been a cornerstone of wheat disease management. This approach involves selecting and cross-breeding wheat varieties that exhibit resistance to specific diseases. Over the years, numerous resistance genes have been identified and incorporated into commercial wheat cultivars (Maré et al., 2020; Mapuranga et al., 2022; Jabran et al., 2023). However, the effectiveness of these resistance genes is often short-lived due to the rapid evolution of pathogen virulence (Mapuranga et al., 2022). To address these challenges, integrated disease management strategies are being developed. These strategies combine the use of resistant cultivars, chemical control, and agronomic practices such as crop rotation and residue management to reduce disease pressure (Figlan et al., 2020; Mapuranga et al., 2022). Additionally, advances in molecular breeding techniques, such as marker-assisted selection (MAS), quantitative trait loci (QTL) mapping, and genome editing, are being employed to develop wheat varieties with durable resistance to multiple diseases (Figure 1) (Babu et al., 2020; Jabran et al., 2023; Luo et al., 2023). Wheat diseases pose a significant threat to global wheat production, necessitating the development of effective and sustainable control methods. While traditional control methods have provided some relief, the integration of advanced molecular breeding techniques holds promise for developing wheat cultivars with durable resistance to a broad spectrum of diseases. This integrated approach is essential for ensuring the long-term sustainability of wheat production and global food security.
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 108 Figure 1 The regular flow charts of molecular marker-assisted breeding programs involved in wheat cultivar improvements against biotic stresses (Adopted from Luo et al., 2023) Image caption: The near-isogenic lines developed from conventional hybrid breeding programs were employed for identification and mapping the resistance genes by adopting the diverse molecular markers, and many dominant genes and QTLs had been mapped on wheat chromosomes. Following that, many candidate genes or QTL allenes had been isolated from the wheat germplasms or its donor species with map-based cloning. Most wheat resistance genes belong to the NBS-LRR family, with the Fhb7 gene encoding a protein with Glutathione S-transferase. Yrs, stripe rust resistance genes; Lrs, leaf rust resistance genes; Sr, stem rust resistance genes; Pms, powdery mildew resistance genes; Dns, Russian wheat aphid Diuraphis noxia resistance genes; Gbs, greenbug Schizaphis graminumresistance genes; Sas, English grain aphid Sitobion avenae resistance genes; QFhbs, scab resistance QTLs; QRps, bird cherry-oat aphidRhopalosiphum padi resistance QTLs; QGb, green (Adopted from Luo et al., 2023) 3 Principles of Molecular Breeding 3.1 Definition and techniques Molecular breeding refers to the application of molecular biology tools to enhance the efficiency and precision of plant breeding. This approach leverages genetic information to select desirable traits, thereby accelerating the development of new cultivars with improved characteristics. Key techniques in molecular breeding include marker-assisted selection (MAS), quantitative trait loci (QTL) mapping, genome-wide association studies (GWAS), and gene editing technologies such as CRISPR/Cas9. Marker-assisted selection (MAS) utilizes molecular markers linked to specific traits to identify and select plants that carry desirable genes. This method allows for the early selection of traits at the seedling stage, significantly reducing the time and cost associated with traditional breeding methods (Miedaner and Korzun, 2021; Jabran et al., 2023). QTL mapping involves identifying regions of the genome associated with quantitative traits, which are often controlled by multiple genes. This technique is particularly useful for traits like disease resistance, which are influenced by several genetic factors (Figure 2) (Jabran et al., 2023). Genome-wide association studies (GWAS) analyze the entire genome to find genetic variations associated with specific traits. This method provides a comprehensive understanding of the genetic architecture of complex traits and helps in identifying new genes for breeding programs (Jabran et al., 2023). Gene editing technologies, such as CRISPR/Cas9, allow for precise modifications of the plant genome, enabling the introduction or removal of specific genes to enhance disease resistance and other desirable traits (Mapuranga et al., 2022; Jabran et al., 2023). 3.2 Advantages over traditional breeding Molecular breeding offers several advantages over traditional breeding methods. One of the primary benefits is the increased speed and efficiency of developing new cultivars. Traditional breeding can take many years to achieve desired traits due to the need for multiple generations of crossing and selection. In contrast, molecular breeding techniques like MAS and gene editing can significantly shorten this timeline by allowing for the direct selection of plants with the desired genetic makeup (Luo et al., 2023; Jabran et al., 2023).
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 109 Figure 2 Scheme of marker-assisted selection (MAS) and identification of quantitative trait loci (QTLs) involved in wheat disease resistance (Adopted from Jabran et al., 2023) Image caption: 1: Biparental mapping population development, i.e., F2 plants, NILs, RILs, BILs, etc., segregating for disease resistance. 2: Precise phenotyping for resistance scaling to a specific pathogen. 3: Genomic DNA isolation from selected plants. 4-6: Evaluation of genome-wide distributed polymorphic DNA markers and construction of linkage maps. 7, 8: Statistical modeling of linkage groups using phenotypic-genotypic data followed by mapping of resistance-associated QTLs (Adopted from Jabran et al., 2023) Another advantage is the precision and accuracy of trait selection. Traditional breeding relies on phenotypic selection, which can be influenced by environmental factors and may not always accurately reflect the plant's genetic potential. Molecular markers and genomic tools provide a more reliable means of selecting for specific traits, reducing the risk of selecting undesirable characteristics (Miedaner and Korzun, 2021; Jabran et al., 2023). Molecular breeding also enables the combination of multiple resistance genes into a single cultivar, enhancing the durability of disease resistance. For example, the use of gene pyramiding, where multiple resistance genes are combined, has been shown to provide more robust and long-lasting resistance to diseases like rust and Fusarium head blight in wheat (Maré et al., 2020; Luo et al., 2021). This approach is particularly important in combating evolving pathogens that can quickly overcome single-gene resistance (Maré et al., 2020; Luo et al., 2021). 3.3 Challenges and limitations Despite its many advantages, molecular breeding faces several challenges and limitations. One of the main challenges is the complexity of the plant genome and the polygenic nature of many important traits. Identifying and manipulating multiple genes that contribute to a single trait can be difficult and time-consuming (Miedaner and Korzun, 2021; Jabran et al., 2023). Additionally, the interactions between different genes and their combined effect on the phenotype are not always well understood, complicating the breeding process (Lowe et al., 2011). Another limitation is the cost and technical expertise required for molecular breeding. Advanced techniques like genome sequencing and gene editing are expensive and require specialized equipment and knowledge. This can be a barrier for smaller breeding programs or those in developing countries with limited resources (Miedaner and Korzun, 2021; Mapuranga et al., 2022).
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 110 There are also regulatory and public acceptance issues associated with some molecular breeding techniques, particularly those involving genetic modification. The use of transgenic plants, where genes from other species are introduced, is subject to strict regulations and can face public resistance due to concerns about safety and environmental impact (Luo et al., 2021; 2023). Even non-transgenic methods like CRISPR/Cas9 can face regulatory hurdles, depending on the country and the specific modifications made (Mapuranga et al., 2022; Jabran et al., 2023). The continuous evolution of pathogens poses a significant challenge to maintaining durable resistance. Pathogens can quickly adapt to overcome resistance genes, necessitating ongoing efforts to identify and deploy new resistance genes. This requires a dynamic and flexible approach to breeding, incorporating the latest genomic tools and knowledge to stay ahead of evolving threats (Hafeez et al., 2021; Mapuranga et al., 2022). While molecular breeding offers significant advantages over traditional methods, it also presents challenges that must be addressed to fully realize its potential. Continued research and innovation in molecular techniques, along with collaboration between researchers, breeders, and policymakers, are essential to overcome these challenges and develop durable disease-resistant wheat cultivars. 4 Genetic Basis of Disease Resistance 4.1 Resistance genes and pathways The genetic basis of disease resistance in wheat involves a complex interplay of major and minor genes, each contributing to the plant's ability to fend off pathogens. Major resistance genes, often referred to as R genes, typically provide high levels of resistance but are vulnerable to being overcome by evolving pathogen races. For instance, genes such as Lr34/Yr18 and Yr36 have been identified as crucial for providing resistance to rust diseases in wheat (Merrick et al., 2011; Mapuranga et al., 2022). These genes encode proteins that are involved in various defense mechanisms, including the production of pathogenesis-related proteins and the activation of defense signaling pathways (Mapuranga et al., 2022). On the other hand, minor genes contribute to quantitative resistance, which is generally more durable but involves a more complex genetic architecture. This type of resistance is controlled by multiple quantitative trait loci (QTL) scattered across the genome, each contributing a small effect (Miedaner et al., 2020; Merrick et al., 2021). For example, resistance to Fusarium head blight (FHB) in wheat is governed by several QTL, such as Fhb1 and Qfhs.ifa-5A, which have been successfully integrated into elite breeding material (Figure 3) (Miedaner and Korzun, 2012). The integration of both major and minor genes is essential for developing wheat cultivars with durable resistance to multiple diseases (Luo et al., 2023). 4.2 Marker-assisted selection Marker-assisted selection (MAS) has revolutionized the breeding of disease-resistant wheat by allowing for the precise selection of resistance genes at the seedling stage, thereby reducing costs and increasing efficiency (Miedaner and Korzun, 2012). MAS is particularly effective for detecting single-major gene resistance, such as the rust resistance genes Lr34 and Yr36, and the eyespot resistance gene Pch1 (Miedaner and Korzun, 2012). However, its application in quantitative disease resistance is more challenging due to the small effects of individual QTL and the prevalence of QTL-background effects (Miedaner and Korzun, 2012; Merrick et al., 2021). Despite these challenges, MAS has been successfully applied in practical breeding programs. For instance, the integration of rust resistance genes Lr34/Yr18 and Lr46/Yr29 into the Australian wheat cultivar 'Stylet' significantly improved its resistance to leaf rust and stripe rust (Kuchel et al., 2007). Similarly, the pyramiding of powdery mildew resistance genes Pm2, Pm4a, and Pm21 into the wheat cultivar 'Yang047' demonstrated the potential of MAS in combining multiple resistance traits (Liu et al., 2000). The future of MAS looks promising with the advent of high-throughput genotyping platforms and chip-based technologies, which are expected to overcome current limitations and open new avenues for molecular-based resistance breeding (Miedaner and Korzun, 2012).
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 111 Figure 3 Heatmap Analysis of Wheat Varieties Genotypes (Adopted from Merrick et al., 2021) Image caption: Heat map and hierarchical clustering for lines in the diversity panel (DP) lines and breeding lines (BL) populations for the major rust markers: IWB12603(Qyr.wpg-1B.1), KASP(Lr68), Xpsp3000(Yr10), and KASP(Yr17). Genotype: 0, homozygous wild-type allele; 1, heterozygous with both alleles present; 2, homozygous resistant allele 4.3 Genomic selection Genomic selection (GS) represents a significant advancement over traditional MAS by utilizing genome-wide marker coverage to predict the genetic value of breeding lines for complex traits like disease resistance (Poland and Rutkoski, 2016; Merrick et al., 2021). GS models incorporate both major and minor genes, making them particularly suitable for breeding programs targeting quantitative resistance (Merrick et al., 2021). For example, GS has been shown to achieve high prediction accuracy for stripe rust resistance in wheat, outperforming traditional MAS methods (Merrick et al., 2021). The implementation of GS in breeding programs can accelerate the development of disease-resistant varieties by reducing the selection cycle length. This is particularly beneficial for traits like adult plant resistance (APR), which require multiple seasons to phenotype accurately (Rutkoski et al., 2011). A proposed GS-based breeding scheme for stem rust resistance in wheat suggests that cycle time can be reduced by up to twofold, facilitating the pyramiding of major and APR genes (Rutkoski et al., 2011). Additionally, the integration of GS with other molecular breeding techniques, such as genome editing and phenotypic evaluations, can further enhance the development of high-quality wheat varieties with durable resistance to multiple pathogens (Miedaner et al., 2020; Mapuranga et al., 2022). In summary, the integration of molecular breeding techniques, including MAS and GS, offers a robust framework for developing wheat cultivars with durable disease resistance. By leveraging the genetic basis of resistance, these techniques can significantly improve the efficiency and effectiveness of breeding programs, ultimately contributing to sustainable wheat production worldwide. 5 Integration of Molecular Techniques in Breeding Programs 5.1 Combining conventional and molecular approaches The integration of conventional and molecular breeding techniques has become a cornerstone in developing
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 112 durable resistance to wheat diseases. Traditional breeding methods, such as direct hybridization, backcrossing, and selection, have been instrumental in introducing desirable traits, including disease resistance, into wheat varieties. However, these methods are often time-consuming and limited by the complexities of screening for multiple stress tolerance traits simultaneously (Mondal et al., 2016). Molecular breeding techniques, including marker-assisted selection (MAS), gene pyramiding, and genome editing, have significantly accelerated the breeding process. MAS, for instance, allows for the precise targeting of resistance genes at the seedling stage, thereby reducing the time and cost associated with phenotypic selection (Miedaner and Korzun, 2012). Gene pyramiding, which involves stacking multiple resistance genes, has been shown to enhance the durability and spectrum of disease resistance in wheat (Luo et al., 2021). The combination of these molecular techniques with conventional breeding methods has led to the development of wheat cultivars with enhanced resistance to a variety of pathogens, including rusts, blotch diseases, and powdery mildew (Hafeez et al., 2021). Despite these advancements, challenges remain. The continuous emergence of new pathogen races with novel virulence factors necessitates ongoing efforts to identify and deploy new resistance genes. The creation of a wheat resistance gene atlas, as proposed by some researchers, could provide a valuable resource for breeders to rapidly respond to these evolving threats (Hafeez et al., 2021). 5.2 High-throughput phenotyping High-throughput phenotyping (HTP) has emerged as a powerful tool in modern wheat breeding programs. HTP technologies enable the rapid and accurate assessment of phenotypic traits across large populations, thereby facilitating the identification of disease-resistant individuals (Mondal et al., 2016). These technologies include imaging systems, remote sensing, and automated data collection platforms, which can capture a wide range of phenotypic data, including disease symptoms, plant height, and biomass. The integration of HTP with molecular breeding techniques has the potential to significantly accelerate the breeding cycle. For example, HTP can be used to validate the effectiveness of resistance genes identified through MAS or genome-wide association studies (GWAS) (Jabran et al., 2023). This combined approach allows for the rapid screening of large breeding populations, thereby increasing the efficiency of selecting disease-resistant individuals. Moreover, HTP can be used to monitor the performance of resistance genes under different environmental conditions, providing valuable insights into their stability and effectiveness. This is particularly important given the impact of climate change on the prevalence and severity of wheat diseases (Mondal et al., 2016). 5.3 Bioinformatics and data analysis The advent of high-throughput sequencing technologies and the accumulation of large-scale genomic data have necessitated the development of advanced bioinformatics tools and data analysis methods. Bioinformatics plays a crucial role in the identification and characterization of resistance genes, as well as in the analysis of complex interactions between host plants and pathogens (Hafeez et al., 2021). One of the key applications of bioinformatics in wheat breeding is the identification of quantitative trait loci (QTL) associated with disease resistance. QTL mapping and GWAS have been used to identify numerous resistance loci, which can then be targeted in breeding programs using MAS (Jabran et al., 2023). Additionally, bioinformatics tools are essential for the analysis of transcriptomic and proteomic data, which can provide insights into the molecular mechanisms underlying disease resistance (Mapuranga et al., 2022). The integration of bioinformatics with molecular breeding techniques also facilitates the development of genomic selection (GS) models. GS involves the use of genome-wide markers to predict the breeding value of individuals, thereby enabling the selection of superior genotypes at an early stage. This approach has the potential to significantly enhance the efficiency and accuracy of breeding programs, particularly for complex traits such as disease resistance.
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 113 The integration of molecular techniques in wheat breeding programs has revolutionized the development of disease-resistant cultivars. By combining conventional breeding methods with advanced molecular tools, high-throughput phenotyping, and bioinformatics, breeders can more effectively respond to the challenges posed by evolving pathogen populations and changing environmental conditions. This integrated approach holds great promise for ensuring the sustainability and productivity of wheat crops in the face of global food security challenges. 6 Case Studies 6.1 Successful implementation in wheat breeding The integration of molecular breeding techniques has led to significant advancements in developing wheat cultivars with durable resistance to various diseases. One notable success is the deployment of multiple resistance genes through marker-assisted selection (MAS). For instance, the combination of eight resistance genes, including Lr19, Lr34/Yr18/Sr57/Pm38/Ltn1, Sr2/Yr30, Sr26, Sr39, Fhb1, Qfhs.ifa-5A-1, and Qfhs.ifa-5A-2, into a single wheat plant has been achieved, resulting in wheat lines with enhanced resistance to rusts and Fusarium head blight (FHB) (Maré et al., 2020). This approach not only improves disease resistance but also maintains desirable agronomic traits, such as strong dough strength and good bread-making qualities. Another successful implementation is the creation of a wheat resistance gene atlas, which serves as an online directory for identifying and deploying resistance genes. This atlas facilitates the rapid response to evolving pathogen populations by providing breeders with the necessary tools and resources to develop resistant cultivars (Hafeez et al., 2021). The atlas includes information on resistance genes for major wheat pathogens, such as rusts, blotch diseases, powdery mildew, and wheat blast, thereby promoting the development of durable resistance. 6.2 Overcoming specific disease challenges Wheat rusts, caused by Puccinia species, are among the most significant threats to wheat production. The continuous emergence of new rust races with novel virulence necessitates the integration of genomic selection, genome editing, and molecular breeding techniques to develop resistant cultivars (Mapuranga et al., 2022). For example, the positional cloning of partial rust resistance genes, such as Lr34/Yr18 and Yr36, has revealed different protein structures, suggesting that these genes can be functionally heterogeneous. This knowledge allows for a more refined classification and deployment of partial resistance genes, enhancing the durability of resistance (Lowe et al., 2011). Fusarium head blight (FHB) is another major disease challenge in wheat production. The pyramiding of multiple resistance genes, such as Fhb1 and Qfhs.ifa-5A, has been shown to provide effective control against FHB. Marker-assisted selection has been instrumental in combining these genes into elite breeding material, resulting in wheat lines with improved resistance to FHB (Miedaner and Korzun, 2012). Additionally, the use of molecular markers has facilitated the identification and characterization of new resistance alleles, further enriching the genetic basis of resistance in breeding programs (Kaur et al., 2008). 6.3 Lessons learned from field trials Field trials have provided valuable insights into the practical application of molecular breeding techniques for developing disease-resistant wheat cultivars. One key lesson is the importance of combining multiple resistance genes to achieve durable resistance. Single resistance genes are often vulnerable to evolving pathogens, but the pyramiding of multiple genes can provide more robust and long-lasting protection (Liu et al., 2000; Maré et al., 2020). Another lesson is the need for continuous monitoring and evaluation of resistance genes in the field. The dynamic nature of pathogen populations requires breeders to regularly assess the effectiveness of deployed resistance genes and make necessary adjustments. The creation of a wheat resistance gene atlas has proven to be a valuable tool in this regard, enabling breeders to quickly identify and deploy new resistance genes as needed (Hafeez et al., 2021).
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 114 Furthermore, the integration of traditional phenotype-based research methods with advanced molecular techniques has been shown to enhance the effectiveness of resistance breeding. Accurate and detailed disease phenotyping, combined with molecular functional characterization and gene cloning, provides a comprehensive understanding of the interactions between wheat and its pathogens. This integrated approach allows for the rational deployment of resistance genes, ultimately leading to more durable resistance (Lowe et al., 2011). The successful implementation of molecular breeding techniques in wheat breeding has led to significant advancements in developing disease-resistant cultivars. Overcoming specific disease challenges, such as rusts and FHB, requires the integration of multiple resistance genes and continuous monitoring of pathogen populations. Field trials have highlighted the importance of combining traditional and molecular approaches to achieve durable resistance, providing valuable lessons for future breeding programs. 7 Future Directions in Molecular Breeding 7.1 Emerging technologies The future of molecular breeding for durable resistance in wheat is promising, with several emerging technologies poised to revolutionize the field. One of the most significant advancements is the application of CRISPR/Cas-9 gene editing, which allows for precise modifications of the wheat genome to enhance disease resistance traits. This technology has shown potential in developing broad-spectrum resistance against various pathogens by targeting specific genes involved in the plant's immune response (Jabran et al., 2023). Additionally, the use of high-throughput phenotyping and next-generation sequencing (NGS) platforms has accelerated the identification of resistance genes and their associated markers, facilitating the rapid development of resistant wheat varieties (Babu et al., 2020). Another promising technology is the use of genome-wide association studies (GWAS) and quantitative trait loci (QTL) mapping. These approaches have been instrumental in identifying genetic loci associated with disease resistance, enabling breeders to select for these traits more effectively (Babu et al., 2020; Jabran et al., 2023). The integration of bioinformatics tools with these technologies has further enhanced our understanding of the genetic basis of disease resistance, paving the way for more targeted breeding strategies (Babu et al., 2020). 7.2. Integrative approaches Integrative approaches that combine traditional breeding methods with modern molecular techniques are essential for developing durable resistance in wheat. One such approach is the use of marker-assisted selection (MAS), which allows breeders to track the presence of resistance genes in breeding populations using molecular markers. This method has been successfully employed to develop wheat varieties with resistance to rust diseases and other pathogens (Li et al., 2020; Jabran et al., 2023). Another integrative approach is the pyramiding of multiple resistance genes into a single variety. This strategy involves stacking different resistance genes to provide broad-spectrum and durable resistance against a range of pathogens. However, recent studies have highlighted potential challenges with this approach, such as the suppression of resistance when multiple alleles of the same gene are combined (Stirnweis et al., 2014). To overcome these challenges, it is crucial to understand the molecular interactions between different resistance genes and to select compatible gene combinations (Stirnweis et al., 2014). The integration of systems biology with traditional phenotype-based research methods also holds great promise. By combining detailed disease phenotyping with molecular functional characterization and gene cloning, researchers can develop a refined classification of resistance genes based on their functional properties. This integrated approach can guide the rational deployment of resistance genes in breeding programs, ensuring more durable protection against evolving pathogens (Lowe et al., 2011). 7.3 Potential for new resistant varieties The potential for developing new resistant wheat varieties is immense, given the advancements in molecular breeding technologies and integrative approaches. The identification and deployment of new resistance genes
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 115 from diverse genetic sources, including wild relatives of wheat, can significantly enhance the genetic diversity of resistance traits in breeding programs (Mondal et al., 2016; Mapuranga et al., 2022). This genetic diversity is crucial for developing varieties that can withstand the continuous evolution of pathogen populations. Moreover, the use of pathogen-informed breeding strategies, which leverage knowledge of pathogen biology and host-pathogen interactions, can lead to the development of more effective resistance genes. For instance, the use of pathogen effector proteins to identify resistance resources and inform cultivar deployment has shown promise in developing durable resistance (Li et al., 2020). These strategies can be further enhanced by incorporating insights from systems biology and functional genomics, providing a comprehensive understanding of the molecular basis of disease resistance (Lowe et al., 2011). The future of molecular breeding for durable resistance in wheat lies in the integration of emerging technologies, traditional breeding methods, and a deep understanding of host-pathogen interactions. By leveraging these approaches, researchers can develop new resistant varieties that are not only effective against current pathogen populations but also resilient to future challenges posed by evolving diseases. 8 Implications for Global Wheat Production 8.1 Enhancing food security The integration of molecular breeding techniques in developing durable resistance to wheat diseases has profound implications for global food security. Wheat is a staple food for a significant portion of the world's population, providing essential nutrients and calories. However, wheat production is frequently threatened by various pests and diseases, which can lead to substantial yield losses and, consequently, food insecurity (Babu et al., 2020; Deng et al., 2020; Luo et al., 2023). By employing advanced genetic tools such as marker-assisted selection, genome editing, and gene pyramiding, researchers have been able to develop wheat cultivars with enhanced resistance to multiple pathogens (Mondal et al., 2016; Luo et al., 2023). These resistant varieties are crucial in maintaining stable wheat production, especially in regions prone to severe disease outbreaks. The development of wheat lines with durable resistance to diseases like rusts and Fusarium head blight (FHB) ensures a more reliable food supply. For instance, the successful deployment of multiple resistance genes in wheat has shown promise in mitigating the impact of evolving pathogen races, thereby reducing the risk of large-scale crop failures (Johnson, 2004; Mondal et al., 2023). This stability in wheat production is essential for meeting the growing global demand for food, driven by increasing population and changing consumption patterns (Mondal et al., 2016). Moreover, the use of molecular breeding techniques accelerates the breeding process, allowing for the rapid introduction of resistant varieties into agricultural systems, further enhancing food security (Nelson et al., 2017; Babu et al., 2020). 8.2 Economic benefits The economic benefits of developing wheat cultivars with durable disease resistance are multifaceted. Resistant varieties reduce the need for chemical inputs such as fungicides and pesticides, leading to significant cost savings for farmers (Maré et al., 2020; Mapuranga et al., 2022; Luo et al., 2023). The reduction in chemical usage not only lowers production costs but also minimizes the environmental and health risks associated with pesticide exposure. Additionally, the stability in wheat yields provided by resistant varieties ensures a more predictable income for farmers, reducing the economic uncertainty associated with crop losses due to disease outbreaks (Nelson et al., 2017; Deng et al., 2020). The adoption of molecular breeding techniques can enhance the overall efficiency of wheat breeding programs. High-throughput phenotyping, genome sequencing, and genomic selection are promising approaches that maximize progeny screening and selection, thereby accelerating genetic gains in breeding more productive and resilient varieties (Mondal et al., 2016; Babu et al., 2020). This increased efficiency translates into faster development and deployment of improved wheat cultivars, which can boost overall agricultural productivity and profitability. The economic benefits extend beyond individual farmers to the broader agricultural sector, contributing to national and global economies by ensuring a stable supply of wheat, a critical commodity in international trade (Luo et al., 2023).
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 116 8.3 Environmental impact The environmental impact of developing durable resistance to wheat diseases through molecular breeding is largely positive. One of the most significant benefits is the reduction in the use of chemical pesticides and fungicides, which are commonly employed to manage wheat diseases. The overuse of these chemicals can lead to environmental degradation, including soil and water contamination, and can harm non-target organisms, including beneficial insects and soil microbes (Maré et al., 2020; Mapuranga et al., 2022; Luo et al., 2023). By developing wheat varieties that are inherently resistant to diseases, the reliance on chemical controls is diminished, promoting more sustainable agricultural practices (Nelson et al., 2017; Deng et al., 2020). Moreover, the use of molecular breeding techniques can contribute to the conservation of genetic diversity in wheat. By identifying and utilizing resistance genes from diverse sources, including wild relatives of wheat, breeders can enhance the genetic base of cultivated wheat, making it more resilient to future disease pressures and environmental changes (Mondal et al., 2016; Jabran et al., 2023). This genetic diversity is crucial for the long-term sustainability of wheat production, as it provides a reservoir of traits that can be tapped into to address emerging challenges. In addition, the development of disease-resistant wheat varieties can contribute to the mitigation of climate change impacts. Diseases often become more prevalent and severe under changing climatic conditions, which can exacerbate yield losses and threaten food security (Mondal et al., 2016; Babu et al., 2020). By ensuring that wheat cultivars are equipped with durable resistance to a range of diseases, molecular breeding helps to safeguard wheat production against the uncertainties of climate change, thereby supporting the resilience of agricultural systems (Johnson, 2004; Nelson et al., 2017). In conclusion, the integration of molecular breeding techniques in developing durable resistance to wheat diseases has significant implications for global wheat production. It enhances food security, provides economic benefits, and promotes environmental sustainability, making it a critical component of modern agricultural practices. The continued advancement and application of these techniques will be essential in meeting the challenges of feeding a growing global population in a changing world. 9 Concluding Remarks The integration of molecular breeding techniques has significantly advanced the development of wheat cultivars with durable resistance to various diseases. Key findings from the reviewed literature highlight the successful deployment of genetic breeding techniques such as transgenic breeding, molecular marker-assisted breeding, gene pyramiding, gene silencing, and gene editing in improving wheat resistance traits. The identification and utilization of over 200 resistance genes and their associated markers have been crucial in combating rust diseases and other pathogens. Additionally, the application of advanced molecular markers and techniques like CRISPR/Cas-9, QTL mapping, and GWAS have shown promise in enhancing disease resistance in wheat. Integrating molecular techniques into wheat breeding programs is essential for several reasons. These techniques allow for precise and efficient selection of resistance traits at the seedling stage, reducing the time and cost associated with traditional breeding methods. Molecular breeding enables the stacking of multiple resistance genes, which is critical for developing cultivars with broad-spectrum and durable resistance. Furthermore, the use of genomic selection and high-throughput genotyping platforms can accelerate the breeding process and improve the accuracy of selecting desirable traits. The integration of systems biology and traditional phenotype-based research methods also provides a comprehensive understanding of the interactions between wheat and pathogens, guiding the rational deployment of resistance genes. Future research should focus on the continuous identification and characterization of new resistance genes and their molecular mechanisms to stay ahead of evolving pathogen races. The creation of a comprehensive wheat resistance gene atlas, as proposed by some researchers, could serve as a valuable resource for breeders to rapidly respond to emerging threats. Additionally, there is a need to refine the classification of partial resistance genes
Molecular Pathogens 2024, Vol.15, No.3, 106-118 http://microbescipublisher.com/index.php/mp 117 based on molecular functions and interactions, which can aid in the strategic deployment of these genes for durable resistance. Breeding programs should also prioritize the integration of advanced molecular techniques such as CRISPR/Cas-9 and GWAS to enhance the precision and efficiency of developing resistant cultivars. Finally, collaboration among international research communities and the sharing of genomic resources will be crucial in addressing the global challenges of wheat disease resistance and ensuring food security. Acknowledgments The MicroSci Publisher extend sincere thanks to two anonymous peer reviewers for their comments on the manuscript of this study. Conflict of Interest Disclosure The author affirms that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest. References Babu P., Baranwal D., Harikrishna, Pal D., Bharti H., Joshi P., Thiyagarajan B., Gaikwad K., Bhardwaj S., Singh G., and Singh A., 2020, Application of genomics tools in wheat breeding to attain durable rust resistance, Frontiers in Plant Science, 11: 567147. https://doi.org/10.3389/fpls.2020.567147 Brown J., 2015, Durable resistance of crops to disease: a Darwinian perspective, Annual Review of Phytopathology, 53: 513-39. https://doi.org/10.1146/annurev-phyto-102313-045914 Deng Y., Ning Y., Yang D., Zhai K., Wang G., and He Z., 2020, Molecular basis of disease resistance and perspectives on breeding strategies for resistance improvement in crops, Molecular Plant, 13(10): 1402-1419. https://doi.org/10.1016/j.molp.2020.09.018 Figlan S., Ntushelo K., Mwadzingeni L., Terefe T., Tsilo T., and Shimelis H., 2020, Breeding wheat for durable leaf rust resistance in southern africa: variability, distribution, current control strategies, challenges and future prospects, Frontiers in Plant Science, 11: 549. https://doi.org/10.3389/fpls.2020.00549 Hafeez A., Arora S., Ghosh S., Gilbert D., Bowden R., and Wulff B., 2021, Creation and judicious application of a wheat resistance gene atlas, Molecular Plant, 14(7): 1053-1070. https://doi.org/10.1016/j.molp.2021.05.014 Jabran M., Ali M., Zahoor A., Muhae-Ud-Din G., Liu T., Chen W., and Gao L., 2023, Intelligent reprogramming of wheat for enhancement of fungal and nematode disease resistance using advanced molecular techniques, Frontiers in Plant Science, 14: 1132699. https://doi.org/10.3389/fpls.2023.1132699 Johnson R., 2004, Past, present and future opportunities in breeding for disease resistance, with examples from wheat, Euphytica, 63: 3-22. https://doi.org/10.1007/BF00023908. Kaur N., Street K., Mackay M., Yahiaoui N., and Keller B., 2008, Molecular approaches for characterization and use of natural disease resistance in wheat, European Journal of Plant Pathology, 121: 387-397. https://doi.org/10.1007/s10658-007-9252-3 Krattinger S., and Keller, B., 2016, Molecular genetics and evolution of disease resistance in cereals, The New Phytologist, 212(2): 320-332. https://doi.org/10.1111/nph.14097 Kozub N., Sozinova O., Sozinov I., Karelov A., Janse L., Mishchenko L., Borzykh O., and Blume Y., 2022, Advances in durable resistance to diseases in staple food crops: a review, The Open Agriculture Journal. https://doi.org/10.2174/18743315-v16-e220922-2022-ht14-3623-2 Kuchel H., Fox R., Reinheimer J., Mosionek L., Willey N., Bariana H., and Jefferies S., 2007, The successful application of a marker-assisted wheat breeding strategy, Molecular Breeding, 20: 295-308. https://doi.org/10.1007/s11032-007-9092-z Li Q., Wang B., Yu J.P., and Dou D.L., 2020, Pathogen-informed breeding for crop disease resistance, Journal of Integrative Plant Biology, 63(2): 305-311. https://doi.org/10.1111/jipb.13029 Liu J., Liu D., Wj T., Li W., Wang S., Chen P., Cheng S., and Gao D., 2000, Molecular marker-facilitated pyramiding of different genes for powdery mildew resistance in wheat, Plant Breeding, 119(1): 21-24. https://doi.org/10.1046/J.1439-0523.2000.00431.X Liu D.M., Yuan C., Singh R.P., Randhawa M.S., Bhavani S., Kumar U., Huerta-Espino J., Lagudah E., and Lan C.X., 2022, Stripe rust and leaf rust resistance in CIMMYT wheat line “Mucuy” is conferred by combinations of race-specific and adult-plant resistance loci, Frontiers in Plant Science, 13: 880138. https://doi.org/10.3389/fpls.2022.880138 Lowe I, Cantu D, Dubcovsky J., 2011, Durable resistance to the wheat rusts: integrating systems biology and traditional phenotype-based research methods to guide the deployment of resistance genes, Euphytica, 179(1): 69-79. https://doi.org/10.1007/s10681-010-0311-z Luo K., He D., Guo J., Li G., Li B., and Chen X., 2023, Molecular advances in breeding for durable resistance against pests and diseases in wheat: opportunities and challenges, Agronomy, 13(3): 628. https://doi.org/10.3390/agronomy13030628
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