1 Introduction

Wheat cultivation is facing serious pest problems worldwide. These pests include insects and pathogens such as rye whiteflies, Russian wheat aphids, green aphids, and sunworms. They bite crops directly and spread diseases, causing great losses (Douglas, 2018; Tadesse, 2021). In addition, pests are becoming more and more resistant to chemical pesticides, making traditional control methods less effective (Luo et al., 2023). In addition, climate change may make pest problems worse, leading to more frequent infestations and greater damage (Arif et al., 2022).

To achieve sustainable agriculture, it is necessary to cultivate wheat varieties that are resistant to insects for a long time. Through genetic resistance, wheat can resist pests without relying on chemical agents, which is both environmentally friendly and protects the ecosystem (Mondal et al., 2016; Singh et al., 2016). New technologies such as transgenic breeding, molecular marker-assisted breeding, and gene editing have shown the potential to improve wheat insect resistance (Qi et al., 2019; Luo et al., 2023). These methods can combine multiple insect resistance traits to cultivate wheat varieties that are both high-yielding and resistant to multiple pests (Bakala et al., 2021; Tadesse, 2021).

This study mainly summarizes the latest progress in genetic strategies for insect resistance in wheat. We will introduce: how to find and use insect resistance genes from different genetic resources, such as wild relatives and old local varieties; how to use methods such as gene clustering, gene silencing, and genome editing to cultivate new insect-resistant wheat varieties; and how to better apply genetic resistance to wheat breeding programs in the face of changing pest populations and environmental changes, as well as future development directions.

2 Understanding Pests and Their Impact on Wheat

2.1 Major Pests Affecting Wheat Yield

Wheat cultivation is often threatened by a variety of pests, such as rye whitefly, Russian wheat aphid, green aphid and wheat trichogrammatid (Tadesse, 2021). In Europe, orange wheat flower borer (OWBM), yellow wheat flower borer (YWBM), saddle gall midge (SGM), thrips and wheat whitefly (FF) are particularly harmful (Arif et al., 2022). These pests not only reduce wheat yields, but also affect wheat quality. To combat these pests, scientists have found insect-resistant genes from local varieties and wild relatives and have achieved good results in breeding (Tadesse, 2021; Arif et al., 2022).

2.2 Economic and environmental costs of pests

Pests have caused huge economic losses to wheat cultivation worldwide. For example, rye whitefly and green stink bug are very harmful, so the promotion of insect-resistant wheat varieties has become the main method of prevention and control (Subramanyam et al., 2023). Although chemical control can control pests, it is costly and pollutes the environment. The misuse of pesticides not only makes pests more difficult to kill, but also harms other beneficial organisms and pollutes soil and water resources (Luo et al., 2023; Subramanyam et al., 2023).

2.3 Problems encountered in current pest management

Pests are evolving rapidly to resist pesticides and insect-resistant wheat, which is one of the biggest problems at present. Modern agriculture has low genetic diversity, making wheat more vulnerable to new pests. When the insect-resistant genes of wild wheat are introduced into excellent varieties, some bad traits are often brought along, and single resistance can easily become ineffective quickly (Wulff and Moscou, 2014). Traditional breeding is too slow, and it is difficult to concentrate multiple insect-resistant traits into one variety in a short period of time (Mondal et al., 2016). Although new technologies such as genome-wide association studies (GWAS) and marker-assisted selection appear promising, they require significant investments of funds and professionals (Ando et al., 2018 ; Norman et al., 2023 ).

3 Conventional Breeding for Pest Resistance

3.1 Traditional Breeding Approaches in Wheat

Traditional wheat breeding methods mainly include direct hybridization, backcrossing and selection. These practices can introduce good traits such as insect resistance from local varieties, wild relatives and existing cultivated varieties (Mondal et al., 2016; Tadesse, 2021). Through these methods, scientists have found some resistance (R) genes to breed wheat varieties resistant to rye whiteflies, Russian wheat aphids and green stink bugs (Tadesse, 2021). However, traditional breeding mainly relies on observing external traits and requires a lot of field trials and screening, so it is usually time-consuming and laborious (Mondal et al., 2016; Afzal et al., 2022).

3.2 Successful cases and existing problems

Although traditional breeding is slow, it has also brought many results. For example, the promotion of resistant varieties has helped control wheat rust and pests, and improved yield and stability (Tadesse, 2021; Afzal et al., 2022). However, it also has many problems. Because insect resistance traits are often complex, the breeding of new resistant varieties is slow. Moreover, it is difficult to combine multiple ideal genes into the same variety (Mondal et al., 2016; Afzal et al., 2022). In addition, single-gene resistance is easily broken by new pest populations, and pest mutation is also an emerging challenge (Wulff and Moscou, 2014; Mapuranga et al., 2022).

3.3 Combination of traditional and modern technologies

In order to make up for the shortcomings of traditional breeding, new technologies such as molecular marker-assisted selection (MAS), genomic selection and gene editing are often combined and used together (Mapuranga et al., 2022; Luo et al., 2023) (Figure 1). These modern methods can find and integrate resistance genes faster and more accurately, speed up breeding, and make resistance more durable (Savadi et al., 2018; Afzal et al., 2022). For example, the use of molecular markers to concentrate multiple resistance genes into one variety has shown great promise in breeding broad-spectrum, durable insect-resistant wheat (Afzal et al., 2022; Norman et al., 2023). In addition, technologies such as high-throughput phenotyping and genome sequencing can also help breeders screen offspring more efficiently and improve the effectiveness of the entire breeding program (Mondal et al., 2016; Savadi et al., 2018).

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 graminum resistance genes; Sas, English grain aphid Sitobion avenae resistance genes; QFhbs, scab resistance QTLs; QRps, bird cherry-oat aphid Rhopalosiphum padi resistance QTLs; QGb, greenbug resistance QTL (Adopted from Luo et al., 2023)

4 Role of Wild Relatives and Landraces in Resistance

4.1 Genetic diversity in wheat’s wild relatives

Wild relatives of wheat are important genetic resources and are crucial to improving the disease resistance of modern wheat. Wheat experienced a genetic bottleneck during domestication, which greatly reduced genetic diversity. However, wild relatives retain a wealth of genetic variation that can be used to enhance disease resistance. For example, scientists have successfully introduced resistance genes from 13 genera and 52 species into wheat, which shows that the wheat genome is very plastic and natural variation is useful in breeding (Wulff and Moscou, 2014). Wild relatives such as Aegilops sphaerocephalus are particularly valuable, as they are resistant to rust, smut, and powdery mildew (Sheikh et al., 2017). In addition, technologies such as molecular markers have also helped scientists better find and use these useful genes (Kaur et al., 2008).

4.2 Resistance genes in local varieties

Landraces are the types of wheat that farmers have grown over the past few hundred years and have also played an important role in improving wheat's resistance to diseases and pests. These varieties have evolved unique genetic characteristics under specific environments and have become a good source of resistance genes. For example, studies have found that about 14% of local varieties are resistant to stem sawflies, and some varieties show both exotic and native resistance (Varella et al., 2017). Molecular genetics studies have also found known resistance genes such as the powdery mildew resistance gene Pm3 in 1,320 local varieties (Kaur et al., 2008). These results show that local varieties can add more useful resistance genes to breeding.

4.3 Methods for transferring resistance genes to new varieties

In order to transfer resistance genes from wild relatives and local varieties to elite wheat, some special pre-breeding strategies are needed. The usual method is to first hybridize wild relatives or local varieties with cultivated wheat, and then retain good traits and remove bad traits through backcrossing and selection. For example, after hybridizing local durum wheat and tauschia, a synthetic hexaploid was obtained, which has high yield, short stature, and resistance to stripe rust (Valkoun, 2004). Now, the development of molecular technologies, such as single nucleotide polymorphism (SNP)-based genotyping and resistance gene screening technologies such as MutRenSeq and AgRenSeq, has also made the transfer of resistance genes faster and more accurate (Norman et al., 2023). These new methods can quickly find useful genes and greatly improve breeding efficiency.

5 Genomics and Marker-Assisted Selection

5.1 Advances in Wheat Genomics for Resistance Traits

Recently, great progress has been made in wheat genomics, which has helped us better understand and improve wheat insect resistance. The emergence of next-generation sequencing (NGS) technology and bioinformatics tools has completely changed the way wheat genome is studied. Now, we can find associations between markers and traits and identify resistance genes. High-throughput genotyping platforms also allow scientists to draw high-density genetic maps to help understand complex resistance traits  (Babu et al., 2020). In addition, genomic selection (GS) technology can more accurately estimate breeding values ​​by utilizing all genetic marker information, thereby accelerating the breeding process for complex traits controlled by many small effect genes (Gesteiro et al., 2023).

5.2 Application of marker-assisted selection in insect resistance

Marker-assisted selection (MAS) has been widely used to improve wheat insect resistance. MAS uses molecular markers linked to resistance genes to select desired traits at the seedling stage, which improves accuracy and reduces breeding costs (Miedaner and Korzun, 2012). For example, MAS has successfully introduced resistance genes such as Lr34, Yr36 and Pch1 into excellent wheat varieties, proving that this method is very effective in actual breeding (Miedaner and Korzun, 2012). Moreover, MAS can help breed wheat with long-lasting rust resistance by integrating multiple resistance genes and slow down the evolution of pathogens (Kuchel et al., 2007). However, MAS also has limitations, such as sometimes lacking good diagnostic markers or the effect of a single quantitative trait locus (QTL) is too small (Miedaner and Korzun, 2012).

5.3 Challenges in the application of genomics

Although genomics has brought many new opportunities, it still faces many challenges in promoting it in wheat breeding. A big problem is economic and biological constraints, such as high investment and low returns in breeding small-grain crops, and QTL background effects often affect results (Miedaner and Korzun, 2012). In addition, in order to integrate genomic data, phenotypic testing needs to be repeated in different locations and years, which takes a lot of time and resources. Quantitative disease resistance in wheat is usually controlled by hundreds of QTLs scattered throughout the genome, which also makes breeding work more complicated (Miedaner et al., 2020) (Figure 2; Table 1). In addition, although genomic selection is more accurate than MAS prediction, it requires complex statistical models and large amounts of data, which are not easily affordable for all breeding programs (Arruda et al., 2016; Merrick et al., 2021).

Figure 2 Techniques for genomics-assisted breeding (Adopted from Miedaner et al., 2020). Image caption: SSR = Single sequence repeat, DArT = Diversity Array technique, SNP = Single nucleotide polymorphism, NGS = Next-generation sequencing, QTL = quantitative trait locus, GWAS = genome-wide association studies, MAS = Marker-assisted selection, MABC = Marker-assisted backcrossing, MARS = Marker-assisted recurrent selection, GS = Genomic selection (Adopted from Miedaner et al., 2020)

Table 1 Main advantages and pitfalls1 for GS in science and breeding (Adopted from Miedaner et al., 2020) Note: 1 leading to an incorrect estimation of prediction accuracies (over-/underestimation)

6 Transgenic Approaches for Pest Resistance

6.1 Genetic engineering of wheat for pest resistance

Genetic engineering has become an important method to improve wheat's insect resistance. Scientists now use Agrobacterium-mediated transformation and direct DNA transfer to introduce pest-resistant genes into wheat (Babu et al., 2003). Most of these genes come from bacteria, such as Bacillus thuringiensis (Bt), which can enable wheat to produce insecticidal proteins and have a good protective effect against a variety of pests (Sharma et al., 2004; Talakayala et al., 2020). In addition, the development of RNA interference (RNAi) and CRISPR-Cas9 gene editing technologies also allows scientists to directly target specific genes of pests and cultivate more insect-resistant wheat (Saeed et al., 2020; Talakayala et al., 2020). These new methods not only improve insect resistance, but also reduce the use of pesticides, which is very helpful for achieving sustainable agriculture (Babu et al., 2003; Sharma et al., 2004).

6.2 Successful cases of transgenic wheat

Some transgenic wheat varieties performed well in field trials. For example, wheat varieties that overexpress the Pm3 gene show stronger resistance to powdery mildew. These varieties have introduced different versions of the Pm3 gene and have higher disease resistance than ordinary wheat (Brunner et al., 2012). Another example is that wheat with the Pm17 gene is not only resistant to powdery mildew, but also further enhances resistance by expressing genes such as Pm3 and Pm8 at the same time (Koller et al., 2023) (Figure 3). These examples show that transgenic technology has great potential in breeding wheat varieties with long-lasting pest resistance.

Figure 3 Powdery mildew infection, Pm17 expression and PM17 protein accumulation in field-grown transgenic Pm17 Bobwhite events (Adopted from Koller et al., 2023) Image caption: (A) Powdery mildew infection of field-grown plants. Area under disease progress curve (AUDPC) scores were calculated from four independent plots for each genotype in field seasons 1 (red), 2 (green), and 3 (blue). Non-transformed Bobwhite and wheat cultivar Amigo, which carries endogenous Pm17, are included as controls. Powdery mildew disease pressure was high during field seasons 1 and 3, and low during field season 2. Different letters next to the bars denote a significant difference within the same season in the Tukey’s honestly significant difference (HSD) test (α=0.050). (B) Pm17 expression in flag leaves from field seasons 2 and 3. Expression values were normalized to the expression of reference gene ADP ribosylation factor (ADPRF) and plotted relative to line Pm17#110. Four biological replicates, each consisting of three pooled flag leaf segments, were used for each genotype in technical duplicates. Different letters above the bars denote a significant difference in expression level (Tukey’s HSD test, α=0.050). (C) PM17–HA protein accumulation in flag leaves from field seasons 2 and 3. Each sample contains three pooled flag leaf segments. Total protein concentration was measured and adjusted to the same concentration prior to loading. Ponceau staining indicates equal loading (Adopted from Koller et al., 2023)

6.3 Issues of regulation and public awareness

Although transgenic wheat has achieved good results, regulation and public attitudes are still great challenges. The promotion and commercialization of transgenic crops must be subject to strict regulatory approval. These regulations require comprehensive safety assessments of crops to ensure that they will not cause harm to human health or the environment (Babu et al., 2003). In addition, public concerns about GM foods, such as possible long-term effects on health or biodiversity, have also led some consumer groups and environmental organizations to oppose them (Babu et al., 2003; Tabashnik and Carrière, 2017). For GM wheat to be more widely accepted, these issues need to be addressed through transparent communication and rigorous scientific evaluation.

7 CRISPR/Cas Technology in Pest Resistance

7.1 Overview of CRISPR Applications in Wheat

CRISPR/Cas9 technology has brought great changes to genetic engineering. It provides a precise, fast and cost-effective genome editing method. Now, this technology has been widely used in wheat and other crops to enhance resistance to pests and diseases. CRISPR/Cas9 can directly modify the genome of wheat without introducing foreign DNA, which also reduces people's concerns about genetically modified crops (GMO) (Borrelli et al., 2018; Ahmad et al., 2020; Wang et al., 2022). This technology has been successfully used to edit genes related to susceptibility in wheat, improving the plant's own disease resistance (Bisht et al., 2019; Mushtaq et al., 2019; Erdoğan et al., 2023).

7.2 Editing resistance genes to enhance insect resistance

A major method for enhancing wheat insect resistance using CRISPR/Cas9 is to modify or knock out susceptibility (S) genes that make plants vulnerable to pest attacks. After disrupting these genes, plants can be much more resistant to a variety of pests and pathogens, including fungi, bacteria, and viruses (Borrelli et al., 2018; Rato et al., 2021; Komal et al., 2023). For example, downregulating or deleting specific S genes can make wheat more resistant to stripe rust, leaf rust, and powdery mildew (Taj et al., 2022). In addition, CRISPR can also modify immune receptors or change the way pests interact with plants, further enhancing wheat's defense capabilities (Bisht et al., 2019; Paul et al., 2021).

7.3 Future prospects of genome editing in wheat improvement

CRISPR/Cas9 has great potential in wheat breeding. With the continuous advancement of technology, it is expected that wheat varieties that can adapt to climate change and resist new pests will be cultivated in the future. CRISPR can make very precise modifications to genetic details, such as quickly adding beneficial traits such as insect resistance, drought tolerance, or high yield (Wang et al., 2022; Erdoğan et al., 2023). In addition, new generation CRISPR technologies, such as the dual Cas9 cutting system and new gene delivery methods, can also reduce the chance of errors and improve editing efficiency (Erdoğan et al., 2023). If CRISPR is combined with other technologies, such as host-induced gene silencing (HIGS) and biological control agents, wheat breeding will be more sustainable and more resistant to stress (Rato et al., 2021).

8 Integrated Pest Management (IPM) with Genetic Approaches

8.1 Combining Genetic and Agronomic Strategies

To effectively manage wheat pests, genetic resistance alone is not enough and must be combined with agronomic practices. Insect-resistant wheat obtained through conventional breeding or genetic engineering can help reduce the number of pests. However, because new pest populations are constantly emerging, multiple methods must be used to deal with them. For example, planting resistant varieties, combined with crop rotation, intercropping and reasonable planting schedules, can make resistance more durable and reduce the use of pesticides (Rand et al., 2020; Mapuranga et al., 2022). In addition, modern technologies such as genomic selection, gene editing, and marker-assisted selection can also be used in combination with traditional agricultural methods to breed good varieties that are resistant to multiple diseases (Mapuranga et al., 2022).

8.2 Combination of biological control and genetic resistance

Combining biological control with genetic resistance can better control pests. For example, using natural enemies such as parasitic wasps and predatory insects, combined with insect-resistant wheat varieties, can greatly reduce the number of pests. Studies have found that the use of resistant varieties or natural enemies alone is not as effective as the combination of the two (Baker et al., 2020; Rand et al., 2020). In addition, Bt proteins expressed in transgenic wheat have also been successfully used in integrated pest management (IPM) programs, which not only reduce the use of pesticides but also protect beneficial insects (Boulter, 1993; Kennedy, 2008). This approach can not only control major pests, but also prevent the outbreak of secondary pests due to the reduced use of pesticides (Kennedy, 2008).

8.3 Problems encountered in the application of integrated methods

Although the combination of genetic methods and biological control has a good effect, there are still many problems in actual promotion. A major challenge is that pests themselves are constantly evolving and may gradually develop resistance to resistance genes and biological control methods (Lamichhane et al., 2016; Green et al., 2020). In addition, communication between researchers, policymakers and farmers is sometimes poor, and knowledge dissemination is not in place, which also affects the implementation of IPM strategies (Lamichhane et al., 2016). Another issue is economic issues. For example, it costs a lot of money to develop resistant varieties and biological control products, which has become an obstacle to promotion (Baker et al., 2020). To solve these problems, it is necessary to strengthen farmer education and extension services, and formulate better policies to support the use of biological control alternatives (Lamichhane et al., 2016; Baker et al., 2020).

9 Case Study: Successful Genetic Strategies in Pest-Resistant Wheat Development

9.1 Background of the case study

Wheat is one of the most important food crops in the world, but various pests seriously threaten wheat yield and quality. To ensure food security, scientists have been working hard to breed insect-resistant wheat varieties. This case study summarizes some successful methods in wheat insect-resistant breeding, especially the combination of traditional breeding and modern technologies.

9.2 Genetic technologies used and their effects

Scientists use many genetic technologies in insect-resistant wheat breeding. Traditional methods, such as direct hybridization, backcrossing, and selection, have helped introduce the excellent traits of wild relatives and local varieties into modern wheat. These methods have successfully introduced genes for resistance to pests such as rye whitefly, Russian wheat aphid, and green stink bug (Mondal et al., 2016; Tadesse, 2021).

Later, modern molecular breeding technologies further accelerated the process. For example, marker-assisted selection (MAS) and quantitative trait loci (QTL) mapping have helped scientists accurately find and integrate resistance genes. For example, a major QTL for resistance to sarsaparilla pests was found on chromosome 4BS of wheat, which explains a large part of the resistance variation (Emebiri et al., 2017). Genome-wide association studies (GWAS) have also helped to link specific gene regions with resistance traits, greatly improving breeding accuracy (Ali et al., 2019; Arif et al., 2022) (Figure 4).

At the same time, transgenic methods and genome editing technologies (such as CRISPR/Cas9) have also played a role in insect-resistant wheat. These technologies can directly modify wheat genes to make it more resistant to pests. For example, studies have used gene silencing and protease inhibitors to improve wheat's resistance to cereal cyst nematodes (CCN) (Ali et al., 2019; Bisht et al., 2019). In addition, genetic modification to transfer disease-resistant genes from wild wheat to elite varieties has also shown the potential to maintain high yields under pest pressure (Alderton, 2018).

9.3 Experience Summary and Applicability to Other Regions

The success of insect-resistant wheat breeding has given us several important insights. First, the combination of traditional breeding and modern molecular technology is the key to achieving lasting resistance. It is also very important to use the genetic diversity of wild relatives and local varieties, which can make modern wheat more resistant to pests (Wulff and Moscou, 2014; Mondal et al., 2016).

Second, molecular tools such as MAS, QTL mapping and GWAS are very useful. They make breeding faster and more accurate, and can quickly find and combine multiple resistance genes (Emebiri et al., 2017; Luo et al., 2023). Genome editing technologies such as CRISPR/Cas9 have also brought new opportunities for insect-resistant breeding with a low error rate (Bisht et al., 2019).

Finally, whether these methods can be extended to other regions depends on local pest pressure and environmental conditions. Wheat populations and pest types vary from place to place, so strategies need to be adjusted according to specific circumstances. Strengthened collaboration between researchers, breeders, and farmers is needed to promote appropriate insect-resistant wheat varieties based on local needs (Tadesse, 2021; Arif et al., 2022).

10 Conclusion and Future Directions

The combination of traditional and modern technologies has made great progress in improving wheat's resistance to insect pests. Traditional breeding methods, such as direct hybridization and backcrossing, help introduce good traits (such as insect resistance) from different gene pools into wheat varieties. Modern methods, such as transgenic breeding, molecular marker-assisted breeding, gene aggregation, gene silencing and gene editing, have also accelerated the development of insect-resistant wheat. The application of next-generation sequencing (NGS) and high-throughput genotyping platforms allows scientists to quickly find and use multiple resistance genes, enhancing wheat's lasting resistance to pests such as rust and aphids. Now, combining genomic selection and genome editing technologies has also shown great potential in breeding high-quality, multi-disease resistant wheat varieties.

However, there are still many problems in wheat insect resistance research and technology application. A major challenge is that new pest populations continue to emerge, and these pests may break existing resistance genes. The genetic basis of modern wheat varieties is too simple, which also makes it easier for pests to adapt, indicating that genetic diversity needs to be increased in breeding. Combining multiple resistance genes into the same variety is a slow and complex process, and screening is also difficult. In addition to genetic resistance, better agronomic methods are needed to reduce the cost of pest and disease management. Another point is that pests can evolve quickly to overcome the natural resistance of wheat, so we also need to have a deeper understanding of the molecular mechanisms between pests and resistance.

In the future, the development of insect-resistant wheat breeding will require the continuous combination of advanced genetic tools and traditional breeding methods. Technologies such as high-throughput phenotyping, genome sequencing, and genome selection will play an important role in accelerating breeding and improving genetic benefits. Cis-gene technology can help introduce useful genes from closely related species to bring more lasting resistance. At the same time, the discovery and use of new resistance genes from wild wheat and other resources can also broaden the genetic basis of wheat and enhance the stability of varieties. Combining genetic resistance with agronomic management to form an integrated pest management (IPM) strategy will also play a key role in sustainable wheat cultivation. Finally, in-depth research on the molecular mechanisms of disease and insect resistance will provide a solid foundation for the breeding of new and durable wheat varieties.

Acknowledgments

Thank you to Dr. Fang from the project team for her careful guidance and strong support. Your professional insights and valuable suggestions have played a crucial role in the smooth progress of this research.

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.

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