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Genetically Modified Organisms [Working Title]
Open access peer-reviewed chapter - ONLINE FIRST
Mutagenesis Application in Plant Improvement: Advancements and Its Future
Written By
Augustine Antwi-Boasiako, Padmore Adu-Antwi,
Richard Adu Amoah, Augustine Boakye Boateng, Joseph Gyau,
Matilda Frimpong, Isaac Newton Boakye-Mensah and
Ivy Odi Ahiamadia
Submitted: 14 May 2023Reviewed: 01 June 2023Published: 12 July 2024
Agricultural plant genetic resources are constantly going into extinction having negative implications for plant genetic banks. Hence, there is a need to generate variations. Stimulated mutagenesis offers an efficient tool to generate genetic variation and explore the function of genes. It also facilitates the identification of genes and their roles in traits of economic interest to breeders, farmers and consumers. Thus, transforming the agro-based industries in overcoming obstacles (poor yield, lodging, shattering, pests and disease infestations). Exploring alternatives to integrate farmers’ and consumers’ desirable traits into their preferred cultivars has led to major advancements in mutation breeding. The chapter provides a comprehensive update on induced mutagenesis approaches, increasing efficiency of targeted mutagenesis and identification of novel traits in mutated populations. Furthermore, it reveals the efforts of ten countries that are leading the development of varieties via mutation across the globe and the most prioritised crops that have received critical attention in mutation breeding. Moreover, it seeks to bring to light the current approaches used in facilitating mutation breeding. It details the current progress made in improving plants with evidence relating to generating genetic resources, biotic and abiotic stresses, nutritional, and quality improvement whiles providing future directions for mutation breeding.
Crops Research Institute, Council for Scientific and Industrial Research, Kumasi, Ghana
National Center for Soybean Improvement, Key Laboratory of Biology and Genetics and Breeding for Soybean, Ministry of Agriculture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, China
Padmore Adu-Antwi
Crops Research Institute, Council for Scientific and Industrial Research, Kumasi, Ghana
Richard Adu Amoah
Plant Genetic Resources Research Institute, Council for Scientific and Industrial Research, Bunso, Ghana
Augustine Boakye Boateng
Crops Research Institute, Council for Scientific and Industrial Research, Kumasi, Ghana
Joseph Gyau
Crops Research Institute, Council for Scientific and Industrial Research, Kumasi, Ghana
Matilda Frimpong
Crops Research Institute, Council for Scientific and Industrial Research, Kumasi, Ghana
Isaac Newton Boakye-Mensah
Crops Research Institute, Council for Scientific and Industrial Research, Kumasi, Ghana
Ivy Odi Ahiamadia
Cocoa Health and Extension Division, Ghana Cocoa Board, Accra, Ghana
*Address all correspondence to: bbbantwi@cropsresearch.org
1. Introduction
Genetic variation is pivotal to ensuring the evolutionary adaptation of plant species. It also facilitates plants’ adaptation to various stresses arising from their environment. Many interventions are designed to promote increased genetic diversity in plants not excluding mutation [1]. Mutation occurs when there is a sudden change in the sequences of the DNA but it is not derived through segregation or recombination. Mutagenesis is the process by which mutation occurs. Plant mutation breeding also termed variation breeding employs the use of physical radiations, chemical means and/or biological mutagens to cause spontaneous genetics. Several methods are used to induce mutagenesis in plants [2]. Physical mutagens (UV, X-ray, fast neutron, as well as gamma radiation); chemical mutagens such as EMS (ethyl methanesulfonate), MNU (N-methyl-N-nitrosourea), HF (hydrogen fluoride), MMS (methyl methanesulfonate) and biological mutagens (Agrobacterium and transposon-based chromosomal integration) are broadly explored. These methods are quite tedious.
The advent of molecular genetic techniques has developed the acquisition and study of mutations. For instance, in vitro mutagenesis protocols are been established in plants (wheat, saffron, and dendrobium) to achieve maximum variability for subsequent characterisation by investigating the germplasm at various levels including molecular, biochemical, and morphology [3, 4, 5]. In vitro mutagenesis has successfully been employed in many plant species to overcome abiotic (drought, salt, frost, and aluminium) and biotic stresses [6]. In addition, next-generation sequencing (NGS) detects mutations very quickly, and it is cost-effective. Integrating induced mutation with whole-genome sequencing supports the use of forward and reverse genetics enabling specific genome editing techniques such as ZFNs (Zinc Finger Nucleases), transcription activator-like effector nucleases (TALENS), and clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated9 (Cas9) endonuclease. The mutants generated are termed mutagenic plants or seeds. They become potential commercial varieties or are used as a parent plant to generate new varieties.
Mutation breeding serves as an avenue for generating demand-driven varieties that meet the needs of customers, industries, and producers. This is made possible by supporting the functional characterisation of genes, and the establishment of gene-trait relationships among numerous crop types. Hence, mutation drives the drift and leading methods in evolution and plant breeding [2, 7]. This account for the continuous use of mutation breeding by breeders after its discovery in 1925 as they are considered as not transgenic in nations where transgenic plants are denied [8]. The advancement in mutation breeding has been discussed to reveal its relevance in the crop improvement process and its future directions. This chapter offers a comprehensive overview of the progresses induced mutagenesis provides in achieving zero hunger by contributing to food security in the light of climate change. Specifically, the chapter presents i) mutagenesis approaches for plant improvement ii) increasing efficiency of targeted mutagenesis and identification of some novel traits iii) contributions of mutagenesis in plant improvement (plant diversity & genetic resources; biotic & abiotic stress resistance; & nutritional quality trait improvement) and iv) future of mutagenesis for improving plants.
Mutation breeding techniques have extensively been employed for crop enhancement. The techniques involve the use of both physical, chemical, biological mutagens, and gene editing (CRISPR/Cas9, TALEN-based, VIGS, RNAi interference) to generate genetic variability in crops and their effects on crops have been well characterised [2, 9, 10, 11]. The physical mutagens commonly used include gamma rays, alpha particles, X-rays, fast neutrons, beta particles and UV light. Also, ethyl methanesulfonate (EMS), N-methyl-N-nitrosourea (MNU), sodium azides, diethyl sulfate and diepoxybutane are effective chemical mutagens used [12]. Ionising radiations cause an array of chemical changes in crop plants by penetrating deep into plant tissues. Inversion, translocation, breakdown, and duplication of chromosomes, as well as point mutation, are among the chemical changes caused by ionising radiations [13]. Gamma rays are the most effective and widely used among ionising radiations in induced mutation [9]. Furthermore, chemical mutagens have also proven effective in inducing mutation. Their usage is easy, does not involve any specialised tools and generates a high rate of mutation. They effect changes in single base-pair or point mutations, or single-nucleotide polymorphisms (SNPs) [9]. Chemical mutagens are often used on vegetative propagules, seedlings, seeds, and tissues cultured in vitro such as explants of leaf and stem, ovules, anthers, microspores, and cell cultures, among others [14, 15]. Biological mutagens use living organisms such as bacteria (Agrobacterium tumefaciens, & Agrobacterium rhizogenes) and viruses (Tobacco mosaic virus) to cause mutation in DNA of organisms. The advancement of NGS strategies has been used to overcome random mutation. This is supported by genome editing tools namely, TALEN, CRISPR/Cas9, and ZFNs and they are applied in diverse plants. The effectiveness of these tools is well documented in different plants (Table 1). Currently, the combination of mutagenesis, PCR-based techniques and NGS provides the avenue to gene function contributing to crop improvement.
3. Increasing efficiency of targeted mutagenesis and identification of some novel traits
The evolution and advancement of targeted mutagenesis have significantly increased its efficiency by limiting the shortfall (error catastrophe and evolutionary escape) linked with the procedure. The quest for highly efficient targeted mutagenesis has resulted in small laboratories an access to targeted mutagenesis [46]. Targeted mutagenesis is achieved by embracing techniques such as Zinc Finger Nucleases (ZFNs), Transcription Activator Like Effector Nucleases (TALENs), and Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) [10, 47]. These techniques stimulate double-stranded breaks within the genomic DNA section of interest and consequently recombine [46, 48]. Setbacks within the application of ZFN include its domain assemble in binding with the nucleotides with high-affinity couple with target site selection [49]. However, off-target effects are reduced by using modified ZFNs and universal deep-learning models which now facilitated targeted mutagenesis [47, 50, 51]. Increasing the efficiency of TALENS requires heterodimer FokI domains and the use of an effective and efficient delivery system (electroporation or viral vectors) [52, 53, 54]. The clarity of design, versatility, and efficiency of CRISPR/Cas9 make it an acceptable and widely used gene editing technique [55, 56]. Thus, leading to advances in induced mutagenesis [57, 58]. Nonetheless, there are some challenges related to the low mutation efficiency in Arabidopsis thaliana and Medicago truncatula compared to the improvement attained in monocot species [59, 60]. Several strategies are designed in optimising CRISPR/Cas9. These include decreasing sgRNA-Cas9 concentration and its length; and truncated gRNAs which result in achieving high on-target efficiency [61, 62, 63]. Other strategies also include the development of Cas9 variant enzymes, efficient expression of several sgRNAs, and promotor-activated expression of Cas9 [63].
Mutation breeding presents breeders an opportunity to overcome plant deficiencies without changing their original identity [64]. Identification of novel traits is supported via induced mutagenesis that could otherwise not be possible in a natural gene pool [65]. This is enhanced by the advent of molecular techniques which increase crop improvement programmes [66]. Non-targeted mutagenesis approaches offer a high possibility of identifying novel traits. The adoption of mutagenesis has engendered the discovery of several unique traits within mutagenized populations of several crops (Tables 1 and 2).
Plant species
Mutagen
Mutagenic significance
Reference
Hordeum vulgare L.
GR, X-ray & Ethylene imine
Enhances tolerance to low temperatures, drought, and frost
4. Contributions of mutagenesis in plant improvement
Mutagenesis has contributed extensively to generating a pool of plant genetic resources (PGRs) resulting in the development of smart, climate-friendly varieties which contribute to enhancing farming resilience, and return on investment for farmers. Mutant varieties have proven to have desirable traits such as tolerance to stresses (biotic and abiotic), higher yields, biofortification and generally, improvement of the genetic composition of plants (Tables 1 and 2).
4.1 Plant biodiversity and genetic resources
There is a constant loss of agricultural PGRs with approximately 37% of them going extinct [72]. Thus, the genetic base of most crops is narrowing and makes them succumb to environmental stresses. Plant biodiversity is key in limiting these consequences and induced mutation plays a vital role in supporting breeder to generate diverse genetic resources to mitigate current climate variations to achieve food security [73, 74, 75, 76]. Mutagenesis offers breeders a tool for generating crop variability in the shortest time as compared to traditional crosses [77]. Consequently, establishing and maintaining PGRs is pivotal to crop improvement. Mutation breeding allows plant breeders to work with farmers to breed varieties of crops that are high-yielding and more resistant to disease, resulting in the intensification of crop production (Tables 1 and 2). Breeding programs utilised PGRs generated via mutagenesis by increasing the gene pools for breeding purposes, development of genetic stocks with desirable traits, characterisation of PGRs, and cultivar development by improving farmers’ preferred cultivars with desirable traits. The availability of PGRs would contribute to overcoming the various challenges affecting plant growth and development. For instance, mutagenesis has resulted in creating 2577 mutant varieties only in 10 top countries across the globe the highest number of crop mutants developed (Figure 1) [67]. China and Pakistan have contributed to producing 817 and 59 mutant varieties respectively [67]. Similarly, several crops have received much attention in terms of induced mutagenesis. For example, 873 rice mutants have been developed, followed by barley (307 mutant), Chrysanthemum (285 mutants), wheat (265 mutants), soybean (182 mutant) and the 10th rank Dahlia (36 mutant crops) globally (Figure 2) [67].
Figure 1.
Top 10 countries in the world highest number of mutants crops developed [67].
Figure 2.
Top 10 crops having highest number of crop mutants [67].
4.2 Biotic stress resistance
Population increase coupled with modernization usually leads to significant changes in the environmental forces that influence the production of agricultural goods. The environmental forces mainly arise from biotic and abiotic elements. The biotic force arises from the actions of fungi, bacteria, viruses, nematodes, and pests, among others. These trigger stress by impeding plants’ growth and development, eventually leading to reduction in yield as well as value. Therefore, it is imperative for crop improvement strategies to be used to devise approaches to counter the effects of biotic stress. Hence, the application of mutation breeding in overcoming biotic stress is crucial and it has proven to be successful. Plant breeders improve plants by generating plant genetic resources by mimicking the process of spontaneous mutation that exists in nature. Exposure of plants to stress triggers a complex and redundancy signals, perception and expression levels crosstalk among several pathways in order to overcome the stress. This demands an array of plants with varied genetic backgrounds, biochemical and metabolic variations to generate alleles required for engineering plants to tolerate biotic stresses.
Stress caused by disease-causing organisms in plants has witnessed improvement in combating them. A number of plants are developed to offer resistance to particular pathogens and insects. The durability of this tolerance is questioned due to the development of biotypes of pathogen strains stimulating breeders to generate new resistance against the biotic stresses that have newly emerged [78]. Many biotic stresses such as fungi, viruses, bacteria, nematodes, and insects interrupt the structure of plants. They are known for causing about 20–40% losses in agricultural production [79]. Specifically, in leguminous crops such as chickpea, common bean, faba bean and alfalfa, Sclerotinia sclerotiorum causes yield loss of up to 100% whiles affecting their seed quality and the entire plant function [80]. To mitigate the problem of hunger, techniques that increase pathogens’ resistance to host crops to reduce their damage to crop production are required [81]. Plant scientists have developed crops against most of these stresses via mutagenesis approaches (Table 1). This is facilitated by plant molecular genetics making induced mutation a highly efficient technique for studies in plants leading to introgression of desirable traits in several crops such as rice, soybean, wheat, and sesame [24]. Although classical plant breeding has engendered the development of novel traits in plants, however, it is time-consuming. On the contrary, mutation breeding is affordable, safe and has no legal restriction on its application. Induced mutagenesis is facilitated by the evolving next-generation sequencing (NGS) and its non-destructive evaluation systems limiting the time frame, and labour needed for mutation breeding. It is undoubted that, for decades to come, induced mutation will retain its value in plant science especially when complex trait improvements such as diseases, and pests are involved. Currently, mutation techniques ranging from physical, chemical, gene editing (CRISPR/Cas9, TALEN-based, VIGS, RNAi interference) are employed in combating biotic stresses conforming plants. For instance, 10 different disease stresses in rice (Oryza sativa L.) are improved via mutagenesis using different approaches (Table 1). Application of EMS in soybean (Glycine max L.) has resorted in the development of Chlorsulfuron-Resistant soybean [27]. Resistance of grapevine (Vitis vinifera), and tomato (Solanum lycopersicum L.) to powdery mildew diseases caused by fungus have been reported to be promoted via induced mutagenesis (Table 1) [36, 38]. Similarly, bacteria blight disease in rice (O. sativa) is reduced by CRISPR/Cas9 mutagenesis through base insertion/deletion of genes (OsSWEET11, 13 and 14; OsXa13/Os8N3; OsAvrXa7) (Table 1) [35, 39, 40]. Data shows the power of gene editing and physical mutagens in recent decades in improving plants’ tolerance/resistance to biotic stresses (Table 1).
4.3 Abiotic stress resistance
The sessile nature of plants makes them very susceptible to the adverse effects of abiotic stress such as cold, heat, flood, drought, salinity, heavy metals, reduced or excessive UV radiation, acidity, alkalinity, and nutrient-deficient soils [82, 83]. Abiotic stress happens to be the primary cause of crop loss globally and leads to an annual yield loss of over 50% in major crops [84].
In our quest to sustain agricultural production and food supply, numerous attempts are being made to generate mutant varieties that can withstand abiotic stress in light of climate change, with the use of various plant-breeding techniques. Currently, mutation breeding has successfully generated superior varieties of legumes, grains and cereals, roots and tubers, cotton, and sugarcane that are high yielding, and tolerant to some abiotic stresses. The mutant variety database (MVD) hosts 3402 mutants of which around 160 mutant varieties are tolerant to abiotic stresses [67]. For instance, ‘Zhefu 802’, a mutant rice variety developed in China is resistant to low temperatures [85]. In Pakistan, induced mutation in Basmati 370 rice generated a new variety “Kashmir Basmati” that has tolerance to cold, matures early and retains parental traits such as cooking quality and aroma [86]. Table 2 presents a highlight of breakthroughs made through induced mutation to improve resistance to abiotic stresses of different crops.
4.4 Nutritional and quality trait improvement
The nutritional qualities of crops are of concerns to humankind. In the worldwide efforts to feed a growing and nutritional demanding human population, mutation breeding is a crucial strategy [87]. Several mutational breeding has targeted enhancing phytonutrients, essential minerals, proteins, and oil for humans and animals. Mutation breeding have played a crucial component in developing variant cultivars having spurious modifications in genes using insertion mutagenesis such as T-DNA insertion in rice, transposon or retrotransposon tagging in maize or rice, and chemical/irradiation mutagenesis that produces new characters for crop improvement [88]. Classical examples are the mutant varieties namely Zornitsa, Madan, and NIFA-Mustard Canola developed with enhanced oil and protein content [67]. Similarly, the nutritional component of rice mutants has been improved compared to its wild type [89]. The development of mutant crops from soybean, rice, wheat and barley have witnessed increases in their bioavailability of nutrients and minerals [90]. The ratio of oleic to linoleic acid has been enhanced and the palmitic acid content in peanut has been reduced through induced mutation [91]. The β-carotene levels in pepper fruits were increased by creating mutants through the application of physical and chemical mutagens [92]. Similarly, in rapeseed application of EMS result in improve its genetic composition in terms of oil content and fatty acids [93].
Induced mutation has proven essential for close to 100 years generating genetic variations and subsequent release of mutant cultivars. Bottlenecks to mutation breeding arise from its lethal, low rate, laborious screening process, and most mutations being recessive, among others. Radiation mutation breeding now takes advantage of space projects as this seems to become common in the future. Specifically, the space environment denotes outer space outside the atmosphere and is accompanied by microgravity, radiation, and alternating magnetic fields. This field will offer more openings for mutation breeding as space breeding provides a high rate of mutation, in several directions [94]. Aerospace (space) mutation is applied in developing a new variety [95]. Crop space breeding studies have been carried out in China since 1987 and shreds of evidence showed have been encouraging resulting in the release of 66 mutant varieties, which include crops such as tomato, pepper, rice, wheat and sesame [96]. This is evident that, in the future countries can tap into the space breeding procedures. This is due to its associated benefits such as resulting inducing genetic changes in the seed of crops and chromosomal aberrations surge in the seeds attributed to the combined effects of cosmic radiation and microgravity. More efforts will concentrate on cooperating mutagenesis, PCR-based methods, and mapping techniques (NGS techniques) to explore further the function of key genes and to embrace integrative platforms to advance functional genomics innovations.
Induced mutagenesis is key to contributing to food security by developing climate-smart crops. Hence, it represents a tool in fighting against hunger, and malnutrition whiles increasing farmers’ profit margins. The usage of mutagens such as chemical agents is easy and does not require high skills making it user-friendly. The key challenges in mutation breeding are the low efficiency in targeted mutagenesis resulting in off-target and random mutation. Current efforts are geared towards embracing PCR-based methods, and NGS techniques in induced mutagenesis. This integration offers the opportunity for reverse breeding and to explore keys and their roles in plants. In summary, multi-omics and precise mutagenesis interventions improve plant yields and qualities by developing climate-smart crops.
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Written By
Augustine Antwi-Boasiako, Padmore Adu-Antwi,
Richard Adu Amoah, Augustine Boakye Boateng, Joseph Gyau,
Matilda Frimpong, Isaac Newton Boakye-Mensah and
Ivy Odi Ahiamadia
Submitted: 14 May 2023Reviewed: 01 June 2023Published: 12 July 2024
Open access peer-reviewed chapter - ONLINE FIRST
