Recent advances in genome editing strategies for balancing growth and defence in sugarcane (Saccharum officinarum)
Maira Tanveer
A , Zain Ul Abidin A , Hussam F. Najeeb Alawadi B , Ahmad Naeem Shahzad C , Athar Mahmood D * , Bilal Ahmad Khan E , Sameer Qari F and Hesham Farouk Oraby G H *
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Abstract
Sugarcane (Saccharum officinarum) has gained more attention worldwide in recent decades because of its importance as a bioenergy resource and in producing table sugar. However, the production capabilities of conventional varieties are being challenged by the changing climates, which struggle to meet the escalating demands of the growing global population. Genome editing has emerged as a pivotal field that offers groundbreaking solutions in agriculture and beyond. It includes inserting, removing or replacing DNA in an organism’s genome. Various approaches are employed to enhance crop yields and resilience in harsh climates. These techniques include zinc finger nuclease (ZFN), transcription activator-like effector nuclease (TALEN) and clustered regularly interspaced short palindromic repeats/associated protein (CRISPR/Cas). Among these, CRISPR/Cas is one of the most promising and rapidly advancing fields. With the help of these techniques, several crops like rice (Oryza sativa), tomato (Solanum lycopersicum), maize (Zea mays), barley (Hordeum vulgare) and sugarcane have been improved to be resistant to viral diseases. This review describes recent advances in genome editing with a particular focus on sugarcane and focuses on the advantages and limitations of these approaches while also considering the regulatory and ethical implications across different countries. It also offers insights into future prospects and the application of these approaches in agriculture.
Keywords: allelic variants, CRISPR, genomics, NHEJ, sugarcane, TALEN, transgene, zinc finger nuclease.
Introduction
Sugarcane (Saccharum officinarum) is a major crop cultivated in different regions worldwide. Sugarcane is classified as a member of the Poaceae family, Saccharum gender and the Andropogoneae tribe (Mirajkar et al. 2019). Over 70% of the world’s sugar comes from sugarcane, which is grown in the essence of producing sugar. It also offers a renewable and sustainable bioenergy source (Cheng et al. 2019). According to the OECD-FAO (Organisation for Economic Co-operation Development–Food and Agriculture Organization) Agricultural Outlook 2019–2020 report, 174 million tons of sugarcane was produced in ~80 countries from approximately 24.9 million ha of land (Hussain 2023). Sugarcane is a C4 crop and is often regarded as one of the most favourable crops for bioenergy production. Countries like Brazil rely almost entirely on sugarcane as it is their primary source of ethanol feedstock (de Moraes Barbosa et al. 2021). The volume of sugarcane ethanol that Brazil produced in 2019–2020 was 32.5 billion L. It is now the organisation that makes the most sugarcane ethanol globally. The United States of America and Brazil are responsible for 85% of total ethanol production globally (Sanches et al. 2023).
Two species, Saccharum officinarum and Saccharum spontaneum, were involved in the interspecific hybridisation that resulted in the contemporary sugarcane cultivars. Approximately 70–80% of the genome is derived from S. officinarum, and 10–20% from S. spontaneum. However, the other 10% results from the interspecies recombination (Wiangwiset et al. 2023). In addition to being extremely aneuploid, polyploid and heterozygous, the sugarcane genome comes in at approximately 10 GB, making it the largest of any other member of the Poaceae family. Most sugarcane cultivars have between 110 and 130 chromosomes (Tripathy 2022). Since the beginning of time, the primary focus of sugarcane crop development has been increasing the amount of sucrose present. However, in recent years, fibre, lignin content and biomass have become essential components of advanced breeding approaches (Ali et al. 2019). It has been proven that the diversity of genes present in the active germplasm banks would be a critical factor in determining the progress of sugarcane breeding efforts that aim to acquire desirable traits (Cursi et al. 2022). Regarding cultivar development, increasing conservation and management significantly impacts the availability of germplasm collections that frequently involve accessions from various gene backgrounds and measuring the genetic diversity in these collections (Franco-Duran et al. 2019). Frequent developments in biotechnology have resulted in the development of effective methods and tools that enhanced conventional breeding programs. Interpreting gene architectures, genomic locations and plant development uses these practical tools and techniques (Ahmar et al. 2020a). The structure and composition of the sugarcane genome have been the subject of a significant number of molecular research. All of these research outcomes have shown that the sugarcane genome is more critical than 10 GB per pixel and that genes may reside in up to 10–12 different allelic variants (Zhang et al. 2022). The estimated size of the monoploid genome may vary anywhere from 800 to 900 MB due to the ploidy level of the sugarcane (Das et al. 2018).
This review article is focused on the emergence and utilisation of genome editing technologies in sugarcane crops. The first part describes the main background of the sugarcane crop, its production and its role in agriculture. The second and third parts highlight the significance of genome editing technologies and their utilisation in improving crop production, growth and defence from diseases. The mechanisms and applications of clustered regularly interspaced short palindromic repeats/associated protein (CRISPR/Cas), zinc finger nucleases (ZFN) and transcription activator-like effector nuclease (TALEN) are thoroughly examined in sections ‘Recent advances in genome editing for sugarcane’ and ‘Genome editing technologies’. Applications in sugarcane are covered in ‘Applications of genome editing in sugarcane improvement’, with a focus on beneficial trait modification and disease resistance. Finally, we describe global ethical and regulatory considerations, future perspectives and conclusions.
Significance of genome editing
Genome editing (GE) is a type of genetic modification where DNA is inserted, removed or replaced in an organism’s genome using specialised nucleases (Petersen 2017). These nucleases synthesise site-specific double-strand breaks (DSBs) in the genome at specified places. Targeted mutations are produced as a consequence of the repair of induced DSBs by either non-homologous end joining (NHEJ) or homologous recombination (HR) (Yang et al. 2020).
Due to the constantly expanding population of the globe, there is a rising need for resources that can provide both food and energy. The demand for species has been growing, and natural species cannot meet it (Fukase and Martin 2020). Scientists have put significant effort into creating crops with a consistent yield, high quality and high resilience to biotic or abiotic challenges (Rivero et al. 2022). The techniques used for crop breeding are continuously being refined because of recent accomplishments and developments in biotechnology. At the beginning of the 20th century, the first artificial nuclease was developed, which made it possible to modify genomes in living organisms. ZFN, TALEN and CRISPR/Cas are the three nucleases that achieve the highest level of technological advancement and are applied widely around the globe (Surabhi et al. 2019). Interchangeable recognition and cleavage domains are the core components of all three genome-editing systems. These domains are also the most critical components. Before any other action, the recognition domain directs the cleavage domain to a particular spot on the genome. After that, the cleavage domain will cleave the DNA in a specific location. Later, this DNA break could be repaired by a process known as NHEJ (Guha et al. 2017). Gene segments will be inserted in line with the repair, the mutation of genes, and changes in the structure of chromosomes, all of which will ultimately result in alterations to the function of the original gene (Fig. 1) (Raina et al. 2021). Through the interaction of proteins and DNA, ZFNs and TALENs can bind DNA. CRISPR/Cas can locate the target location by exchanging RNA and DNA. Crop breeding is one of the many research areas where these highly effective genome-editing tools could be applied. They enable researchers to grow and generate new types of crops by increasing their agronomic hallmarks or resilience to climatic challenges (Das et al. 2022).
Application of CRISPR/Cas9 for development of stress tolerant plants (Razzaq et al. 2021). sgRNA, single guide RNA.
Recent advances in genome editing for sugarcane
According to Jung and Altpeter (2016), the first known case of sugarcane genome editing was discovered by knocking out the COMT gene in sugarcane using TALENs to reduce the amount of lignin in the plant. It was noted that between 8% and 99% of the wild-type COMT alleles could be changed in different lines, and they were successful in achieving target alterations in 74% of the transgenic lines that they developed. During the glasshouse experiments, the transgenic events with a mutation frequency of 99% showed a decrease in lignin content that ranged from 29 to 32% compared to the control plants that had not been transformed. Furthermore, regarding the vegetatively replicated clones, neither the mutations nor the mutant phenotypes exhibited any changes. However, it has been suggested that ‘biological plasticity’ might occasionally protect knockout target activity even though it is not evident why a mutation frequency of 99% only induced a decrease of 29–32% in the amount of lignin.
Recently, it has been discovered that using genomic selection (GS) approaches in sugarcane to predict important cane features has resulted in high prediction accuracy (Islam et al. 2022). G-BLUP, BayesR and genomic single step (GenomicsSS) were the three genomic prediction methods used to evaluate the GEBV (genomic estimated breeding values) accuracies for flowering features. These flowering traits included days to flowering, pollen and gender viability, and they also had a high heritability of 0.57, 0.78 and 0.72, respectively (Meena et al. 2022). According to the prediction accuracy for many attributes (ranging from 0.3 to 0.44), GS can be used in sugarcane breeding programs to enhance these features (Meena et al. 2022). In a breeding program in Australia, Deomano et al. (2020) discovered that the genomic prediction accuracies for sugar and cane yield were optimistic, coming in at 0.25 and 0.45, respectively.
With CRISPR/Cas9 technologies, the gene for magnesium chelatase was modified in sugarcane using CRISPR/Cas9, which allowed for the effective editing of several alleles (Eid et al. 2021). Oz et al. (2021) successfully achieved efficient and repeatable gene targeting in sugarcane in a different study. This was a significant achievement for them as it made it feasible to accurately co-edit various alleles of the herbicide-resistant acetolactate synthase (ALS) gene by using template-mediated and homology-directed repair (HDR) to repair DNA DSBs generated by CRISPR/Cas9.
Genome editing technologies
GE technologies directly target specific genes (genes of interest) for modifications in a particular species (Ahmar et al. 2020b). GE gives plant breeders significant opportunities for the improvement of food production. Furthermore, gene insertion or long-lasting allele knock-out can now accomplish function (Weeks et al. 2016). Knock-out phenotypes can be created using genome editing. Researchers from the field of molecular biology take advantage of different possibilities by targeting specific genes more easily with the utilisation of gene editing technologies (Thurtle-Schmidt and Lo 2018).
Plant breeders have produced several new cultivars with desired traits via genome editing. GE technologies may effectively silence or insert genes that produce specific functions or characteristics (Duensing et al. 2018). Several genetic engineering technologies have been introduced to operate the genomes of eukaryotic organisms, including plants. These techniques include mega nucleases, CRISPR/Cas9, TALENs and ZFNs. From these techniques, CRISPR/Cas9 is one of the most widely used technologies for genetic modifications (Platani et al. 2023). Other approaches, like ZFN and TALEN, are time consuming and cost-effective because they use extensive technological designs to accomplish particular targeting (Sanagala et al. 2017).
CRISPR/Cas9 system
CRISPR is a well-defined bacterial defence system that has been adapted for use in genome editing. CRISPR/Cas systems consist of various varieties where the effector modules of each type contain hallmark proteins characterised by their specific structure (Tyagi et al. 2021). Modifications in eukaryotic organisms’ genomes are done using this advanced technology known as the CRISPR/Cas9 system (Tyagi et al. 2020). Cas9 nuclease and single guide RNA (sgRNA) are the two significant parts of the CRISPR/Cas9 system. Single guide RNA attacks the target sequence of the genome, and the other part, Cas9 nuclease, directs the cleavage of that sequence (Boyle et al. 2021). In the target sequence, a 3′-NGG motif known as PAM (protospacer adjacent motif) is present, and that target sequence is recognised by sgRNA (Corsi et al. 2022). Any DNA with sequence complementarity to the first 20 nucleotides of the single guide RNA can potentially be a target.
Conversely, PAM must be present at the 3′ end of the DNA targets for DNA to be cut (Anzalone et al. 2020). The pattern sequence of PAM may differ significantly depending on the source of the bacteria that gave rise to the CRISPR system and the Cas protein variants employed. By a significant margin, the CRISPR/Cas9 system is often taken from Streptococcus pyogenes (Sp). SpCas9 has a PAM sequence identified as 5′-NGG (Wu et al. 2023).
DNA, messenger RNA (also known as in vitro transcripts or IVT) and protein format are all potential methods for delivering CRISPR components into the plant genome (Mirajkar et al. 2019). Many plant transformation methods may be used with the DNA format. Some available delivery methods are electroporation, virus-based, agroinfiltration, Agrobacterium infection, biolistics or particle bombardment, and PEG-mediated transformation (Mohan et al. 2022). Using mRNA as a delivery method for genome-editing reagents is also effective. This transitory administration leads to stable transgenic events and has fewer off-target effects than other delivery methods (Chen et al. 2021).
Another significant feature associated with the CRISPR technology is that it may be used to control the expression of genes. Cas9 is modified into an inactive form known as dCas9 (‘d’ stands for dead), which is then used for particular gene activation (also known as CRISPRa or CRISPR activation) or suppression (also known as CRISPRi or CRISPR interference) (Karlson et al. 2021). Genetic diversity is essential for boosting agricultural yields via plant breeding. Plant breeders rely on various crop genetic resources and breeding methods to incorporate genetic diversity to produce more effective cultivars (Saini et al. 2020). Currently, the CRISPR/Cas technology presents remarkable new possibilities to generate genetic diversity for breeding in a way that has never been possible. For example, multiple articles have used the CRISPR/Cas system to alter regulatory regions or components to produce a range of new alleles with different expression levels (Ahmad 2023).
Transcription activator-like effector nuclease (TALEN)
Transcription activator-like effector (TALE) is a family of proteins secreted by the plant pathogenic bacterial species (Xanthomonas spp). Usually, the type III secretion system is used to introduce these proteins into plant cells, where they activate the transcription of particular target genes that cause plant disease (Khojasteh et al. 2020). In every TALEN, there is a core DNA binding domain that is made up of a varied number of repetitions of 33–35 amino acids. Two variable amino acids, RVDs (repeat variable di-residues), whose repetitions are almost similar, are located at 12 and 13 positions (Becker and Boch 2021). A particular TALEN’s DNA target sequence depends on the RVD composition and repetition number. Each repeat variable di-residue is intended to recognise a single specific nucleotide (Anderson et al. 2020). A chimeric protein known as TALEN consists of two main domains. The first is a FokI nuclease domain, and the other is a TALE DNA binding domain.
Additionally, a pair of TALENs is used to cut the targeted area of DNA when combined with ZFNs (Shankar et al. 2018). For gene editing via TALENs, the first investigated species was yeast. In plant breeding and protection, TALEN technology introduced significant advancements and discoveries (Kurita et al. 2022).
A comprehensive view of the risks, public perception and challenges associated with using non-transgenic methodology in modern agricultural practices (Fig. 2) (Lassoued et al. 2019). Scientists used TALENs for GE for almost all significant crop plants like Arabidopsis thaliana, barley (Hordeum vulgare) and tobacco (Nicotiana tabacum) (Ansari et al. 2020). TALEN technology has been used in potatoes and tobacco to generate mutations in the target gene, referred to as ALS (acetolactate synthase) (Olusola et al. 2021). TALENs have been used to edit the corn glossy2 (gl2) gene and the S. lycopersicum PROCERA gene to generate heritable mutations. TALEN has been used to grow fragrant rice (Oryza sativa) that resists blast disease and bacterial blight. These studies show that the TALEN system is vital for crop improvement (Char et al. 2019).
TALENs-mediated gene alteration is an adaptable and cutting-edge technology for site-specific modifications of plant genomes. It can significantly impact and considerably influence crop development (Bhardwaj and Nain 2021). Mirajkar et al. (2019) suggested that TALEN-mediated genome alteration has been implemented in several plant species (Table 1). Rice was the first crop to be investigated as being improved using TALEN technology. Blight disease is produced by a pathogen known as Xanthomonas oryzae, which causes a significant loss in rice production each year worldwide (Yugander et al. 2017).
| Genes | Plant species | TALEN assembly technique | Delivery methods | References | |
|---|---|---|---|---|---|
| BdABA1, BdMC6, BdCO11 | Brachypodium distachyon | Golden Gate | Agrobacterium-mediated and Protoplast transformation | Shan et al. (2013) | |
| FAD2-1A, FAD2-1B | Glycine max | Golden Gate | Agrobacterium-mediated transformation | Haun et al. (2014) | |
| HvPAPhy | Hordeum vulgare | Golden Gate | Agrobacterium-mediated transformation | Wendt et al. (2013) | |
| TaMLO-A1, TaMLO-B1, TaMLO-D1 | Triticum aestivum | Golden Gate | Protoplast and Biolistic transformation | Wang et al. (2014) | |
| SurA, SurB | Nicotiana tabacum | Golden Gate | Protoplast transformation | Zhang et al. (2013) | |
| ZmIPK1A, ZmIPK, ZmMRP4 | Zea mays | Golden Gate | Protoplast and Agrobacterium-mediated transformation | Liang et al. (2014) | |
| PROCERA | Solanum lycopersicum | Golden Gate | Agrobacterium-mediated transformation | Lor et al. (2014) |
Zinc finger nucleases (ZFNs)
At the beginning of the 1990s, ZFNs were synthesised using the type IIS restriction enzyme FokI, which had separate recognition and non-specific cleavage domains (Namo and Belachew 2021). Scientific studies have extensively used ZFN, the first ‘genome-editing nuclease,’ to make it accessible for purchase. The use of ZFN in plant breeding has shown to be beneficial for various plants, including Arabidopsis, tobacco, soybeans (Glycine max) and rice (Bilichak et al. 2020). ZFNs may modify and change the genome by deletions, insertions, point mutations, duplications, inversions and translocations. This makes ZFNs useful for genomic modifications. ZFNs were the first GE nucleases to achieve broad usage and reputation for breeding various plants and animals (Ricroch 2019). ZFNs have been used by scientists as a breeding technique in several plant species, including multiple types of crops. Furthermore, ZFN continues to be widely used in biomedicine (Bhambhani et al. 2022).
In one crop breeding experiment using ZFNs, the insertion of PAT gene cassettes disrupted the maize gene ZmIPK1. This disturbance altered maize seed inositol phosphate profiles and herbicide tolerance (Rana et al. 2022). American Dow Agro-Sciences researchers were competent in effectively changing a particular endogenous gene in tobacco by using ZFN technology. Because of this alteration, tobacco can resist herbicide-based treatments (Rout et al. 2023). A few months later, scientists working for the same company used the same method to create herbicide-tolerant maize by editing the maize IPKI gene and adding the pat herbicide resistance. This procedure was required to achieve the desired outcome (Sharma et al. 2023).
Other genome editing tools
Gene knock-ins, base editing and prime editing have been developed as methods for genome editing based on the CRISPR/Cas system that is more focused and maintains fidelity to the particular nucleotide (Wada et al. 2020). Gene knock-in allows site-specific mutagenesis by HDR repair after a DSB. Because plant cells rarely repair HDRs, gene knock-in remains inefficient and unknown (Li et al. 2024). Generation of alterations targeted explicitly to specific genes is also possible through base editing. Unlike knock-ins, individual base pairs may be altered without causing a DSB with a base editing (Edmondson et al. 2021). It is possible to merge a Cas9 enzyme that has been rendered catalytically inactive (dCas9) or a Cas9 nickase with a base editor, both of which keep their ability to precisely bind to DNA via a gRNA (guide RNA) (Wang et al. 2022).
Watermelons (Citrullus lanatus) that have undergone base editing are resistant to herbicides because base editing has been demonstrated and applied in plants, especially in orphan crops. Furthermore, natural polymorphisms for disease resistance in model species have been replicated via base editing (Chen et al. 2019). With fewer restrictions, prime editing provides the same benefits as ‘find and replace’ gene editing. Prime editing gRNA (pegRNA) with high specificity and a modified Cas endonuclease is used to achieve this. Although studies have not yet shown phenotypic findings, excellent editing will be extensively employed in all crops, including sugarcane, as a consequence of increased attempts to enhance the efficiency of the process (Venezia and Creasey Krainer 2021).
Applications of genome editing in sugarcane improvement
For sugarcane, there are not any reports about how the CRISPR/Cas system has been used to make virus-resistant crops (Khan 2023). Usually, two methods are used to make viruses less likely to spread: (1) engineering the virus; and (2) changing human factors needed for virus reproduction. A successful use of the CRISPR/Cas system was in plants to make them resistant to single stranded DNA (ssDNA) geminiviruses. Single stranded RNA (ssRNA) and double stranded DNA (dsDNA) viruses are the primary causes of viral infections that affect sugarcane (Surya Krishna et al. 2023a). Several crops have shown that breeding technologies can make plants resistant to pests and diseases (Fig. 3). Four principal viral diseases may harm sugarcane: (1) sugarcane mosaic disease; (2) sugarcane leaf fleck disease; (3) sugarcane yellow leaf disease; and (4) sugarcane Fiji disease. Notably, the first three of these are destructive and may be found all over the globe, resulting in significant harm to sugarcane production (Holkar et al. 2020). GE of host-sensitive components would be a potential technique to create resistance to mosaic and yellow leaf diseases in sugarcane. These diseases are caused by ssRNA viruses responsible for the disease (Putra et al. 2023). The CRISPR/Cas system has effectively created viral resistance in various plant species (Table 2).
Breeding technologies for sugarcane genetic improvement against disease and pest resistance (Iqbal et al. 2021).
| Plant | Virus | Cas system | Gene | References | |
|---|---|---|---|---|---|
| Rice | Rice Dwarf Virus | LshCas13a | Three regions of SRBSDV | Khan et al. (2022) | |
| Rice Tungro Spherical Virus | spCas9 | eIF4G | |||
| Cotton | Cotton Leaf Curl Virus | spCas9 | Six regions of CLCuVs | Binyameen et al. (2021) | |
| Cotton Leaf Curl Virus | spCas9 | Three regions of CLCuVs | |||
| Potato | Potato Virus Y | Cas13a | P3, CI, Nib, CP | Tiwari et al. (2022) | |
| Potato Virus Y | spCas9 | eIF4E1 | |||
| Potato Virus Y | spCas9 | eIF4E | |||
| Soybean | Soybean Mosaic Virus | dpCas9 | GmF3H1, GmF3H2 and GmFNSII-1 | Cao et al. (2020) | |
| Cucumber | Cucumber Vein Yellowing Virus | spCas9 | eIF4G | Mahas and Mahfouz (2018) | |
| Tomato | Tomato Yellow Leaf Curl Virus | spCas9 | IR, CP, Rep | Tashkandi et al. (2018) | |
| Pepper Mottle Virus | spCas9 | eIF4E1 | |||
| Tomato Yellow Leaf Curl Virus | spCas9 | SlPelo | |||
| Tobacco | Tobacco Mosaic Virus | LshCas13a | Five regions of TMV | Jogam et al. (2023) |
CRISPR/Cas9 system is commonly utilised for gene knockout, which is a method of disrupting gene expression. Gene knockouts are not the only applications for the CRISPR/Cas9 technology; they may also be used to delete an entire gene at a particular location or erase a chromosome (Chojnacka-Puchta and Sawicka 2020). Other applications of CRISPR technology include replacing and repairing a malfunctioning allele and generating an opening for integrating a gene at a particular location (Nidhi et al. 2021). Using CRISPR/Cas9, mutations were effectively generated in all four alleles, completely deleting potatoes’ granule-bound starch synthase (GBSS) enzyme activity (Tussipkan and Manabayeva 2021).
Another example that illustrates the potential of such a strong technique is editing the tomato genome using TALENs to modify the PROCERA gene. They developed a TALENs construct regulated by an oestrogen-activated XVE promoter to achieve this goal. A very modest degree of mutation occurred due to spraying plants with oestradiol. After that, they repeated the process of immersing the cotyledons of T1 plants in a solution that contained oestradiol at weekly intervals (Salava et al. 2021). Because of segregation, it was shown that the TALEN construct was lost, and the changed plants carried the intended mutations. These mutations were inherited stably. To target many genes in various plant species, including H. vulgare, N. tabacum and Brachypodium, TALENs have been effectively used for multiple purposes (Vats et al. 2019).
Scientists used TALENs to target the promoter region of the HvPaphya phytase gene in barley (Haq et al. 2022). Multiple INDELs (insertions and deletions) were found in 16–31% of the stable altered plants (Liu et al. 2019). In soybean, site-directed mutation was performed using TALENs. Oleic acid converts into linoleic acid through desaturase genes of fatty acid (FAD2-1A and FAD2-1B), which were their attack targets. Plants with solid transformations precisely altered the desaturase gene (Heddleson and Kodali 2022). ZFNs could efficiently knock out or replace the two paralogues of ALS (SuRA and SuRB) detected in tobacco (Ansari et al. 2020). In a later study, Cantos et al. (2014) used ZFNs to locate safe locations for gene integration in rice. The discovered sites should be able to function as dependable loci for further gene insertion and trait stacking. In addition, Rajput et al. (2023) revealed that ZFN homologous recombination may be used to modify rice via genetic engineering.
It is expected that in the coming years, sugarcane biotechnology will make advances that will increase crop value and usefulness while also improving production. These improvements are projected simultaneously (Huang et al. 2020). Several biotechnological techniques have been created over the last two and a half decades to increase the sugarcane yield and quality. Multiple molecular marker systems have been developed for trait mapping, varietal identification and diversity analysis research (Singh et al. 2019). Significant advancements have been made in sugarcane’s functional genomics since the SUCEST (sugarcane expressed sequence tag) investigation that contains 23,800 ESTs from 26 cDNA libraries, 1069 ESTs and 26,000 tissue-specific ESTs accomplished from red rot-infected tissue (Ali et al. 2019). Various molecular markers based on EST have been developed to estimate sugar content and yield and perform other quantitative and qualitative analyses related to these factors. It has been discovered that sugarcane has many quantitative trait loci (QTLs) associated with the number of tillers, suckering, sugar content and yield-related variables (Mahadevaiah et al. 2021).
Sugarcane has been identified as a polyploid plant, which indicates that it has many sets of chromosomes. Despite this, it has a minimal number of recombinant chromosomes because it behaves in a diploidised manner. Conventional plant breeders face a tremendous challenge (Oliveira et al. 2023). By utilising techniques that are rapidly developing, such as ZFNs, TALENs, single-stranded oligonucleotides, RNA-guided engineered nucleases and type II CRISPR/Cas9, which are associated with many polyploid crops, it has become possible to edit some or all the genes that are intended to be modified on homologous chromosomes. This has brought about a significant advancement in the field of genetic engineering. Some of these approaches involve enhancing essential plant characteristics and disease resistance (Rana et al. 2022). Because sugarcane is the most crucial source of white sugar in the world and also plays a role in producing ethanol and biofuels, it is predicted that sugarcane will be a primary target for gene editing (Khan et al. 2019). CRISPR/Cas9, the newest crop plant technology, is more flexible than ZFNs and TALENs. Although it is being used successfully in several crop plants, its application to sugarcane has been limited (Rasheed et al. 2021). By protecting against both biotic and abiotic challenges, the development of engineered sugarcane will improve it more rapidly. As a result of the absence of any alien DNA, non-genetically modified (GM) sugarcane will be subject to fewer regulatory constraints. The social system will accept it to a far greater extent (Shrivastava et al. 2017).
Applications in balancing growth and defence
GE technology has progressed in the agriculture field. It has been used to change plant morphology, provide disease resistance and overexpress genes to improve physiological processes occurring in plants. The abilities associated with growth and defence against pests and diseases in sugarcane plants can be enhanced via precise genetic modifications. For example, precise genetic modification may augment the expression of genes linked to growth, resulting in higher yields and enhanced sugar content. Through these genomic techniques, different strategies are employed for getting positive results. These include the knock-out technique, the knock-in technique and the gene replacement (Zhang et al. 2017).
Modifying crop plants and improving plant growth and production through plant breeding is becoming necessary. Genomics techniques like CRISPR/Cas9 or TALEN modify interested trait genes in plants to achieve balanced growth and higher crop yield. Using these genome editing strategies with plant breeding, specific genes in a plant are transformed, which enhances plant growth and looks identical to their parent plant. Zhang et al. (2018) also reported that genome editing is the most significant advancement in plant breeding. In their study, Xia et al. (2021) revealed that these genome editing techniques (ZFN, TALEN and CRISPR/Cas system, CBE) were used in tomato plant breeding for fruit ripening and resistance to stress. CRISPR/Cas tools were also employed in other studies, which enhanced rice plant growth and wheat (Triticum aestivum) kernel production (Xu et al. 2016; Zhang et al. 2016). The development of non-transgenic CRISPR-edited sugarcane varieties with altered cell wall components and high sucrose content, like Cana Flex I and Cana Flex II in Brazil, is one example of successful applications in the crop (Touzdjian Pinheiro Kohlrausch Távora et al. 2022).
Nitrogen use efficiency is a complex trait controlled by several plant genes associated with nitrogen assimilation, absorption and metabolism. Nitrogen metabolism is essential to plant growth and development (Iqbal et al. 2020). Genome editing tools have been used in rice plants for nitrogen metabolism by transporters of the NRT1/NPF family (Lebedev et al. 2021). To improve nitrogen use efficiency, specific genes that enhance the absorption and utilisation of nitrogen by plants are introduced. As reported in the Tiwari et al. (2020) study, NAC2-5A and TFs genes were introduced in wheat and rice plants, improving nitrogen use efficiency. In context to photosynthesis, genes like OsHXK1 are introduced in plants like rice through CRISPR/Cas method for improved photosynthesis and higher crop yield.
Similarly, Chen et al. (2020) have reported that overexpressing the D1 protein through a nuclear origin supplementation pathway is a helpful bioengineering strategy to improve photosynthetic efficiency and boost crop yield under changing climate conditions. A study by Garcia Tavares et al. (2018) revealed that genetic manipulation, including gene editing to target ScGAI, can be an excellent method to increase sugarcane yield and sugar accumulation. Moreover, Eid et al. (2021) used the CRISPR system to modify the multiallelic magnesium chelatase subunit I (MgCh) gene, a primary component for chlorophyll biosynthesis. Sanger sequencing verified that they had effectively targeted 49 copies/alleles of the MgCh gene with CRISPR/Cas9. The modified plants showed a phenotype with light green to yellow leaves, proving that genome editing in polyploid crops is possible.
With the assistance of genetic engineering technologies, plants have been genetically engineered to develop antiviral defences through RNA interference, a post-transcriptional gene silencing technique. Recently, new genome editing techniques like ZFN, CRISPR/Cas and TALEN have revolutionised the tools available to confer virus resistance in plants (Romay and Bragard 2017). The CRISPR/Cas tool adds and deletes genes from plants; genes causing diseases in plants can be removed through the CRISPR/Cas tool (Mohan 2016). A 1.6-kb GUS gene was eliminated by Mohan et al. (2022) targeting both ends of the gene with two gRNAs and Cas9. Different methods of plant breeding have also been used for plant disease resistance, such as fast breeding platforms, precise genome editing and high thrash-out genotyping (Wei et al. 2020; Sufyan et al. 2023). Previously, it was reported by Yin and Qiu (2019) that the pure line method has been used for wheat rust resistance, the backcross method and recurrent selection for rice blast resistance. To develop insect and pest resistance in sugarcane, insecticidal DNA sequences are integrated into sugarcane through genetic modifications. Some transgenic sugarcane that was engineered genetically for pest resistance (Table 3). The first phase focuses on creating and assessing modified sugarcane lines to resist diseases and insect pests. Genes that can stress or disease resistance are introduced in sugarcane from other organisms (Iqbal et al. 2021).
| Promoter | Gene | Transformation method | Target pest | References | |
|---|---|---|---|---|---|
| Maize Ubi-1 | Gna | Particle bombardment | Antitrogus consanguineous | Dinesh Babu et al. (2022) | |
| CaMV35S | cry1Ab | Electroporation | Diatraea saccharalis | Sanghera and Malhotra (2018) | |
| Ubi-1 | cry1Ab | Agrobacterium | Diatraea saccharalis | Babu et al. (2021) | |
| Maize Ubi-1 | Synthetic-cry1Ac | Particle bombardment | Proceras venosatus | Ashwin Narayan et al. (2020) | |
| Maize Ubi-1 | Soybean Kunitz trypsin inhibitor (skti) | Particle bombardment | Diatraea saccharalis | Iqbal et al. (2021) | |
| Maize PEPC | cry1Ab | Particle bombardment | Diatraea saccharalis | Ashwin Narayan et al. (2020) | |
| ST-LSI | cry2A | Particle bombardment | Chilo sacchariphagus, Scirpophaga nivella | Thuy et al. (2022) | |
| RUBISCO | CryIAb-CryIAc | Agrobacterium | Scripophaga excerptalis | Koerniati et al. (2020) | |
| CaMV 35S | cry1Aa3 | Agrobacterium | Chilo infuscatellus, Chilo sacchariphagus | Thuy et al. (2022) | |
| CaMV35S and FMV | cry1Ab and cry2Ab | Agrobacterium | Diatraea saccharalis | Talakayala et al. (2020) | |
| RSs-1 Maize Ubi-1 | Gna | Agrobacterium | Ceratovacuna lanigera | Zhao et al. (2022) | |
| Maize Ubi-1 | Snowdrop lectin | Paint-sprayer delivery | Eoreuma loftini, D. saccharalis | Budeguer et al. (2021) | |
| Ubi | cry1Ac | Particle bombardment | Diatraea saccharalis | Dessoky et al. (2021) |
Using GE, researchers can manipulate new disease resistance pathways in sugarcane. The enhancement of protection against fungal and viral infections in sugarcane can possibly be achieved by the inclusion of genes expressing antimicrobial peptides, pathogenesis-related (PR) proteins, or other defence-related molecules. This novel methodology expands the range of accessible resistance mechanisms, providing exciting possibilities for managing the ever-changing diseases and enhancing strategies for protecting crops (Parvaiz et al. 2022).
Sugarcane major diseases include red rot, wilt and smut caused by Colletotrichum falcatum, Fusarium sacchari and Sporisorium scitamineum fungus, respectively. Similarly, it is also affected by abiotic stresses like heavy metals, cold and heat stress. Recently innovated techniques like transgene-free genome editing have eradicated these diseases from crops like sugarcane (Surya Krishna et al. 2023b). Additionally, it is reported that sugarcane plants that overexpressed the AtBBX29 and H+-PPase (H+-pyro-phosphatase) gene in response to water stress showed higher rates of plant growth, photosynthesis as well as higher antioxidant and osmolyte levels (Raza et al. 2016; Mbambalala et al. 2021). According to Oz et al. (2021), the CRISPR-Cas system successfully acquired herbicide tolerance in sugarcane.
Likewise, another essential target for gene editing in sugarcane refers to the enhancement of resistance against viral infections, including sugarcane smut (caused by S. scitamineum), Sugar Cane Mosaic Virus (SCMV) and other comparable hazards. The sugarcane plants get infected with SCMV, resulting in the manifestation of mosaic symptoms on the leaves, hindered growth and reduced sugar content, eventually leading to an adverse effect on crop yield. By use of genome editing strategies such as gene knockout, gene insertion and RNA interference (RNAi), it is possible to modify particular genes (resistance genes, pathogenesis-related genes and RNAi-related genes) that are involved in the recognition and defensive responses of SCMV, consequently providing resistance. The implementation of genetic modification in sugarcane varieties to increase their resistance to SCMV enables farmers to reduce yield losses and protect their crops from this highly destructive viral pathogen (Chakraborty et al. 2022).
The use of genome editing provides a possible effective approach to enhancing the resistant capacity of sugarcane, a perennial plant that has significant economic value in terms of sugar and biofuel production. Phytoplasmas are a group of bacteria that are specific to the phloem and are transferred by insect vectors. These bacteria are responsible for producing diseases such as sugarcane white leaf (SCWL) and yellow leaf syndrome (SCYLS), which have a substantial negative impact on the productivity and quality of sugarcane (Rao et al. 2018). The process of modifying genes that provide resistance to phytoplasma diseases offers an opportunity to reduce the impact of these destructive diseases and ensure the long-term growth of sugarcane. These genes may encode receptors that recognise phytoplasma effectors or components of the plant defence system that are activated when the plant detects a pathogen. An example of a gene that has been found as susceptible to sugarcane is SUGARWIN1. This gene has been targeted for disruption using CRISPR/Cas9 technology, which aims to provide resistance to SCWL. The alteration of SUGARWIN1 in sugarcane plants resulted in a decrease in susceptibility to phytoplasma infection, exhibiting the capacity of gene editing to improve resistance against phytoplasma pathogens (Parvaiz et al. 2021).
In plant immunological signalling pathways, including those linked to salicylic acid or jasmonic acid-mediated defences, genes manipulation takes place that has the potential to enhance sugarcane’s capacity to initiate efficient defensive mechanisms against phytoplasma infection (Arora and Malik 2021). Manipulation of crucial genes within the salicylic acid pathway, such as NPR1 or EDS1 plays a crucial role in the enhancement of sugarcane’s systemic acquired resistance (SAR) to phytoplasma infections (Song et al. 2023). By selectively targeting genes associated with jasmonic acid signalling, such as COI1 or JAZ proteins, the enhancement of sugarcane’s inducible defences against phytoplasma infection might be achieved. The purpose of these specific modifications is to enhance the sugarcane’s immune system, enabling it to quickly and effectively combat phytoplasma invasion. This will result in a decrease in the severity of the disease and a reduction of yield losses (Thomas and Singh 2020).
Regulatory and ethical consideration
Globally, there are differences in the regulatory framework surrounding genome editing, with various countries adopting unique strategies. GE events without transgenes do not need regulatory approval in the United States. However, Brazilian regulations classify some varieties, such as Cana Flex I and II, as non-transgenic based on individual case studies. If a specific genome-edited product is transgene, it is advised in India to remove it from the biosafety evaluation. Transgenic breeding, which involves inserting foreign genes into plant genomes, became popular in the past century because of introducing genetic variations into crops (Visarada et al. 2009). Transgenic science progress has made it possible and easy to transfer genes from relatives of wild plants to crops by removing barriers to interspecies reproduction. This method increases crop tolerance to different stresses, and linkage drag problems are avoided. Transgenic lines are extensively used due to the success of transgenic breeding, mainly in developing insect resistance and herbicide tolerance (Anwar and Kim 2020).
GM crops were first brought to the market in 1996. In 2018, the cultivated area increased by 113 times and is now at peak level. In agriculture, pest- and insect-resistant Bt-cotton (Gossypium hirsutum modified with Bacillus thuringiensis) varieties have been adopted. GE has not only enhanced the yield of crops but also improved crops with a reduction in diseases like cancer, heart disease and obesity (Kumar et al. 2020). Every country has made unique regulatory approval processes for genetically modified organisms (GMOs) to investigate the risks to human safety and the environment before permitting the use and release of GMOs. According to the rules, exporting GM crops or seeds between different countries requires approval. Also, GM foods must be labelled in many countries before selling (Gabol et al. 2012). The area covered by genome-edited crops according to the nations is shown in (Fig. 4) (Gupta et al. 2021; Rozas et al. 2022). It is reported that about 95% of genome-edited crops are grown in these countries.
Using GE technology in plants has raised questions about possible environmental and human health effects, mainly in Asian countries where laws governing GMOs are still being developed. Similarly, these genetically engineered plant breeding laws are still not made in South Korea or India. Because of this, the regulatory frameworks in these countries cannot handle the problems that genome-edited plants cause (Yang and Zhou 2024). Additionally, in Pakistan, the use of GM crops is controversial. Only one GM crop is approved for cultivation, Bt-cotton, which is grown widely in the Punjab. Pakistan Atomic Energy Commission (PAEC) provided approximately 40,000 kg of insect resistance cotton seeds in 2005 (Riaz et al. 2018).
Applying CRISPR/Cas technology to genome editing in crops causes some ethical questions for agriculture and health. Some countries like Europe and the USA have restricted the use of germline genome editing on humans. Some countries prioritise protecting the public and label GM foods. Religious beliefs can also be a source of ethical restriction. Some support labelling and are against genome-edited crops. Genome-edited crops’ development and social acceptance depend heavily on moral issues, labelling and awareness (Munawar et al. 2024).
Future perspectives
The enormous application of GE technologies in agriculture has made it possible to modify crops to meet essential needs like functional genomics and disease resistance. Instead of their benefits, these methods have disadvantages such as interference with gene regulation, off-target editing and on-target effects. Particularly with the introduction of gene drives, engineered traits can have unexpected interactions and environmental hazards that could adversely affect the population. Because of these risks, government organisations should take precautions before approving and marketing genome-edited crops. The approval of crops and food derived from GE should be moving forward by assessments for food safety and environmental impact. A regulatory framework that can adapt to new developments is essential, especially in multiplex genome-edited crops and complex traits. It is suggested that a global regulatory framework should be established to address scientific and social concerns. Developers should openly and honestly inform the public about the benefits and drawbacks of GM crops. We need a global regulatory framework to harness the potential advantages of genome-edited crops for sustainable agriculture and food security.
Conclusion
Sugarcane is currently getting more attention for increasing its production due to its great importance as a table sugar and bioenergy resource. It is now difficult to meet the demands of this growing population using natural varieties as these varieties are more sensitive to climate change. Natural disasters have negatively affected these cultivars, resulting in decreased yields. Different techniques like gene editing are currently used to improve crop plants and increase their resistance to disease and stress. The rapid advancement of genome editing technologies has altered plant biology and opened previously unheard-of opportunities to improve crop traits important to global agriculture’s sustainability. Genome editing has provided different results, such as enhanced growth-related characteristics and increased resistance to diseases and pests. Genomics has also been utilised to enhance photosynthesis with the overexpression of D1 proteins. A lot of progress in sugarcane has been made by applying cutting-edge technologies like TALEN, ZFN and CRISPR/Cas9. These technologies have progressed and been used to improve crops like rice and tomato.
Data availability
The data that support this study will be shared upon reasonable request to the corresponding author.
Declaration of funding
Author Hesham Oraby acknowledges the Deputyship for Research and Innovation, Ministry of Education in Saudi Arabia for funding this work through the project number: IFP22UQU4350043DSR107.
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