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Wang, Y.;  Zafar, N.;  Ali, Q.;  Manghwar, H.;  Wang, G.;  Yu, L.;  Ding, X.;  Ding, F.;  Hong, N.;  Wang, G.; et al. CRISPR/Cas Technique for Disease Resistance. Encyclopedia. Available online: https://encyclopedia.pub/entry/38546 (accessed on 27 December 2024).
Wang Y,  Zafar N,  Ali Q,  Manghwar H,  Wang G,  Yu L, et al. CRISPR/Cas Technique for Disease Resistance. Encyclopedia. Available at: https://encyclopedia.pub/entry/38546. Accessed December 27, 2024.
Wang, Yaxin, Naeem Zafar, Qurban Ali, Hakim Manghwar, Guanying Wang, Lu Yu, Xiao Ding, Fang Ding, Ni Hong, Guoping Wang, et al. "CRISPR/Cas Technique for Disease Resistance" Encyclopedia, https://encyclopedia.pub/entry/38546 (accessed December 27, 2024).
Wang, Y.,  Zafar, N.,  Ali, Q.,  Manghwar, H.,  Wang, G.,  Yu, L.,  Ding, X.,  Ding, F.,  Hong, N.,  Wang, G., & Jin, S. (2022, December 12). CRISPR/Cas Technique for Disease Resistance. In Encyclopedia. https://encyclopedia.pub/entry/38546
Wang, Yaxin, et al. "CRISPR/Cas Technique for Disease Resistance." Encyclopedia. Web. 12 December, 2022.
CRISPR/Cas Technique for Disease Resistance
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This entry is adapted from the peer-reviewed paper 10.3390/cells11233928

Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) techniques were mostly used against viral infection and for fungal and bacterial disease resistance. The CRISPR/Cas system has been used to develop resistance to many pathogen species. 

CRISPR/Cas9 CRISPR/Cas12 CRISPR/Cas13 base editing

1. Introduction

Plants produce food, fuel, and feed, which are essential in daily human and animal life for nourishment and growth. In the process of plant growth, they will be affected by a variety of biological stresses (bacteria, viruses, fungi, and insects) and abiotic stresses [1][2][3][4][5]. Due to continuous global climate change and anthropogenic activity, the impact of abiotic stresses on crop growth and development is becoming more serious. Abiotic stresses, including drought, salinity, waterlogging, heat/cold, and heavy metals, significantly reduce agricultural production worldwide. Therefore, the ability to breed new species that are tolerant to various stresses in order to reduce yield loss will be a sustainable way to overcome these obstacles and meet the growing needs of human beings. Different types of biotic stresses involve a complex interplay among pathogens and host plants based on the susceptibility/resistance of crop plants to any disease. The latest advances in molecular tools have provided insights into a wide array of pathogen infection mechanisms and their interactions with specific crop plants. The insertions/deletions (Indels) mutations by artificial or natural phenomena might be involved in altering these interactions and hinder the pathways involved in the mode of infection [6][7].
Traditional crop breeding such as crossbreeding is an effective method that has been widely used to modify various plant species. Crop productivity and varieties can be increased effectively through crop breeding programs. In modern agriculture, the key methodologies used for breeding purposes are transgenic breeding, mutation-breeding, and GE-mediated breeding for crop improvement [8]. Cross-breeding and genetic recombination require years to introduce desirable alleles and increase variability [8]. Transgenic breeding is easy and well-known, improving crop traits by the exogenous transformation of genes into economically important elite varieties greatly shortens the breeding time. Still, this method inserts specific genes into the genome at random locations through plant transformation, which results in varieties containing foreign DNA. Compared to crossbreeding, mutation-breeding, and traditional transgenic breeding, GE-mediated crop breeding is fast, efficient, and accurate (Figure 1). Genome editing (GE) improves a targeted trait in a very fast and short time and exactly revising the target gene or regulatory sequence or changing the DNA and/or RNA bases in elite varieties. The current GE technique includes meganuclease (MegN), zinc-finger nucleases (ZFNs), transcription activator-like effector nucleases (TALENs), and clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) (CRISPR/Cas9) [7][9][10][11]. In 2013, genetic modifications through the CRISPR/Cas9 method were developed in plants and revolutionized the field by eliminating the barriers to targeted GE. The CRISPR system has been used in wheat, rice, tobacco, and Arabidopsis thaliana [12][13][14][15][16][17][18][19][20][21][22][23][24][25]. Till now, GE has been practiced in more than 50 plant species, and it will revolutionize plant breeding [26][27][28][29][30][31][32][33][34][35][36][37][38][39][40].
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Figure 1. Evolution of crop breeding techniques. Crossbreeding takes a great deal of time (8–10 years) to improve desirable characters/traits (in a particular species for disease tolerance or resistance) through crossing an elite variety line with a donor variety line and selecting the new outstanding offspring with desirable characters/traits. To introduce new progeny with desirable traits from the donor variety line to the elite variety line, the selected offspring must be backcrossed to the elite variety line for several years to remove undesirable related traits. In mutation breeding, mutations are used to improve traits in the time (6–7 years) of the genome through chemical treatment or physical irradiation to create novel genetic variations. Transgenic breeding is easy and well-known, improving crop traits within (4–6 years) by the exogenous transformation of genes into economically important elite varieties. Genome editing: improving a targeted trait in a very fast and short time (2–3 years) and exactly revising the target gene or regulatory sequence or changing the DNA and/or RNA bases in elite varieties.
Based on the composition of the CRISPR locus, this system has been divided into two classes: Class 1 requires multiple effector proteins with subtypes I, III, and IV, while class 2 requires only a single effector protein with subtypes II, V, and VI. The mode-of-action of GE by site-directed nucleases (SDNs) is that once present in a cell by insertion/expression and or transfection, the SDN is capable of cutting the genome at a targeted site. The cellular DNA-repair mechanisms fix the cut sites either by the non-homologous end joining (NHEJ) or by homology-directed repair (HDR). As NHEJ can be an error-prone process, indels can appear at the respective genomic site, leading to a loss-of-function edited gene sequence due to frameshift mutations. GE by using SDNs, can be categorized into three types: SDN-1 introduces small insertions or deletions which carry no additional or recombinant DNA. SDN-2 introduces short insertions or editing of a few base pairs by an external DNA-template sequence. The SDN-3, using a similar method to SDN-2, can be considered transgenic due to the insertion of large DNA pieces [41][42]. Since its introduction, in recent years, constant improvements have been made to make CRISPR systems easier and more suitable for different constraints, such as CRISPR/Cas9 [12][13][43][44], CRISPR/Cas12a [45][46][47][48][49], CRISPR/Cas12b [50], CRISPR/Cas13 [51][52], base editing tools [53][54][55][56][57][58][59], and CRISPR transcriptional activation (CRISPRa) [60][61][62][63][64] (Figure 2). A new form of GE technology, known as Prime Editing (PE) has recently been developed which is capable of achieving various forms of editing, for example, some base-to-base transfer, such as all transformations (C→T, G→A, A→G, and T→C) and transversion mutations (C→A, C→G, G→C, G→T, A→C, A→T, T→A, and T→G), as well as small indels without double-stranded breaks in the DNA. Since PE has enough versatility to accomplish specific forms of editing in the genome, it has great potential to grow superior crops for different purposes, including production, avoiding various biotic and abiotic stresses, and enhancing the quality of plant products [57][58][65][66][67][68][69][70][71][72][73].
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Figure 2. The methodology of major CRISPR/Cas systems. (A) CRISPR/Cas9 induces double-stranded breaks (DSBs) in DNA strands. (B) CRISPR/Cas12a cleaves the target DNA and introduces DSBs. (C) CRISPR/Cas methods can achieve different research goals: (a–c) are results of non-homologous end-joining NHEJ, and (d,e) are results of the homology-directed repair HDR repair pathways using a donor DNA template. (D–F) Base editing tools mainly include Cytidine Base Editor (CBE), Adenine Base Editor (ABE), and Prime Editor (PE). (D) CBE converts C-G base pairs to T-A base pairs at the target site. (E) ABE converts A-T base pairs to G-C base pairs at the target site. (F) PE is a new base editing system, which enables precise sequence substitution, insertion, and deletion. PE mainly consists of a Cas9 nickase (nCas9), an engineered reverse transcriptase (RT), and pegRNA. PegRNA includes PBS (Primer Binding Site) sequence and RT Template. (G) CRISPR/Cas13 consists of a Cas13, a crRNA, and a target RNA. Cas13:crRNA complexes bind target RNA and cleave the target RNA. (H) CRISPR transcriptional activation (CRISPRa) consists of a nuclease-deficient Cas9 (dCas9) and transcription activation domain (TAD). CRISPRa activates the transcription of single or multiple target genes.
CRISPR/Cas method has become the most popular among editing technologies and, thus far, has revealed the greatest potential to overcome the developing challenges (such as yield and biotic and abiotic stresses) of agriculture [9][74][75][76]. For example, mutations conferring resistance to various diseases in lettuce also exist [77]. Resistance against powdery mildew has been successfully acquired in barley by creating mutants at the mildew resistance locus o (MLO) [78]. The mutation at MLO is remarkable because it provides extraordinary, stable, and precise resistance for two decades against mildew without breakage of alleles; this long-lasting resistance is because of gene knockout [79][80].

2. CRISPR/Cas Technique for Disease Resistance

Biotic stresses, such as bacterial, viral, and fungal diseases, as well as herbivores, damage plant products every year, affecting 11% to 30% of worldwide agriculture production [81]. Plant defense against pathogens can reduce the effects of disease on plant growth and productivity, which is highly relevant to the lack of food availability in the world with the increasing population. Improvements in new methods or GE techniques have improved the new resistant crops, reducing yield losses due to plant defense. Until now, CRISPR/Cas techniques were mostly used against viral infection and for fungal and bacterial disease resistance (Figure 3). The CRISPR/Cas system has been used to develop resistance to many pathogen species [26][82].
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Figure 3. Future applications of CRISPR/Cas in plants against the biotic and abiotic stress. CRISPR/Cas represents the future of genome editing technology and the potential use of the CRISPR/Cas system in various disciplines under biotic and abiotic stresses of agriculture. With the maturity of genome editing (GE) technology and the development of new GE tools, the application of CRISPR/Cas is becoming more and more extensive. CRISPR/Cas can now achieve gene knockout, knock-in, and knock-up in plants, replacing a single base to cause amino acid changes, etc. Therefore, CRISPR/Cas can be used to modify key genes of biotic and abiotic stresses, improving crop growth and development and coping with various environmental stresses to create more germplasm resources that meet human needs.

2.1. CRISPR/Cas-Mediated Fungal Resistance in Plants

Many fungal pathogens cause lethal diseases in crop plants, such as rust, mildew, rot, and smut, which not only damage yield yearly in the biosphere but also damage the quality of the product. CRISPR/Cas has improved mycological resistance in various crop species based on the available information of the genomic mechanisms involved in crop-pathogen interactions. Defined candidate genes and gene products have provided the potential to increase plant defense against fungi [83][84]. In three crop varieties, RNA-guided Cas9 endonuclease was used to target MLO loci, such as tomato (Solanum lycopersicum), grapevine (Vitis vinifera), and wheat [85][86][87][88][89], and transgene-free plants have been generated [90]. An MLO encoded protein is localized in the cell membrane and contains seven transmembrane domains, which universally exist in all dicots and monocots [91]. Plants carrying loss-of-function alleles (mlo) of the MLO, such as A. thaliana, tomato, and barley, confer durable resistance against powdery mildew [92][93][94]. Using precision GE to target the MLO-B1 locus of the wheat genome to generate a 304K deletion Tamlo-R32 mutant maintains wheat growth and yield while providing robust powdery mildew resistance [79]. Out of three MLO home alleles, one (TaMLO-A1) has been mutated by CRISPR/Cas9 in triticum aestivum and displayed resilient resistance against Blumeria graminis f. sp. tritici infection [85]. The CRISPR/Cas-mediated transgene-free and self-pollinated tomato variety, which was developed by deleting the 48 bp fragment in the SlMlo1 gene (out of 16 important SlMlo genes), offers resistance against powdery mildew Oidium neolycopersici [87].
In grapevine, loss of VvMLO7 function by RNAi reduced sensitivity against powdery mildew Erysiphe necator [95]. In parallel, the knockout of VvMLO7 and VvMLO3 using CRISPR/Cas9 enhanced resistance to powdery mildew in grapevine [88][89]. In apple (Malus Domestica) protoplasts, RNP-based technology has been successfully used to edit three (DIPM-1, DIPM-2, and DIPM-4) genes to create resistance against fire blight Erwinia amylovora [88]. CRISPR/Cas9 scheme was used to target the VvWRKY52 transcription factor with four guide RNAs. The results showed 21% biallelic mutations in regenerated plants, and these plants confer resistance to the fungus Botrytis cinerea compared with monoallelic mutant plants [96]. To accelerate the GE application in woody plants, another approach based on transient leaf transformation together with disease assays was first demonstrated by researchers in Theobroma cacao [97]. Pathogenesis-Related 3 (NPR3) gene (the immune system suppressor) was targeted in cacao leaves, transiently by CRISPR/Cas9 system, so the leaves showed enhanced resistance against Phytophthora tropicalis. GE of a fungicide resistant gene PcMuORP1 by CRISPR/Cas9 elucidates a novel selection marker for Phytophthora (a genus of oomycetes) species [98]. In rice, CRISPR/Cas9-mediated disruption of OsSEC3A and OsERF922 genes confer resistance against rice blast disease [99][100]. In addition, the pi21 gene in rice also induced durable resistance to rice blast [101]. Furthermore, resistance to Magnaporthe oryzae disease in rice was enhanced by generating the OsSEC3A mutants and showed a pleiotropic type of phenotype with an increase in salicylic acid (SA) concentration, and several genes were induced related to SA- and pathogenesis related genes [99]. To conclude, all these successful fungal disease resistance results determined the advantage, efficacy, and potential of the CRISPR/Cas-based editing system to enhance resistance in crop plants.

2.2. CRISPR/Cas-Mediated Viral Resistance in Plants

Plant viruses are among the most common pathogens and cause hazardous diseases in a variety of economically important crops. There are five main groups based on viral genomes characters: sense-single-stranded-RNA (ssRNA+), antisense-single stranded-RNA (asRNA-), single-stranded-DNA (ssDNA), double-stranded-DNA (dsDNA), and double-stranded-RNA (dsRNA) viruses [102]. A rolling-circle amplification system is required to replicate the virus genome through recombination-mediated duplication or by a dsDNA replicative form [103]. Their genome holds a mutual fragment of 220 bp, which is prearranged in one (A, monopartite) or two (A and B, bipartite) constituents [104]. The Geminiviridae are a large family (over 360 species) of ssDNA plant viruses that cause significant losses to agriculturally and economically important crop plants worldwide [103], such as Malvaceae, Solanaceae, Fabaceae, Euphorbiaceae, and Cucurbitaceae [105]. The commercial term for a large genus of geminiviruses is Begomoviruses. Begomoviruses mostly produce diseases in dicotyledonous plants, for example, Nicotiana tabacum and sweet potato (Ipomoea batatas), and these viruses are mostly transmitted via the whitefly or leafhopper [106][107]. CRISPR/Cas9 system was used in Nicotiana benthamiana and A. thaliana to target two different geminiviruses: Bean yellow dwarf virus (BeYDV) and Beet severe curly top virus (BSCTV), respectively [108][109]. Recently, CRISPR/Cas9 techniques have also been applied to attain resistance against Begomoviruses [110]. In the (BSCTV) genome, 43 candidates were selected to target their coding and non-coding regions using CRISPR/Cas9 [109]. In inoculated leaves, virus accumulation was significantly reduced in all CRISPR/Cas9 constructs at variable levels. However, the highest resistance was observed in A. thaliana and N. tabacum to virus infection displaying the maximum expression level of sgRNAs and Cas9. Similar results have been detected by employing 11 sgRNAs in N. benthamiana, targeting the non-nucleotide sequence, Rep-binding sites, Rep motifs, and the hairpin of BeYDV [108], and decreased up to 87% load of the targeted viral. A tobacco rattle virus (TRV) vector was used to deliver the sgRNA molecules to the N. benthamiana, stably overexpressing the Cas9 endonuclease to target the Tomato yellow leaf curl virus (TYLCV) genome [110]. In that study, the CRISPR/Cas approach was effectively implemented to cleave and target the virus genome during duplication to confer resistance against TYLCV [86][110][111].
By using specific sgRNAs, several genome loci of TYLCV (non-coding and coding sequences) were targeted in their intergenic region (IR), the RCRII motif replication protein (Rep), and the viral capsid protein (CP). Targeting the IR stem-loop invariant structure showed the lowest viral accumulation and replication [110]. A similar CRISPR/Cas9 system was established to target the geminiviruses monopartite beet curly top virus (BCTV), and bipartite Merremia mosaic virus (MerMV), which possess a similar IR stem-loop sequence. CRISPR/Cas9 system-edited BCTV and MerMV viruses displayed tempered symptoms, indicating that combined resistance against various viral strains can be achieved by a single sgRNA specific for the conserved region of the pathogen.
The traditional SpCas9 system recognizes only dsDNA, so the defense against RNA-based viruses is difficult to attain. Nevertheless, the characterization and search for associated nucleases have steered to the discovery of LwaCas13a from (Leptotrichia wadei) and FnCas9 from (Francisella novicida), which have the ability to bind and cut the RNA [112]. FnCas9 was reported to demonstrate resistance against RNA viruses [113]. The sgRNAs designed to target the RNA of cucumber mosaic virus (CMV) and tobacco mosaic virus (TMV) in N. benthamiana and A. thaliana transgenic plants showed a significant reduction in TMV and CMV by 40–80% compared to wild-type (WT) plants [113]. It demonstrated that FnCas9-mediated application could be deliberated as a CRISPR interference (CRISPRi) apparatus, similar to the mitigation of gene expression by catalytically inactive proteins of SpCas9 [114]. A similar study was carried out with Cas13a for manipulating the RNA genome of turnip mosaic virus (TuMV) using RNA-guided ribonuclease [115]. The minimum spread and replication of TuMV was observed in tobacco leaves by using the most proficient virus interference, detected with CRISPR RNA excision of GFP2 and HC-Pro genes.
Furthermore, the pre-CRISPR RNA was processed by Cas13 (due to its innate ability) into functional CRISPR RNA to target many viral mRNAs simultaneously. This may provide an alternative system to improve its efficiency distinctly [115][116][117]. A second strategy is to achieve viral resistance by editing the specific plant genes that are responsible for virus resistance traits [118][119][120]. RNA viruses need plant host factors to preserve their normal life cycle, containing the eukaryotic translation initiation factors eIF4E, eIF4G, and eIF(iso)4E [121]. Host susceptibility gene eIF4E was targeted at two different sites to create resistance against plant potyviruses by CRISPR/Cas9 [118][122][123]. A similar approach in A. thaliana plants induced site-specific mutations at eIF(iso)4E locus and conferred complete resistance to single-stranded RNA potyvirus -TuMV by 1 bp deletions and 1 bp insertions without any off-target modification [119]. Recently, resistance to rice tungro spherical virus (RTSV) was developed by the mutagenesis in eIF4G alleles [120]. In addition, no negative effects on the growth of mutant plants were observed in studies by Macovei et al. and Pyott et al., although additional research should be conducted to verify and test the durability and efficacy of recessive resistance edited plants [119][120].

2.3. CRISPR/Cas-Mediated Bacterial Resistance in Plants

Many pathogenetic bacteria cause diseases in crops, and the crops show several types of symptoms [124]. Compared to fungal and viral resistance, few studies have been reported about the utilization of CRISPR/Cas against bacterial diseases in crop plant species. The Xanthomonas oryzae pv. Oryzae causes host gene expression to induce susceptibility by utilizing the type III transcription-activator-like effectors (TALEs) system. The X. oryzae pv. oryzae effector protein PthXo2 targets the host sucrose transporter gene OsSWEET13 and is recognized as a sensitive gene for pathogen progression. Disease susceptibility was conferred by transferring the indica rice IR24 OsSWEET13 allele to japonica rice Kitaake, while CRISPR/Cas9-mediated mutations in the allele offered resistance against bacterial blight [125]. Recently, a mutation in the promoter of three rice genes confers broad-spectrum resistance against bacterial blight in rice [126]. CRISPR/Cas9 was used to edit the promoter of the Xa13, a pluripotent gene for recessive resistance to bacterial blight in rice to obtain the highly resistant rice that does not affect agronomic traits [127]. Downy mildew resistance 6 (DMR6) is a well-known negative regulator of plant defense. In tomato, DMR6 ortholog SlDMR6-1 was reported to be up-expressed during Pseudomonas syringae pv. tomato pathogen progression and Phytophthora capsici infection [128]. By targeting the SlDMR6-1 (exon-3), the mutated plants conferred wide-spectrum resistance against P. capsici, Xanthomonas gardneri, P. syringae, and X. perforans [128][129][130]. The tomato bacterial speck disease (causal agent Pseudomonas syringae) causes stomatal opening using coronatine (COR) to facilitate bacterial progression. This stomatal response in A. thaliana relies on AtJAZ2 (Jasmonate ZIM-domain-2), a COR co-receptor. The JAZ2 does not have the C-terminal Jas domain (JAZ2Δjas) that avoids stomatal opening using COR [131]. The homologous gene of AtJAZ2 in tomato is SlJAZ2 [132]. Resistance against the model pathogen Pseudomonas syringae pv. tomato DC3000 (Pto) DC3000 was developed by targeting the dominant JAZ2 repressor- SlJAZ2Δjas by using CRISPR/Cas9 technology that prohibited stomatal opening. Improving and refining the CRISPR/Cas9 and CRISPR/Cas12a systems provide a new opportunity to edit perennial crops species such as citrus to introduce resistance against citrus greening disease [133].
After producing successful bacterial disease-resistant tomato and A. thaliana, the CRISPR/Cas9 system recently effectively produced citrus bacterial canker (CBC) (causal agent Xanthomonas citri subsp. citri (X. citri) resistant citrus plants. The X. citri is the most widespread disease in commercially cultivated citrus [134]. CBC resistance was firstly reported in Duncan grapefruit by altering the PthA4 effector binding elements in the promoter of the Lateral Organ Boundaries 1 (CsLOB1) gene [135]. A significant decline in Xcc symptoms was detected in the mutated lines with no additional phenotypic alterations confirming the link between CBC disease susceptibility and CsLOB1 promoter activity Citrus (Citrus sinensis) (Osbeck) Wanjincheng orange [136]. In Wanjincheng orange, editing of CsWRKY22 by CRISPR/Cas9 reduces susceptibility to X. citri [137]. CBC disease resistance was enhanced by deleting the EBEPthA4 sequence completely from both CsLOB1 alleles, and no additional changes were observed in plants with altered CsLOB1 promoter. Recently, the CRISPR/Cas9-FLP/FRT system has been successfully induced in apple cultivars to reduce fire blight susceptibility [138]. In conclusion, these fruitful results demonstrate that CRISPR/Cas has the potential to not only create bacterial resistance in annual and biennial crop species but also confer durable bacterial disease resistance in perennial crop plants.

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Subjects: Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Yaxin Wang
,
Naeem Zafar
,
Qurban Ali
,
Hakim Manghwar
,
Guanying Wang
,
Lu Yu
,
Xiao Ding
,
Fang Ding
,
Ni Hong
,
Guoping Wang
,
Shuangxia Jin
View Times: 597
Revisions: 2 times (View History)
Update Date: 12 Dec 2022
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