Genome Editing for Sustainable Crop Improvement

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This entry is adapted from the peer-reviewed paper 10.3390/plants11192625

Climate change poses a serious threat to global agricultural activity and food production. Plant genome editing technologies have been widely used to develop crop varieties with superior qualities or can tolerate adverse environmental conditions. Unlike conventional breeding techniques (e.g., selective breeding and mutation breeding), modern genome editing tools offer more targeted and specific alterations of the plant genome and could significantly speed up the progress of developing crops with desired traits, such as higher yield and/or stronger resilience to the changing environment.

biotechnology climate change CRISPR crop improvement genome editing

1. Introduction

Climate change, such as extreme weather or temperature, drought, increasing soil salinity, and flooding, significantly affects the food production system, posing serious threats to food security. The adverse effects of climate change on agricultural productivity have been reported in several regions, including Asia ^[1], sub-Saharan Africa ^[2], and the European Union (EU) ^[3]. For example, the heatwave and drought in the EU in 2018 have reduced cereal production by 8% compared to the previous five-year average ^[4], causing fodder shortages for livestock and increasing commodity prices. The impacts of climate change on agriculture in developing countries are more significant than in developed countries, mainly as these countries are located in tropical latitudes, which are more sensitive to climate change ^[5]. In addition, differences in vulnerability between these regions might be due to differences in endowments of human skills, physical infrastructure, and rapid demography growth, causing developing countries to have lower levels of resilience ^[6]^[7]^[8]. Ensuring sustainable crop production and food security has become challenging not only due to the growing environmental pressures but also the ever-increasing human population. Around 720 to 811 million people, about a tenth of the global population, still suffer from hunger. Meanwhile, more than 2 billion people are in the ‘food insecure’ category ^[9]. Another 130 million people may be added to the latter category due to the recent COVID-19 pandemic ^[10]. These problems will continue to worsen with the projected global population growth since the yield of grain crops, such as rice, wheat, and maize, has already reached a plateau ^[11]. With an estimated world population of 9.7 billion by 2050, crop productivity will need to increase by another ~70% while simultaneously reducing the environmental impacts ^[12]. Moreover, climate change increases the severity of biotic and biotic stresses on crops. Biotic stresses, such as pathogens, insect pests, and weeds, cause average output losses ranging from 17.2% in potatoes to 30.0% in rice ^[13]. Likewise, abiotic stresses, such as temperature extremes, drought, and lack of nutrient deficiency, caused the loss of 51–82% of the global crop output annually ^[14]. As the intensity of biotic and abiotic stresses on crops increases because of climate change, novel approaches are required to enhance plant tolerance. Given that conventional agricultural practices are inadequate to meet current and future food demands and deal with the aggravated impacts of biotic and abiotic stresses due to climate change, developing practical and effective adaptation strategies is indispensable to enhance crop productivity and ensure food security. Ideally, the strategies driving this effort should be sustainable and environmentally friendly while minimizing adverse environmental impacts.

Crop breeding, including cross-breeding and mutation breeding, has been used to enhance crop performance under climate change scenarios. However, breeding programs can be laborious and time-consuming, even aided by marker-assisted selection. It can take 8 to 10 years ^[15] or 6 to 15 years ^[16] to produce a genetically superior cultivar for agricultural production. Plant breeders have used cross-breeding based on naturally occurring mutations ^[15] or mutation breeding techniques based on ionizing radiation and chemical mutagens to generate new varieties with desired agronomic traits, including improved stress-tolerance potential and biofortification ^[17]. Nevertheless, since cross-breeding is limited to traits present in the parental genomes, low variability in elite germplasms restrains the use of this technique. The outcomes of the mutation breeding technique are unpredictable even though lower mutation rates have been reported in essential genes compared to non-essential genes ^[18]. In addition, complex and tedious screening and selection procedures are required to identify the desired trait from a large population of mutagenized plants ^[19]. Transgenic technologies that involve transferring desired trait-coding genes into the elite cultivars are undoubtedly an alternative to counter losses in crop yield ^[20]. However, the time and expenses of developing a genetically modified (GM) crop with desirable traits are enormous. The major limitation of this method is the low public acceptance of GM crops and, related to this, the complex and strict safety regulatory procedures ^[21]. In addition, different countries have adopted different regulatory procedures. However, to date, only a few countries, such as Switzerland, strictly restricted or legally prohibited the cultivation of GMOs ^[22].

2. CRISPR/Cas9 for Genome Editing in Crops

The CRISPR/Cas9 system has been used in various crops to develop desirable and heritable traits, such as yield improvement and biotic and abiotic stress management. Table 1 summarizes the applications of CRISPR/Cas9 for crop improvement.

Table 1. Examples of CRISPR/Cas9 applications for crop improvement.

Improvement	Trait	Crop	sgRNA Target Area	Type of Editing	Target Area	Result	References
Abiotic stress resistance	Drought	Chickpea	cDNA	Frameshift deletion	Coumarate ligase (4CL) and Reveille 7 (RVE7)	Enhanced tolerance	^[23]
	Cold	Rice	cDNA	InDel mutation	OsMYB30	Improved tolerance	^[24]
	Herbicide	Maize	cDNA	Base editing	ZmALS1, ZmALS2	Plants with Sulfonylurea herbicide-resistant	^[25]
	Salinity	Tomato	DBD domain of cDNA	49-bp deletion	SlARF4	Enhanced salinity tolerance	^[26]
	Heavy metals	Rice	cDNA	Downregulation	OsNramp5	Decreased cadmium accumulation	^[27]
	Heat	Tomato	cDNA	1-bp insertion 4-bp deletion	SlMAPK3	Enhanced heat tolerance	^[28]
Biotic stress resistance	Viral disease	Barley	Coding sequence	Base editing	MP, CP, Rep/Rep, IR/Virus genome	Resistant plants	^[29]
	Fungal disease	Rice	Genome	80-bp insert	ALB1, RSY1/ Fungal gene	Improved resistance to rice blast	^[30]
	Bacterial disease	Tomato	JAS domain C-terminal	Deletion	SIDMR6-1/Host S-gene	Resistant plants	^[31]
	Insect pest	Soybean	Coding region	1-bp and 33-bp deletion	GmUGT	Enhanced resistance to Helicoverpa armigera and Spodoptera litura	^[32]
Plant/crop quality	Crop growth	Rice	cDNA	Frameshift	PYL1–PYL6 and PYL12(gp-1), PYL7–PYL11 and PYL13(gp-2)	Improved plant growth and grain productivity	^[33]
	Crop yield	Wheat	cDNA	10-bp deletion	TaCKX2-1, TaGLW7, TaGW2, and TaGW8	Improved grain yield	^[34]
	Crop nutrition	Rice	Genomic Safe Harbor	5.2kb insertion	5.2 kb carotenoid cassette insertion	Increased β-carotene content	^[35]
	Grain size	Rice	cDNA	InDel mutation	OsGS3	Increased grain size	^[36]
	Grain number	Rice	cDNA	InDel mutation	OsGn1a	Increased grain number	^[36]^[37]
	Fruit size	Tomato	Promoter	85-bp deletion	SlENO	Enhanced fruit size	^[38]

2.1. Abiotic Stress

Climate change leads to various abiotic stresses, threatening agricultural food production worldwide ^[39]. About 90% of all arable lands are prone to single or multiple abiotic stresses, such as water stress, extreme temperature, and salinity ^[40]. To survive, plants have evolved various mechanisms to respond to and cope with these stresses ^[41]. However, the plant stress-responsive and adaptation mechanisms are complex and governed by various genes, posing challenges to developing novel cultivars using conventional methods ^[42]. As such, targeted genome editing on single or multiple target sites through the CRISPR/Cas9 system could be a promising approach to developing abiotic stress-resilient crop varieties ^[43].

The CRISPR/Cas9 approach has been exploited to improve crop survival under adverse environmental stresses. For example, Zhang et al. ^[44] developed salinity-resistant rice through the CRISPR/Cas9 approach. By knocking out the OsRR22 gene, the authors found that the generated rice showed better plant growth than wild-type under salinity conditions ^[44]. A recent study indicated that OsNAC041 is a critical transcription factor involved in the salt stress response in rice. A targeted osnac041 mutant obtained using the CRISPR/Cas9 method showed a higher plant height than the wild-type ^[45]. Other studies demonstrated that members of the AP2/ERF domain containing the RAV (related to ABI3/VP1) transcription factor family are involved in salinity stress adaption ^[46]^[47]. For instance, when the rice was exposed to salt stress, the OsRAV2 gene was activated. To determine the role of the GT-1 element in the OsRAV2 gene, Duan et al. ^[48] designed a sgRNA targeting the GT-1 region of the promoter. They found that the mutant lines could not express the OsRAV2 gene under salinity conditions, confirming the importance of this gene in response to salinity stress. A similar finding has been reported by Liu et al. ^[49], where the CRISPR/Cas9-mediated OsGTγ-2 knockout lines showed salt-hypersensitive phenotypes. Besides rice, the CRISPR/Cas9 genome editing technology has also been applied to other crops, such as wheat ^[50], soybean ^[51], maize ^[52], and tomato ^[53].

Drought stress disturbs physiological and biochemical processes in plants, limiting plant growth and yield ^[54]. Several genes and phytohormone signaling pathways have been shown to play critical roles in drought stress responses. Of these, abscisic acid (ABA) is a central regulator of water use and coordinates the plant’s responses to drought stress. Hence, several studies have been conducted to improve drought tolerance in crops by targeting the genes involved in ABA signaling. For example, Zhang et al. ^[55] determined the role of OsABA8ox2, which encodes ABA 8′-hydroxylase, in rice drought tolerance. The authors found that the CRISPR/Cas9-mediated OsABA8ox2 knockout lines showed increased drought-induced ABA in roots and induced root formation beneficial to drought tolerance. In contrast, overexpressing OsABA8ox2 in rice suppressed root elongation and exhibited hypersensitivity to drought stress ^[55]. The ENHANCED RESPONSE TO ABA1 (ERA1), which encodes the β-subunit of the protein farnesyltransferase, was mutated in Japonica rice cv. Nipponbare using the CRISPR/Cas9 system ^[56]. The rice osera1 mutant lines showed increased sensitivity to ABA and drought tolerance through stomatal regulation, suggesting that ERA1 could be a potential candidate gene for enhancing drought tolerance in crops. Another study by Yin et al. ^[57] showed that the OsEPFL9 (Epidermal Patterning Factor like-9) mutants had more than an eight-fold reduction in stomatal density (SD) in the CRISPR/Cas9-edited rice plants. The reduced SD allows the edited rice lines to resist drought stress. Under optimal conditions, a significant reduction in carbon assimilation and conductance and enhanced water use efficiency (WUE) was observed when SD was reduced by 50% in barley and wheat ^[58]^[59]. Likewise, in well-watered conditions, a CRISPR-based knockout of grapevine VvEPFL9-1 reduced SD by 60% and caused reduced carbon assimilation as compared to WT ^[60]. In tomatoes, slmapk3 mutants generated through CRISPR/Cas9 showed that SlMAPK3 is involved in drought response, and the slmapk3 mutants showed more severe wilting symptoms and suffered cell membrane damage under drought stress ^[61].

Some studies used the CRISPR/Cas9 technology to reduce mineral toxicity. For example, Nieves-Cordones et al. ^[62] developed low cesium-containing rice plants by inactivating the K+ transporter OsHAK1 using the CRISPR/Cas9 system. In rice, knocking out OsARM1 and OsNramp5 showed improved arsenic tolerance ^[63] and low cadmium accumulation ^[64]. Another example of increasing plant stress resistance was shown by Shao et al. ^[65], where the authors developed a semi-dwarf variety of bananas using the CRISPR/Cas9 system to disrupt the genes responsible for the gibberellin biosynthesis. As a result, the developed bananas are more resistant to storms and heavy wind. Besides generating knockouts on the susceptible genes, genome-editing tools can also be used for knock-ins of a desirable gene. For instance, Shimatani et al. ^[66] used CRISPR/Cas9 to insert a maize promoter before the drought tolerance gene, ARGOS8. Consequently, the edited maize crops showed a greater grain yield during water stress.

These studies demonstrated that the CRISPR/Cas system could edit the plant genome, allowing the researchers to investigate the role of genes involved in response to abiotic stresses. However, reports on targeting abiotic stress tolerance genes are scarce, primarily due to the complexity associated with abiotic stress tolerance, often involving the modulation of several genes to alter the trait of interest.

2.2. Biotic Stress

Plants are constantly plagued by pathogens, such as viruses, bacteria, and fungi, which can significantly reduce crop quality and yield ^[67]. The majority of disease-resistant crops against non-viral diseases are produced through genome editing and targeted mutagenesis of genes that negatively influence defense ^[68]. While few such genes are available for increasing disease resistance, many of these loci have already been successfully exploited for increased resistance.

In rice, genome editing has shown a remarkable result in combating diseases using CRISPR/Cas9. Most pathogens use the sucrose transporters that are encoded by the SWEET gene family in many plants ^[69]. In two experiments, CRISPR/Cas9 was utilized to target the promoter region of a few OsSWEET genes to develop resistance against bacterial leaf blight ^[70]^[71]. Knockout of the OsERF922 gene that expresses ethylene response in the plant using CRISPR/Cas9 reduced the effect of leaf blast disease, thereby enhancing its tolerance toward it ^[72]. Additionally, CRISPR/Cas9 editing of the eukaryotic elongation factor, eIF4G, in rice resulted in plants that were immune to the rice tungro virus ^[73]. The infected CRISPR-edited plants contained no detectable viral proteins and produced better yields than wild-type plants.

The advancement of the CRISPR/Cas9 system has furthered the development of resistance to multiple diseases at the same time. Engineering the broad spectrum of disease resistance in staple crops on a large scale could provide a single solution to several diseases that are affecting crop production ^[70]. The editing of bsr-k1, a rice gene that binds to and increases the turnover of defense-related genes ^[74], is an example of this strategy. By “turning off” these critical defense genes, edited rice plants were resistant to both leaf blast and bacterial leaf blight. When challenged with rice leaf blast in the field, the transgenic lines show a greater yield of 50% more without affecting other agronomic features ^[74]. Likewise, the same strategy has also been applied to other crops for disease resistance. For example, broad-spectrum resistance was obtained by altering a single locus in tomatoes ^[75]. The SlDMR6-1 mutations by CRISPR/Cas9 in the edited lines maintain an increased salicylic acid level in the plant with a significant reduction of disease symptoms and pathogen abundance, gaining resistance to Pseudomonas syringae, Phytophthora capsici, and Xanthomonas spp. ^[75]. In barley, CRISPR/Cas9-mediated editing of MORC1, a defense-related gene, increased resistance to barley powdery mildew and Fusarium graminearum ^[76]. In addition, the authors showed that the edited barley plants had lower levels of fungal DNA and fewer lesions.

In some species, targeting homologs of Mildew-resistance Locus (MLO) and other loci enhanced the resistance to these fungal infections. By concurrently targeting the three homologs of the MLO, TaMLO-A, TaMLO-B, and TaMLO-D, CRISPR/Cas9 can increase the resistance of wheat to powdery mildew ^[77]. Another example is the Tomelo transgene-free tomato, which is resistant to powdery mildew disease and was produced by targeting SlMlo1 gene using CRISPR/Cas9 ^[78]. Zhang et al. ^[79] changed the three homologs of the wheat TaEDR1 gene simultaneously using CRISPR/Cas9 to improve resistance to powdery mildew disease. In grapevine, targeting the MLO homologs boosted the resistance to powdery mildew, whereas the edited line of grapevine had a two-fold reduction in powdery mildew sporulation ^[80]. In other efforts, knockout of the 14-3-3 c and 14-3-3 d protein simultaneously, a negative regulator of disease response, in cotton enhanced resistance to Verticillium dahliae ^[81]. The edited cotton showed fewer disease symptoms and lowered pathogen presence compared to the control ^[81].

2.3. Yield

One of the essential keys to sustaining food production is crop yield. It is the most direct means to address the ever-rising food demand from a growing population. However, crop yield is a complex trait regulated by many factors. Therefore, much research has been done to identify the quantitative trait loci (QTLs) associated with morpho-agronomic and yield-related traits in various crop plants ^[82].

One way genome editing can increase crop yield is to eliminate genes that have a detrimental impact on yields, such as genes limiting grain size and weight ^[83]^[84]. In one recent example, CRISPR/Cas9 was used to individually knock out the genes of four negative yield regulators (Gn1a, DEP1, GS3, and IPA1) in the rice cultivar Zhonghua 11. Each of the individual knockout mutants, Gn1a, DEP1, and GS3, showed increased yield characteristics in the T₂ generation ^[85]. Similarly, Xu et al. ^[86] used a CRISPR/Cas9-mediated multiplex genome-editing technology to knock out three main rice negative regulators of grain weight (GW2, GW5, and TGW6) simultaneously, and the resulting mutants had a considerable increase in thousands of grain weights. In another study on wheat, CRISPR/Cas was used to knock out the three homoeoalleles of GASR7, and the mutant plant produced a much heavier kernel weight when compared to wild-type wheat plants ^[87]. Besides grain, targeting a tomato cis-regulatory region in the CLAVATA-WUSCHEL stem cell circuit (CLV-WUS) using CRISPR/Cas9 resulted in an edited tomato with an increased number of locules (seed compartments) and bigger fruit size ^[88].

Alternatively, genome editing can also influence crop yield through other strategies. CRISPR/Cas9 technology was employed in maize to create high amylopectin variants from superior cultivars by knocking out the waxy gene ^[89]. The edited maize cultivars yielded 5.5 bushels per acre more than conventionally bred high amylopectin varieties. Furthermore, they could be developed in a shorter time, demonstrating the feasibility of genome editing in particular specialized applications ^[89]. Furthermore, reducing the ABA response of rice plants can also enhance the yield. Rice plants with simultaneous mutations of class I PYL genes (encoding receptors for ABA) using CRISPR/Cas9 had better yields than the control ^[33]. Under well-watered conditions, triple knockout of PYLs 1,4,6 resulted in a 30% increase in yield ^[33]. It is interesting to see how these ABA-encoding PYL genes affect yield under less-optimal conditions. A recent study shows that under drought conditions, the wheat PYL1-1B (TaPYL1-1B) is responsible for increased yield and drought resistance, where it exhibited higher ABA sensitivity, photosynthetic capacity and WUE ^[90].

A higher yield of tomatoes can also be achieved by modifying the flower repressor gene using CRISPR/Cas9. Knockout of the flowering repressor SELF-PRUNING 5G (SP5G) gene produced tomato plants that have rapid flowering, which in turn yield earlier with compact determined growth ^[91]. In contrast, mutations in the SELF PRUNING (SP) gene changed the plant architecture to a bushier state with more branches ^[92]. The resultant mutants with two modifications had faster flowering time and earlier fruit ripening than the control lines. In another study, CRISPR-based knockout of tomato SlAGL6 enhanced yield under heat stress. The tomato agl6 mutants displayed facultative parthenocarpy without any pleiotropic effect and produced seedless fruits of equal weight and shape to WT ^[93]. Under salinity stress, the CRISPR-edited soybean gmaitr mutants yield was much less affected than the WT in plant height, number of pods per plant, and seed weight ^[51]. The number of studies on plant yield and resilience improvement is expected to grow, in line with the rapid advancement of genome editing tools.

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