Genome Editing for Sustainable Crop Improvement

Version	Summary	Created by	Modification	Content Size	Created at	Operation
1		Boon Chin Tan	--	3020	2022-10-23 16:28:11	\|
2	format corrected.	Beatrix Zheng	+ 1 word(s)	3021	2022-10-24 05:42:54	\|

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.

References

Ozdemir, D. The impact of climate change on agricultural productivity in Asian countries: A heterogeneous panel data approach. Environ. Sci. Pollut. Res. 2022, 29, 8205–8217.
Kuyah, S.; Sileshi, G.; Libère, N.; Chirinda, N.; Ndayisaba, P.; Dimobe, K.; Oborn, I. Innovative agronomic practices for sustainable intensification in sub-Saharan Africa. A review. Agron. Sustain. Dev. 2021, 41, 16.
Brás, T.; Seixas, J.; Carvalhais, N.; Jägermeyr, J. Severity of drought and heatwave crop losses tripled over the last five decades in Europe. Environ. Res. Lett. 2021, 16, 065012.
EC. Short-Term Outlook for EU Agricultural Markets in 2018 and 2019. Available online: https://agriculture.ec.europa.eu/data-and-analysis/markets/outlook/short-term_en (accessed on 1 May 2022).
Yim, H. Incorporating climate change adaptation into sustainable development. J. Int. Dev. Coop. 2017, 2017, 139–171.
Galluzzi, G.; Seyoum, A.; Halewood, M.; Lopez Noriega, I.; Welch, E.W. The role of genetic resources in breeding for climate change: The case of public breeding programmes in eighteen developing countries. Plants 2020, 9, 1129.
Bandt, O.d.; Jacolin, L.; Lemaire, T. Climate Change in Developing Countries: Global Warming Effects, Transmission Channels and Adaptation Policies; Banque de France: Paris, France, 2021; pp. 1–65.
Ludwig, F.; Terwisscha van Scheltinga, C.; Verhagen, J.; Kruijt, B.; van Ierland, E.; Dellink, R.; de Bruin, H.; Kabat, P. Climate Change Impacts on Developing Countries—EU Accountability; Think Tank Publications: Bulgaria, The Netherlands; pp. 1–45.
FAO; IFAD; UNICEF; WFP; WHO. The State of Food Security and Nutrition in the World 2021: Transforming Food Systems for Food Security, Improved Nutrition and Affordable Healthy Diets for All; World Health Organization: Rome, Italy, 2021; pp. 1–240.
UN. Policy Brief: The Impact of COVID-19 on Food Security and Nutrition; United Nations: Rome, Italy, 2020; pp. 1–22.
Grassini, P.; Eskridge, K.M.; Cassman, K.G. Distinguishing between yield advances and yield plateaus in historical crop production trends. Nat. Commun. 2013, 4, 2918.
Lau, S.-E.; Teo, W.F.A.; Teoh, E.Y.; Tan, B.C. Microbiome engineering and plant biostimulants for sustainable crop improvement and mitigation of biotic and abiotic stresses. Discov. Food 2022, 2, 9.
Savary, S.; Willocquet, L.; Pethybridge, S.J.; Esker, P.; McRoberts, N.; Nelson, A. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 2019, 3, 430–439.
Oshunsanya, S.O.; Nwosu, N.J.; Li, Y. Abiotic stress in agricultural crops under climatic conditions. In Sustainable Agriculture, Forest and Environmental Management; Jhariya, M.K., Banerjee, A., Meena, R.S., Yadav, D.K., Eds.; Springer Singapore: Singapore, 2019; pp. 71–100.
Gao, C. Genome engineering for crop improvement and future agriculture. Cell 2021, 184, 1621–1635.
Lyzenga, W.J.; Pozniak, C.J.; Kagale, S. Advanced domestication: Harnessing the precision of gene editing in crop breeding. Plant Biotech. J. 2021, 19, 660–670.
Chaudhary, J.; Deshmukh, R.; Sonah, H. Mutagenesis approaches and their role in crop improvement. Plants 2019, 8, 467.
Zhang, J. Important genomic regions mutate less often than do other regions. Nature 2022, 602, 38–39.
Ma, L.; Kong, F.; Sun, K.; Wang, T.; Guo, T. From classical radiation to modern radiation: Past, present, and future of radiation mutation breeding. Front. Public Health 2021, 9, 11.
Sedeek, K.E.M.; Mahas, A.; Mahfouz, M. Plant genome engineering for targeted improvement of crop traits. Front. Plant Sci. 2019, 10, 16.
Herman, R.A.; Fedorova, M.; Storer, N.P. Will following the regulatory script for GMOs promote public acceptance of gene-edited crops? Trends Biotechnol. 2019, 37, 1272–1273.
Turnbull, C.; Lillemo, M.; Hvoslef-Eide, T.A.K. Global regulation of genetically modified crops amid the gene edited crop boom—A review. Front. Plant Sci. 2021, 12, 19.
Badhan, S.; Ball, A.S.; Mantri, N. First report of CRISPR/Cas9 mediated DNA-free editing of 4CL and RVE7 genes in chickpea protoplasts. Int. J. Mol. Sci. 2021, 22, 396.
Zeng, Y.; Wen, J.; Zhao, W.; Wang, Q.; Huang, W. Rational improvement of rice yield and cold tolerance by editing the three genes OsPIN5b, GS3, and OsMYB30 with the CRISPR-Cas9 system. Front. Plant Sci. 2019, 10, 1663.
Li, Y.; Zhu, J.; Wu, H.; Liu, C.; Huang, C.; Lan, J.; Zhao, Y.; Xie, C. Precise base editing of non-allelic acetolactate synthase genes confers sulfonylurea herbicide resistance in maize. Crop J. 2020, 8, 449–456.
Bouzroud, S.; Gasparini, K.; Hu, G.; Antonia, M.; Barbosa, M.; Luan Rosa, B.; Fahr, M.; Bendaou, N.; Bouzayen, M.; Zsögön, A.; et al. Down regulation and loss of auxin response factor 4 function using CRISPR/Cas9 alters plant growth, stomatal function and improves tomato tolerance to salinity and osmotic stress. Genes 2020, 11, 272.
Chen, Q.; Tang, W.; Zeng, G.; Sheng, H.; Shi, W.; Xiao, Y. Reduction of cadmium accumulation in the grains of male sterile rice Chuang-5S carrying Pi48 or Pi49 through marker-assisted selection. 3 Biotech 2020, 10, 539.
Yu, W.; Wang, L.; Zhao, R.; Sheng, J.; Zhang, S.; Li, R.; Shen, L. Knockout of SlMAPK3 enhances tolerance to heat stress involving ROS homeostasis in tomato plants. BMC Plant Biol. 2019, 19, 354.
Kis, A.; Hamar, E.; Tholt, G.; Ban, R.; Havelda, Z. Creating highly efficient resistance against wheat dwarf virus in barley by employing CRISPR/Cas9 system. Plant Biotechnol. J. 2019, 17, 1004–1006.
Foster, A.J.; Martin-Urdiroz, M.; Yan, X.; Wright, H.S.; Soanes, D.M.; Talbot, N.J. CRISPR-Cas9 ribonucleoprotein-mediated co-editing and counterselection in the rice blast fungus. Sci. Rep. 2018, 8, 14355.
Ortigosa, A.; Gimenez-Ibanez, S.; Leonhardt, N.; Solano, R. Design of a bacterial speck resistant tomato by CRISPR/Cas9-mediated editing of SlJAZ2. Plant Biotechnol. J. 2019, 17, 665–673.
Zhang, Y.; Guo, W.; Chen, L.; Shen, X.; Yang, H.; Fang, Y.; Ouyang, W.; Mai, S.; Chen, H.; Chen, S.; et al. CRISPR/Cas9-mediated targeted mutagenesis of GmUGT enhanced soybean resistance against leaf-chewing insects through flavonoids biosynthesis. Front. Plant Sci. 2022, 13, 802716.
Miao, C.; Xiao, L.; Hua, K.; Zou, C.; Zhao, Y.; Bressan, R.A.; Zhu, J.-K. Mutations in a subfamily of abscisic acid receptor genes promote rice growth and productivity. Proc. Natl. Acad. Sci. USA 2018, 115, 6058–6063.
Zhang, Z.; Hua, L.; Gupta, A.; Tricoli, D.; Edwards, K.J.; Yang, B.; Li, W. Development of an Agrobacterium-delivered CRISPR/Cas9 system for wheat genome editing. Plant Biotechnol. J. 2019, 17, 1623–1635.
Dong, O.X.; Yu, S.; Jain, R.; Zhang, N.; Duong, P.Q.; Butler, C.; Li, Y.; Lipzen, A.; Martin, J.A.; Barry, K.W.; et al. Marker-free carotenoid-enriched rice generated through targeted gene insertion using CRISPR-Cas9. Nat. Commun. 2020, 11, 1178.
Zhou, J.; Xin, X.; He, Y.; Chen, H.; Li, Q.; Tang, X.; Zhong, Z.; Deng, K.; Zheng, X.; Akher, S.A.; et al. Multiplex QTL editing of grain-related genes improves yield in elite rice varieties. Plant Cell Rep. 2019, 38, 475–485.
Yuyu, C.; Aike, Z.; Pao, X.; Xiaoxia, W.; Yongrun, C.; Beifang, W.; Yue, Z.; Liaqat, S.; Shihua, C.; Liyong, C.; et al. Effects of GS3 and GL3.1 for grain size editing by CRISPR/Cas9 in rice. Rice Sci. 2020, 27, 405–413.
Yuste-Lisbona, F.J.; Fernandez-Lozano, A.; Pineda, B.; Bretones, S.; Ortiz-Atienza, A.; Garcia-Sogo, B.; Muller, N.A.; Angosto, T.; Capel, J.; Moreno, V.; et al. ENO regulates tomato fruit size through the floral meristem development network. Proc. Natl. Acad. Sci. USA 2020, 117, 8187–8195.
Neupane, D.; Adhikari, P.; Bhattarai, D.; Rana, B.; Ahmed, Z.; Sharma, U.; Adhikari, D. Does climate change affect the yield of the top three cereals and food security in the world? Earth 2022, 3, 45–71.
Lau, S.E.; Hamdan, M.F.; Pua, T.L.; Saidi, N.B.; Tan, B.C. Plant nitric oxide signaling under drought stress. Plants 2021, 10, 360.
Mohd Amnan, M.A.; Pua, T.L.; Lau, S.E.; Tan, B.C.; Yamaguchi, H.; Hitachi, K.; Tsuchida, K.; Komatsu, S. Osmotic stress in banana is relieved by exogenous nitric oxide. PeerJ 2021, 9, e10879.
Vats, S.; Kumawat, S.; Kumar, V.; Patil, G.B.; Joshi, T.; Sonah, H.; Sharma, T.R.; Deshmukh, R. Genome editing in plants: Exploration of technological advancements and challenges. Cell 2019, 8, 1386.
Wada, N.; Ueta, R.; Osakabe, Y.; Osakabe, K. Precision genome editing in plants: State-of-the-art in CRISPR/Cas9-based genome engineering. BMC Plant Biol. 2020, 20, 234.
Zhang, A.; Liu, Y.; Wang, F.; Li, T.; Chen, Z.; Kong, D.; Bi, J.; Zhang, F.; Luo, X.; Wang, J. Enhanced rice salinity tolerance via CRISPR/Cas9-targeted mutagenesis of the OsRR22 gene. Mol. Breed. 2019, 39, 47.
Bo, W.; Zhaohui, Z.; Huanhuan, Z.; Xia, W.; Binglin, L.; Lijia, Y.; Xiangyan, H.; Deshui, Y.; Xuelian, Z.; Chunguo, W.; et al. Targeted mutagenesis of NAC transcription factor gene, OsNAC041, leading to salt sensitivity in rice. Rice Sci. 2019, 26, 98–108.
Xie, Z.; Nolan, T.M.; Jiang, H.; Yin, Y. AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Front. Plant Sci. 2019, 10, 228.
Faraji, S.; Filiz, E.; Kazemitabar, S.K.; Vannozzi, A.; Palumbo, F.; Barcaccia, G.; Heidari, P. The AP2/ERF gene family in Triticum durum: Genome-wide identification and expression analysis under drought and salinity stresses. Genes 2020, 11, 1464.
Duan, Y.B.; Li, J.; Qin, R.Y.; Xu, R.F.; Li, H.; Yang, Y.C.; Ma, H.; Li, L.; Wei, P.C.; Yang, J.B. Identification of a regulatory element responsible for salt induction of rice OsRAV2 through ex situ and in situ promoter analysis. Plant Mol. Bio. 2016, 90, 49–62.
Liu, X.; Wu, D.; Shan, T.; Xu, S.; Qin, R.; Li, H.; Negm, M.; Wu, D.; Li, J. The trihelix transcription factor OsGT γ-2 is involved adaption to salt stress in rice. Plant Mol. Bio. 2020, 103, 545–560.
Nazir, R.; Mandal, S.; Mitra, S.; Ghorai, M.; Das, N.; Jha, N.K.; Majumder, M.; Pandey, D.K.; Dey, A. Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated genome-editing toolkit to enhance salt stress tolerance in rice and wheat. Physiol. Plant. 2022, 174, 12.
Wang, T.; Xun, H.; Wang, W.; Ding, X.; Tian, H.; Hussain, S.; Dong, Q.; Li, Y.; Cheng, Y.; Wang, C.; et al. Mutation of GmAITR genes by CRISPR/Cas9 genome editing results in enhanced salinity stress tolerance in soybean. Front. Plant Sci. 2021, 12, 779598.
Zhang, M.; Cao, Y.; Wang, Z.; Wang, Z.Q.; Shi, J.; Liang, X.; Song, W.; Chen, Q.; Lai, J.; Jiang, C. A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na(+) exclusion and salt tolerance in maize. New Phytol. 2018, 217, 1161–1176.
Tran, M.T.; Doan, D.T.H.; Kim, J.; Song, Y.J.; Sung, Y.W.; Das, S.; Kim, E.J.; Son, G.H.; Kim, S.H.; Van Vu, T.; et al. CRISPR/Cas9-based precise excision of SlHyPRP1 domain(s) to obtain salt stress-tolerant tomato. Plant Cell Rep. 2021, 40, 999–1011.
Amnan, M.A.M.; Aizat, W.M.; Khaidizar, F.D.; Tan, B.C. Drought stress induces morpho-physiological and proteome changes of Pandanus amaryllifolius. Plants 2022, 11, 221.
Zhang, Y.; Wang, X.; Luo, Y.; Zhang, L.; Yao, Y.; Han, L.; Chen, Z.; Wang, L.; Li, Y. OsABA8ox2, an ABA catabolic gene, suppresses root elongation of rice seedlings and contributes to drought response. Crop J. 2020, 8, 480–491.
Ogata, T.; Ishizaki, T.; Fujita, M.; Fujita, Y. CRISPR/Cas9-targeted mutagenesis of osera1 confers enhanced responses to abscisic acid and drought stress and increased primary root growth under nonstressed conditions in rice. PLoS ONE 2020, 15, e0243376.
Yin, X.; Biswal, A.K.; Dionora, J.; Perdigon, K.M.; Balahadia, C.P.; Mazumdar, S.; Chater, C.; Lin, H.C.; Coe, R.A.; Kretzschmar, T.; et al. CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice. Plant Cell Rep. 2017, 36, 745–757.
Caine, R.S.; Yin, X.; Sloan, J.; Harrison, E.L.; Mohammed, U.; Fulton, T.; Biswal, A.K.; Dionora, J.; Chater, C.C.; Coe, R.A.; et al. Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol. 2019, 221, 371–384.
Hughes, J.; Hepworth, C.; Dutton, C.; Dunn, J.A.; Hunt, L.; Stephens, J.; Waugh, R.; Cameron, D.D.; Gray, J.E. Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiol. 2017, 174, 776–787.
Clemens, M.; Faralli, M.; Lagreze, J.; Bontempo, L.; Piazza, S.; Varotto, C.; Malnoy, M.; Oechel, W.; Rizzoli, A.; Dalla Costa, L. VvEPFL9-1 knock-out via CRISPR/Cas9 reduces stomatal density in grapevine. Front. Plant Sci. 2022, 13, 878001.
Wang, L.; Chen, L.; Li, R.; Zhao, R.; Yang, M.; Sheng, J.; Shen, L. Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. J. Agric. Food Chem. 2017, 65, 8674–8682.
Nieves-Cordones, M.; Mohamed, S.; Tanoi, K.; Kobayashi, N.I.; Takagi, K.; Vernet, A.; Guiderdoni, E.; Perin, C.; Sentenac, H.; Very, A.A. Production of low-Cs+ rice plants by inactivation of the k+ transporter OsHAK1 with the CRISPR-Cas system. Plant J. 2017, 92, 43–56.
Wang, F.Z.; Chen, M.X.; Yu, L.J.; Xie, L.J.; Yuan, L.B.; Qi, H.; Xiao, M.; Guo, W.; Chen, Z.; Yi, K.; et al. OsARM1, an R2R3 MYB transcription factor, is involved in regulation of the response to arsenic stress in rice. Front. Plant Sci. 2017, 8, 1868.
Tang, L.; Mao, B.; Li, Y.; Lv, Q.; Zhang, L.; Chen, C.; He, H.; Wang, W.; Zeng, X.; Shao, Y.; et al. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep. 2017, 7, 14438.
Shao, X.; Wu, S.; Dou, T.; Zhu, H.; Hu, C.; Huo, H.; He, W.; Deng, G.; Sheng, O.; Bi, F.; et al. Using CRISPR/Cas9 genome editing system to create MaGA20ox2 gene-modified semi-dwarf banana. Plant Biotechnol. J. 2020, 18, 17–19.
Shimatani, Z.; Kashojiya, S.; Takayama, M.; Terada, R.; Arazoe, T.; Ishii, H.; Teramura, H.; Yamamoto, T.; Komatsu, H.; Miura, K.; et al. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol. 2017, 35, 441–443.
Talakayala, A.; Ankanagari, S.; Garladinne, M. CRISPR-Cas genome editing system: A versatile tool for developing disease resistant crops. Plant Stress 2022, 3, 100056.
Yin, K.; Qiu, J.L. Genome editing for plant disease resistance: Applications and perspectives. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2019, 374, 20180322.
Jiang, W.; Zhou, H.; Bi, H.; Fromm, M.; Yang, B.; Weeks, D.P. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 2013, 41, e188.
Xu, Z.; Xu, X.; Gong, Q.; Li, Z.; Li, Y.; Wang, S.; Yang, Y.; Ma, W.; Liu, L.; Zhu, B.; et al. Engineering broad-spectrum bacterial blight resistance by simultaneously disrupting variable tale-binding elements of multiple susceptibility genes in rice. Mol. Plant. 2019, 12, 1434–1446.
Oliva, R.; Ji, C.; Atienza-Grande, G.; Huguet-Tapia, J.C.; Perez-Quintero, A.; Li, T.; Eom, J.-S.; Li, C.; Nguyen, H.; Liu, B.; et al. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat. Biotechnol. 2019, 37, 1344–1350.
Wang, F.; Wang, C.; Liu, P.; Lei, C.; Hao, W.; Gao, Y.; Liu, Y.G.; Zhao, K. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE 2016, 11, e0154027.
Macovei, A.; Sevilla, N.R.; Cantos, C.; Jonson, G.B.; Slamet-Loedin, I.; Čermák, T.; Voytas, D.F.; Choi, I.R.; Chadha-Mohanty, P. Novel alleles of rice eif4g generated by CRISPR/Cas9-targeted mutagenesis confer resistance to rice tungro spherical virus. Plant Biotechnol. J. 2018, 16, 1918–1927.
Zhou, X.; Liao, H.; Chern, M.; Yin, J.; Chen, Y.; Wang, J.; Zhu, X.; Chen, Z.; Yuan, C.; Zhao, W.; et al. Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proc. Natl. Acad. Sci. USA 2018, 115, 3174–3179.
Thomazella, D.P.d.T.; Seong, K.; Mackelprang, R.; Dahlbeck, D.; Geng, Y.; Gill, U.S.; Qi, T.; Pham, J.; Giuseppe, P.; Lee, C.Y.; et al. Loss of function of a dmr6 ortholog in tomato confers broad-spectrum disease resistance. Proc. Natl. Acad. Sci. USA 2021, 118, e2026152118.
Kumar, N.; Galli, M.; Ordon, J.; Stuttmann, J.; Kogel, K.-H.; Imani, J. Further analysis of barley MORC1 using a highly efficient RNA-guided Cas9 gene-editing system. Plant Biotechnol. J. 2018, 16, 1892–1903.
Wang, Y.; Cheng, X.; Shan, Q.; Zhang, Y.; Liu, J.; Gao, C.; Qiu, J.-L. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 2014, 32, 947–951.
Nekrasov, V.; Wang, C.; Win, J.; Lanz, C.; Weigel, D.; Kamoun, S. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci. Rep. 2017, 7, 482.
Zhang, Y.; Bai, Y.; Wu, G.; Zou, S.; Chen, Y.; Gao, C.; Tang, D. Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant J. 2017, 91, 714–724.
Wan, D.-Y.; Guo, Y.; Cheng, Y.; Hu, Y.; Xiao, S.; Wang, Y.; Wen, Y.-Q. CRISPR/Cas9-mediated mutagenesis of VvMLO3 results in enhanced resistance to powdery mildew in grapevine (Vitis vinifera). Hortic. Res. 2020, 7, 116.
Wang, Y.Y.; Zhang, Y.J.; Zhou, R.; Dossa, K.; Yu, J.Y.; Li, D.H.; Liu, A.L.; Mmadi, M.A.; Zhang, X.R.; You, J. Identification and characterization of the bzip transcription factor family and its expression in response to abiotic stresses in sesame. PLoS ONE 2018, 13, 21.
Wei, J.; Fang, Y.; Jiang, H.; Wu, X.T.; Zuo, J.H.; Xia, X.C.; Li, J.Q.; Stich, B.; Cao, H.; Liu, Y.X. Combining QTL mapping and gene co-expression network analysis for prediction of candidate genes and molecular network related to yield in wheat. BMC Plant Biol. 2022, 22, 288.
Song, G.; Jia, M.; Chen, K.; Kong, X.; Khattak, B.; Xie, C.; Li, A.; Mao, L. CRISPR/Cas9: A powerful tool for crop genome editing. Crop J. 2016, 4, 75–82.
Ma, X.; Zhu, Q.; Chen, Y.; Liu, Y.-G. CRISPR/Cas9 platforms for genome editing in plants: Developments and applications. Mol. Plant 2016, 9, 961–974.
Li, M.; Li, X.; Zhou, Z.; Wu, P.; Fang, M.; Pan, X.; Lin, Q.; Luo, W.; Wu, G.; Li, H. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front. Plant Sci. 2016, 7, 377.
Xu, R.; Yang, Y.; Qin, R.; Li, H.; Qiu, C.; Li, L.; Wei, P.; Yang, J. Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J. Genet. Genomics 2016, 43, 529–532.
Zhang, Y.; Liang, Z.; Zong, Y.; Wang, Y.; Liu, J.; Chen, K.; Qiu, J.-L.; Gao, C. Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat. Commun. 2016, 7, 12617.
Rodriguez-Leal, D.; Lemmon, Z.H.; Man, J.; Bartlett, M.E.; Lippman, Z.B. Engineering quantitative trait variation for crop improvement by genome editing. Cell 2017, 171, 470–480.
Gao, H.; Gadlage, M.J.; Lafitte, H.R.; Lenderts, B.; Yang, M.; Schroder, M.; Farrell, J.; Snopek, K.; Peterson, D.; Feigenbutz, L.; et al. Superior field performance of waxy corn engineered using CRISPR-Cas9. Nat. Biotechnol. 2020, 38, 579–581.
Mao, H.; Jian, C.; Cheng, X.; Chen, B.; Mei, F.; Li, F.; Zhang, Y.; Li, S.; Du, L.; Li, T.; et al. The wheat ABA receptor gene TaPYL1-1b contributes to drought tolerance and grain yield by increasing water-use efficiency. Plant Biotechnol. J. 2022, 20, 846–861.
Soyk, S.; Muller, N.A.; Park, S.J.; Schmalenbach, I.; Jiang, K.; Hayama, R.; Zhang, L.; Van Eck, J.; Jimenez-Gomez, J.M.; Lippman, Z.B. Variation in the flowering gene self pruning 5g promotes day-neutrality and early yield in tomato. Nat. Genet. 2017, 49, 162–168.
Carmel-Goren, L.; Liu, Y.S.; Lifschitz, E.; Zamir, D. The self-pruning gene family in tomato. Plant Mol. Biol. 2003, 52, 1215–1222.
Klap, C.; Yeshayahou, E.; Bolger, A.M.; Arazi, T.; Gupta, S.K.; Shabtai, S.; Usadel, B.; Salts, Y.; Barg, R. Tomato facultative parthenocarpy results from slagamous-like 6 loss of function. Plant Biotechnol. J. 2017, 15, 634–647.

© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.

Upload a video for this entry

Information

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 :

Mohd Fadhli Hamdan

Chou Khai Soong Karlson

Ee Yang Teoh

Su-Ee Lau

Boon Chin Tan

View Times: 484

Update Date: 24 Oct 2022

Table of Contents

Video Upload Options

Confirm