Fruit Crop Improvement with Genome Editing, Transgenic Approaches: Comparison
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Fruit crop species contribute to nutritional and health security by providing micronutrients, antioxidants, and bioactive phytoconstituents, and hence fruit-based products are becoming functional foods presently and for the future. The threat of climate change and need for improvement in several traits including biotic and abiotic stress tolerance and higher nutritional quality has necessitated novel biotechnological  and genomics strategies for large-scale multiplication of elite clones, in vitro, mutagenesis, genetic transformation and genome editing for a diverse agronomic and nutritional quality traits. 

  • fruits
  • genomics
  • fruit quality
  • transgenic crops
  • genome editing

1. Genomics Insights into Fruit Quality

Since the advent of genomics tools and availability of sequencing platforms for most organisms, functional genomic analysis has become a reality in many crops. In fruit crops, genomic sequence information has been reported [24,90,91][1][2][3] paving the way for molecular insights into fruit quality and plant traits based on whole-genome or single gene duplication, transposon insertions, and gene function. The red fruit color in many fruit crops has been shown to be due to specific MYBs mediated regulation of different anthocyanins, phlobaphenes, and betalains [92][4]. In addition, MYBs also have a role in carotenoid synthesis and flavor, texture, taste and aroma, astringency, and piquancy [92,93][4][5]. It is also possible to induce higher levels of flavonoids through the overexpression approach; for example, in apple, MYB10 resulted in enhanced anthocyanins including epicatechin, procyanidin B2, and quercetin glycosides and, when the MYB10 engineered apples were fed to mice, altered expression of inflammatory genes and reduced inflammation was observed in treated mice [94][6]. The studies suggest that fruit nutritional quality may be manipulated through MYB transcription factors for better health.
Gene duplications have resulted in fruit sweetness, nutritional content, and quality, e.g., high ascorbic acid associated with GalUR gene expansion in orange and jujube fruits [95,96][7][8], and fruit sweetness associated with expansion of sorbitol metabolism-related genes S6PDH, SDH, and SOT in fruits of the Rosaceae [97][9] and pear [98][10]. Variation in gene structure, phenotype, and functional attributes in fruit crop genomes has been shown to be associated with transposon insertion(s), for example, high-fruit quality in apple with a long terminal repeat retrotransposon insertion upstream of MdMYB1 [99[11][12],100], parthenocarpic fruit development in apple due to insertion in MdPI gene [101][13], TE insertion in the 5′ flanking region of MYBA1 blocking anthocyanin expression and yielding white berry skin color [102[14][15],103], blood orange color due to a Copia retrotransposon insertion [104][16], retrotransposon Rider insertion leading to elongated fruit shape in tomato [105][17], and transposon insertion in the YUCCA gene in peach causing stony hard phenotype [106][18].
Genomics based approaches have relevance to fruit crop breeding because of the limitations of long generation time and extended juvenile period [24,107,108,109][1][19][20][21]. Approaches such as GWAS (genome wide association) enable the appraisal of the positions and effects of QTLs/genes using available cultivars/lines and does not need a segregating progeny [109][21], whereas genomic selection (GS) can be useful to accurately exercise selection and genetic gain required for the improvement of fruit quality and yield traits [110][22]. Early selection during the juvenile phase can fasten the selection efficiency to minimize the population required to be taken to subsequent field trials [111,112][23][24]. QTLs for several important agronomic traits such as fruit quality and disease resistance have been reported and are being used in marker-assisted breeding [108][20]. QTLs have been developed for different fruit related characters such as harvest time, fruit skin color, fruit weight, and sugar content in apple, pear, peach, mango, avocado, papaya, and grapevine [113,114,115,116,117,118,119,120][25][26][27][28][29][30][31][32]. QTLs for disease resistance include scab resistance in apple [121][33] and pear [122][34], plum pox virus resistance in apricot [123][35], brown rot resistance in peach [124][36], and downy and powdery mildew resistance in grapevine [125,126][37][38]. Major QTLs were mapped on linkage group 3 for skin and flesh color (anthocyanin pigment) in sweet cherry, anther color in almond × peach progenies, and skin color in peach, Japanese plum, and apricot [127,128][39][40]. Advances in sequencing methods have facilitated the detection of polymorphism at single nucleotide level in apple, pear [129][41], prunus [130][42], plum [131][43], citrus, and banana [132][44]. Cao et al. [133][45] performed GWAS in 104 landrace accessions of peach using 53 genome-wide SSR markers and found good association with fruit traits and phenological period. Another GWAS based study in Japanese pear using 76 cultivars showed association of 162 markers with fruit harvest time and black spot resistance [134][46]. In a significant GWAS study in apple, Kumar et al. [135][47] found few hundred SNPs associated with fruit related traits.

2. Transgenic Approaches

Genetic engineering based on genetic transformation methods is now routinely applied to improve plants [136][48]. Transgenic breeding has an important role in the improvement of fruit crops, as fruit crop breeding is limited by problems such as long-life cycle, propagation method, high heterozygosity, and reproductive barriers [137][49]. Among the different transformation methods, Agrobacterium tumefaciens mediation is widely used based on efficient tissue and cell culture conditions, somatic embryogenesis, and plant regeneration. Genetic transformation of fruit crops has been very successful for enhancing disease resistance and drought, frost, and salt tolerance, modified plant growth pattern, and fruit quality [6][50]. Since the first commercialization of genetically engineered Flavr Savr™ tomato [138][51], several fruit crops have been transformed using a wide variety of genes for improving plant productivity, resistance to insect/pests and diseases, and fruit ripening. There have been several examples of induction of abiotic stress tolerance in fruit crops [5][52]. Cold tolerance has been developed in apple by overexpression of the cold-inducible Osmyb4 gene [139][53], multiple stress tolerance in banana plants by overexpressing the stress-responsive WRKY transcription factor (MusaWRKY71) gene [140][54], drought and salt tolerance in banana through overexpression of the dehydrin gene [141][55], cold tolerance in papaya by expression of a Transcriptional activator gene, C-repeat binding factor (CBF) [142][56], and salt tolerance in kiwi fruit through expression of AtNHX1 with high K to Na ratio [143][57]. To impart resistance to Xanthomonas wilt caused by Xanthomonas campestris pv. Musacearum, hypersensitive response-assisting protein (Hrap) or plant ferredoxin-like protein (Pflp) gene from sweet pepper (Capsicum annuum) was constitutively expressed, and resistance was achieved in banana transgenic plants [144][58]. Transgenic banana plants of cv. Grand Naine were developed for fungal disease resistance using three genes (endochitinase gene from Trichoderma harzianum, stilbene synthase from grape, and superoxide dismutase from tomato) [145][59]. One of the successful transgenic events in banana include the biofortification of pro-vitamin A by using phytoene synthase enzyme (PSY) and iron (Ferritin gene from soybean) [146,147][60][61].
Development of transgenic fruits began with the ‘first phase’ in which fruit crops such as apple, pear, plum, cherry stock, grapes, walnuts, kiwifruit, citrus, and European chestnut were all transformed using the Agrobacterium method. In the second phase of development, RNAi technologies were majorly adopted for generating GM fruit crops (plum, cherry, apple) in addition to fine-tuning of protocols for Agrobacterium genetic transformation (blueberry, sour cherry), marker-free plants (apple, citrus, and apricot), and commercialization of some transgenic events, such as of non-browning apples. Phase II has covered the development of protocols for genome editing in fruit crops (apple, grape, sweet orange, grapefruit, kiwifruit). In major food crops, adoption of GM varieties has been phenomenal, with large areas under cultivation and economic gain [148][62]. A report by ISAAA in 2019 estimates that GM crops are grown in 29 countries on 190.4 million hectares (~112-fold increase over 1.7 million hectares in 1996). This includes growing of GM fruit crops in countries such as the USA (papaya, squash, apple), China (papaya), and Costa Rica (pineapple). GM virus-resistant papaya has been the most widely cultivated genetically engineered fruit, followed by virus-resistant squash, apples, and pineapple.

3. New Breeding Techniques

The advances in the new breeding techniques such as cisgenesis/intragenesis, RNAi, and genome editing have provided great impetus to targeted trait improvement [149,150][63][64]. It is significant to note the success achieved in the improvement in quality attributes and those conferring better plant architecture and tolerance to biotic and abiotic stresses. The cisgenesis and intragenesis strategies rely on the incorporation of genetic sequences derived from sexually compatible species or the host plant itself (thus obviating the concern of foreign sequences in the host genome), and there have been developments in the isolation and application of cisgenic/intragenic reporter genes and promoters and selectable markers [151,152][65][66]. On the other hand, the phenomenon of RNA interference (RNAi) is based on the naturally conserved mechanism in plants and operates through the interference of translation of mRNA through the mediation of double-stranded RNA (dsRNA) molecules that target the silencing of specific transcripts in a sequence-dependent manner [153][67]. These biotechnological advances have been successfully exploited in fruit crops; however, limitations of efficient regeneration system, long generation time, and genotypic dependency still exist, warranting optimization of culture parameters [154,155][68][69]. Nevertheless, there has been significant research efforts in fruit crops on the implementation of the above NBTs in fruit crop improvement [156][70], and it is interesting to note that cisgenesis and RNA interference have been successful for the development of transgenic fruit crops for different plant traits.

4. Genome Editing

One of the advancements in the past decade has been the precise editing of the plant genome [178][71]. Plant genome editing has immense scope for the targeted modification of plant genes controlling various important traits. The method is based on a restriction nuclease that can detect specific sequences in genomic locations and subsequently cut the specific gene sequences. Named molecular scissors, the nucleases are zinc finger nucleases (ZFNs), transcription activator-like effector-based nucleases (TALEN), and the clustered regularly interspaced short palindromic repeats associated nucleases (CRISPR/Cas) [179,180][72][73]. All these nucleases (ZFNs and TALENs) are studied with successful editing opportunities in a wide variety of organisms ranging from plants to animals; however, based on the cumbersome methodologies and cost involved in the genome editing process, these are now replaced by a popular method referred to as CRISPR/Cas. Currently, this method is extensively used in plant genome editing [179,181][72][74] and comprises RNA guided engineered nucleases that recognize their associated nucleotide sequences in the target sequence (genes). The process of genome editing is accomplished either by directly delivering the single-guide RNA (sgRNA) with pre-complexed purified CAS9 protein or through cell transfection with a plasmid encoding CRISPR-associated protein 9 (CAS9) and sgRNA [182][75]. CRISPR/Cas9 system has been applied in several fruit crops, including tomato (Solanum lycopersicum) [183][76], apple (Malus domestica) [184][77], grape (Vitis vinifera) [185][78], grapefruit (Citrus paradisi) [186][79], sweet cherry [187][80], strawberry, orange, and banana. Some notable examples of genome editing in fruit crops are presented.
Some successful examples include development of disease resistance against citrus canker in Wanjincheng orange upon the deletion of entire EBEPthA4 sequence from both CsLOB1 alleles [188][81], high resistance of grapes to Botrytis cinerea, by CRISPR/Cas9-mediated knockout of WRKY52 [189][82], and lower susceptibility to the fire blight disease pathogen, Erwinia amylovora, in apple by CRISPR/Cas9-mediated alteration in MdDIPM4 [190][83]. Tripathi et al. [191][84] developed banana plants resistant to banana streak virus, one of several serious diseases, through CRISPR/Cas9 mediated induction of mutations in the BSV sequences. They observed that genome-edited plants displayed no symptoms of viral disease. Banana plants exhibiting dwarfism have also been generated using the CRISPR/Cas9 system by mutations in the MaGA20ox2 gene, which regulates endogenous GA levels [192,193][85][86] suggesting the usefulness of the genome editing tool for developing dwarf banana cultivars.
Fruit crop improvement through conventional means is often hampered by a long generation period and long juvenile period, in the range of 13–16 years. Since juvenility is associated with high levels of terminal flowering (TFL) protein, intersecting studies by Charrier et al. [190,200][83][87] demonstrated early flowering by editing of the genes (MdTFL1.1, PcTFL1.1), resulting in 93% apple lines and 9% pear lines. Such studies go a long way in establishing fast breeding schemes for fruit crops. In other interesting research, the juvenile phase in fruit crops could be shortened through inducing a flowering gene or/and silencing a floral repressor combined with MAS [191,192,201,202][84][85][88][89].
There have been several studies demonstrating the potential of genome editing in crop plants and that the technology could contribute to global food security and climate resilience [203,204][90][91]. Globally, several countries have already adopted regulations for the GE plants for commercialization and/or cultivation [205][92] based on the premise that the use of the GE crops in agriculture is similar to conventionally bred lines, provided they do not contain a transgene. Menz et al. [206][93] introduced the term ‘marker-oriented’ for the genome edited events based on the criteria that the editing is applied in a crop plant or ornamental plant, the trait has relevance to plant functionality, and the event is analyzed as being distinct and unique. In an interesting study, Shew et al. [207][94] investigated the public responses in some countries, including the USA, Canada, Belgium, France, and Australia, to see if they were willing to accept and consume both GM and CRISPR foods. The data suggest that 56, 47, 46, 30, and 51% of respondents in the USA, Canada, Belgium, France, and Australia, respectively, showed willingness to consume both GM and CRISPR foods and were more willing to consume CRISPR than GM food.
Buchholzer and Frommer [205][92] summarized the present status of GE crops in the global context and concluded that the USA and several other countries were classified as transgene-free, and that they are as equivalent to conventionally bred lines. Several countries, including Russia, countries in Central and South America, two countries in Africa, China, and India have developed and placed new guidelines for the use of genome-edited plants in agriculture. Regulatory guidelines to exempt GE crops from GMO regulations are also being proposed in Europe, the UK, and Switzerland [205][92].
Despite the success achieved in genome editing of fruit species, some of the challenges that need extensive research include lack of annotated genomes, large genome size, long in vitro growth periods, dependence on a specific genotype and mode of transformation, lack of stable transformation of a wide range of fruit crops, and polyploidy associated problems of having multiple homologous genes. There has been some success of multiallelic editing in the case of banana [206][93] and induction of allelic variants and their segregation to enable developing genome editing in polyploid species [207][94]. Further, genetic variation in fruit architecture or quality traits governed by SNPs can be manipulated through base replacement using a homology directed repair method [208][95]. Successful examples include tomato [208,209][95][96]. Prime editing has been developed to enable precise alteration of a specific DNA base replacement [210,211][97][98].

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