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Genome-Edited Camelina Sativa with a Unique Fatty Acid Content and Its

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Genome-Edited Camelina Sativa with a Unique Fatty Acid Content and Its Kawall Environ Sci Eur (2021) 33:38 https://doi.org/10.1186/s12302-021-00482-2 REVIEW Open Access Genome-edited Camelina sativa with a unique fatty acid content and its potential impact on ecosystems Katharina Kawall* Abstract ‘Genome editing’ is intended to accelerate modern plant breeding enabling a much faster and more efcient devel- opment of crops with improved traits such as increased yield, altered nutritional composition, as well as resistance to factors of biotic and abiotic stress. These traits are often generated by site-directed nuclease-1 (SDN-1) applications that induce small, targeted changes in the plant genomes. These intended alterations can be combined in a way to generate plants with genomes that are altered on a larger scale than it is possible with conventional breeding techniques. The power and the potential of genome editing comes from its highly efective mode of action being able to generate diferent allelic combinations of genes, creating, at its most efcient, homozygous gene knockouts. Additionally, multiple copies of functional genes can be targeted all at once. This is especially relevant in polyploid plants such as Camelina sativa which contain complex genomes with multiple chromosome sets. Intended alterations induced by genome editing have potential to unintentionally alter the composition of a plant and/or interfere with its metabolism, e.g., with the biosynthesis of secondary metabolites such as phytohormones or other biomolecules. This could afect diverse defense mechanisms and inter-/intra-specifc communication of plants having a direct impact on associated ecosystems. This review focuses on the intended alterations in crops mediated by SDN-1 applications, the generation of novel genotypes and the ecological efects emerging from these intended alterations. Genome editing applications in C. sativa are used to exemplify these issues in a crop with a complex genome. C. sativa is mainly altered in its fatty acid biosynthesis and used as an oilseed crop to produce biofuels. Keywords: Genome editing, CRISPR/Cas, Camelina sativa, Environment, Fatty acid composition, Polyploidy, Volatile organic compounds, Plant communication Background literature reviews show that CRISPR/Cas has become ‘Genome editing’ encompasses techniques such as oli- one of the most dominant techniques of SDNs applied in gonucleotide-directed mutagenesis (ODM) and site- plants over the last few years [3, 4]. Terefore, the focus directed nucleases (SDNs) like zinc fnger nucleases here is on CRISPR/Cas-applications. CRISPR/Cas allows (ZFNs), transcription activator-like efector nucleases the targeting of an endonuclease (e.g., Cas9 from Strep- (TALENs), meganucleases and clustered regularly inter- tococcus pyogenes) to specifc genomic regions using a spaced short palindromic repeats/CRISPR-associated guide RNA (gRNA) [5, 6]. Te gRNA is designed depend- (CRISPR/Cas) techniques. In this paper the terminol- ing on the genomic loci to be altered. Cas9 interacts with ogy ‘genome editing’ is used even though there is some the gRNA and upon recognition of the target sequence controversy about the term [1, 2]. Recently published introduces a DNA double-strand break (DSB) at that part of the genome [7]. DNA DSBs subsequently activate the *Correspondence: [email protected] non-homologous end joining (NHEJ) repair and homol- Fachstelle Gentechnik und Umwelt, 80807 Munich, Germany ogy-directed repair (HDR) [8–10]. Te NHEJ pathway is © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Kawall Environ Sci Eur (2021) 33:38 Page 2 of 12 known to be error-prone and frequently results in base Camelina is closely related to the plant model organ- insertions or deletions (indels) at the DNA break sites ism Arabidopsis thaliana and the oilseed crop Brassica [11]. Tese indels can generate frameshift mutations napus. Unlike other crops of the Brassicaceae family, or disrupt important functional domains, which, for camelina has historically not been subjected to extensive example, disturb the functions of the target genes [12]. breeding, and only a small number of cultivars are availa- Te HDR pathway utilizes exogenous DNA donor tem- ble for agricultural purposes [41]. However, over the pre- plates to introduce nucleotide substitutions and DNA vious decade, C. sativa has become more popular mainly insertions at the target sites [13, 14]. Applications using because of its seed oil composition. Camelina oil contains SDNs are used to either introduce small-sized, undi- high amounts of polyunsaturated fatty acids (PUFAs) rected (SDN-1) or directed sequence changes (SDN-2 such as linoleic acid and linolenic acid, which are essen- and SDN-3) at specifc, predefned genomic loci [15]. tial omega-6 and omega-3 fatty acids, respectively [42, SDN-3 approaches aim to insert transgenic constructs 43]. Te oil is mainly used to produce biofuels, industrial at specifc, predefned locations [16]. In addition to the compounds, dietary supplements and human food [44– intended alterations, CRISPR/Cas causes unintended 46]. PUFAs are known for the formation of trans-fatty alterations including of-target efects, on-target efects acids during processing as well as their oxidative instabil- and chromosomal rearrangements [4, 17–21]. Tese ity. Terefore, the genetic material of camelina is being unintended alterations could potentially lead to a variety altered to shift the content from linoleic and linolenic of unexpected efects. For example, the integrity of a non- acid towards the monounsaturated fatty acid oleic acid target gene may be compromised if its coding region has which becomes less easily oxidized. been cleaved by CRISPR/Cas. Tis could lead to changes In general, the outcomes of genome editing applica- in the organisms’ metabolism, which could afect its tox- tions in crops are considered to require assessment on icity and allergenicity. Such efects are highly dependent three diferent levels [3, 22, 47]: in regard to (1) unin- on the genomic context within which such unintended tended efects resulting from the genetically engineer- alterations occur [3, 22]. Unintended efects can also be ing process, (2) the efects of the intended alteration(s) induced by applying frst-generation genetic engineer- on the metabolism of the genome-edited organism ing techniques to insert the CRISPR/Cas components and its overall composition, and (3) the ecological into plant cells [23–28]. A detailed and comprehensive impact of the genome-edited organism on the receiving description of unintended efects in the genome that cor- environment(s). Tis paper uses published research on relate with the application of genome editing and older the application of SDN-1 in C. sativa to provide evidence genetic engineering techniques is given elsewhere [3, 22]. of the extent of genomic changes possible using only Here, the special focus is the potential of SDN-1 tech- SDN-1 applications and how these intended changes have niques to generate novel genotypes and the impact of the potential to unintentionally alter secondary metabo- intended changes in genome-edited plants in relation lism. Te intended trait and potential unintentional to the interactions in their respective environments. changes to secondary metabolism are considered in the Numerous applications of genome editing in crops have context of potential ecological consequences following a already demonstrated that SDN-1 techniques can pro- release to the environment. Finally, the signifcance in the duce plants with novel genotypes resulting in traits EU for the regulation of genome-edited crops, developed unlikely to be achieved by conventional breeding tech- through the application of SDN-1, is outlined. niques [3, 4, 29–34]. Camelina sativa is an allohexaploid plant composed Genomic content of C. sativa of three sub-genomes which originate from closely Major agricultural relevant crops such as rapeseed, related species [35, 36]. Tus, it contains multiple alleles wheat, potato, cotton, apple, sugarcane and camelina of homologous genes. SDN-1 applications have already are polyploid, i.e. combine more than two paired sets been applied in C. sativa, primarily to alter fatty acid of chromosomes, which either originate from genome composition [37–39], but also modulating the seed meal doubling within a species (autopolyploids) or interspe- protein composition by editing factors such as crucif- cies hybridization (allopolyploids) [35]. Hutcheon et al. erins [40]. Such alterations are extremely difcult with (2010) suggested that C. sativa is allohexaploid with three conventional or mutagenesis breeding as changes to mul- single-copy nuclear genes present as three paralogous tiple alleles of genes are required. Tus, C. sativa serves copies in the genome [48]. Kagale et al. (2014) confrmed as a good example to demonstrate the power of SDN-1 the allohexaploidy by publishing a reference genome genome editing. and showing that camelina contains three sub-genomes C. sativa is an annual plant in the Brassicaceae family of an unknown origin [49]. One of the sub-genomes and cultivated mostly in Europe and in North America. contains six chromosomes, while the other two contain Kawall Environ Sci Eur (2021) 33:38 Page 3 of 12 seven chromosomes each [49]. Recently, it was proposed desaturase (FAD2) in the endoplasmic reticulum (ER) 6 that the allohexaploid genome of C.
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