Abstract
The genus Allium represents many economically important crops including onion (Allium cepa), shallot (A. cepa L. Aggregatum group), garlic (A. sativum), Welsh onion (A. fistulosum), and leek (A. ampeloprasum). Its consumption as ethnomedicine or food is mainly attributed to the medicinal and cuisinal properties, including anticholesterolemic, anti-asthmatic, and antimicrobial. However, the large genome size of many Allium species with a high level of duplication and repetitive DNA is the main constraint for any molecular-based studies. The present chapter aims to provide a documented source of new information regarding bioactive metabolites and their related genes for improving stress tolerance in Allium crops. We firstly provide an introduction about different species of Allium and their economic importance for the human diet. Secondly, the key bioactive metabolites and their biosynthesis pathway in different Allium species are discussed. Finally, we summarize and discuss the recent metabolome and transcriptome approaches of different Allium species in response to environmental stress.
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7.1 Introduction
Allium plants represent the most economically important and representative genus of the Alliaceae family. References to these plants in the Quran and Bible reflect their significance to ancient civilizations both as flavorful foods and healing herbs. Allium is a huge genus (850 species) that is spread widely across the Northern Hemisphere from the boreal zone to the dry subtropics. A region of high species diversity spreads from the Mediterranean Basin to Central Asia, and a second smaller center of species diversity is located in North America (Kamenetsky and Rabinowitch 2006; Fritsch et al. 2010; Abdelrahman et al. 2016, Abdelrahman et al. 2017d) (Fig. 7.1). The Allium species have adapted to diverse ecological niches, which led to the development of several distinct morphotypes, resulting in difficulties in classification and taxonomy of Allium (Gregory et al. 1998; Abdelrahman et al. 2015). A multidisciplinary approach, including morphological and anatomical examinations, and systematic studies using molecular and biochemical markers have led to an infrageneric classification of Allium species into six subgenera (Melanocrommyum, Rhizirideum, Caloscordum, Bromatorrhiza, Amerallium, and Allium) and 43 sections (Hanelt et al. 1992; Hanelt and Fritsch 1994; Khassanov 1996; Friesen et al. 1999; Fritsch and Friesen 2002; Ricroch et al. 2005; Fritsch et al. 2010). Many species of Allium genus have high economic importance, including vegetables [bulb onion (A. cepa), shallot (A. cepa L. Aggregatum group), Japanese bunching onion (A. fistulosum), garlic (A. sativum), leek, kurrat, and great-headed garlic (A. ampeloprasum), chives (A. schoenoprasum), Chinese chives (A. tuberosum)], and ornamentals [(A. giganteum, A. aflatunense, A. karataviense)]. Also, about two dozens of Allium species are locally collected or cultivated as highly valued seasonings and medicinal plants. However, detailed information about the widespread use of these species remains incomplete (Khassanov 1996; Friesen et al. 2000; Fritsch and Friesen 2002; Keusgen et al. 2006).
During initial domestication, many immediate ancestors of Allium species have either been changed or lost. For instance, increasing numbers of different repetitive DNAs or retrotransposons, the lower GC content together with a minor DNA restructuring by point mutation is accountable for the enormousness size and complexity of the genome of many Allium crop species. For example, 2C DNA amounts per genome in 75 Allium species range between 16.93 and 63.57 pg (Ohri and Pistrick 2001), and onion has 16,415 megabase pairs (MbPs) of DNA per 1C nucleus which is 6 times higher than maize (Zea mays) and 16 times than rice (Oryza sativa), while garlic has ~15, 901 Mbp (Orhi et al. 1998). Also, the GC content of onion DNA is 32%, which is considered as the lowest among angiosperms (Kirk et al. 1970). Such a complicated genome reorganization is estimated to cause the speciation of Allium, which is the primary factor for reproductive isolation followed by the enlargement of habitat range. Genetic shifts and severe unbalanced selection pressure by breeders and farmers resulted in the loss of many useful agronomic traits for modern agriculture; therefore, genes of potentially useful characteristics were lost or are not readily available for crop improvement (Friesen et al. 2000; Fritsch and Friesen 2002; Kamenetsky and Rabinowitch 2006; Keusgen et al. 2006; Abdelrahman et al. 2014; Abdelrahman et al. 2018).
With the rise of next-generation sequencing (NGS) technologies, an increase in the speed and efficiency of DNA sequencing with higher throughputs and greater genome coverage became achievable in many plant species including Allium (Abdelrahman et al. 2017a, b, c, d, f; Valliyodan et al. 2017; Yuan et al. 2017). These technologies led to the initial waves of crop genome sequences and facilitated the development of gene expression atlases and increased our understanding of the signaling pathways involved in the responses of plants to abiotic and biotic stressors (Rothberg et al. 2011; Pavlovich 2017; Abdelrahman et al. 2019b). The Allium international research community has developed several types of genetic stocks and applied these stocks to the latest modern technologies, which will be a milestone to accelerate Allium functional genomic studies. In this chapter, we will discuss the recent studies in Allium functional genomics as an innovative means of targeting the gene and bioactive metabolites responsible for the development of elite Allium varieties with unique chemical constituents and, subsequently, improved plant stress tolerance and human health benefits.
7.2 Organosulfur Compounds: A Prospective Active Ingredient for Allium Breeding
The Allium consumption as ethnomedicine or food ingredient is mostly associated with its nutritional and functional properties, which is mainly attributed to a variety of secondary metabolites (Caruso et al. 2014; Abdelrahman et al. 2016; Abdelrahman et al. 2019a). Among these secondary metabolites, organosulfur compounds are essential substances in terms of both biological activity and chemotaxonomic value of Allium species (Rose et al. 2005; Mostafa et al. 2013). There are four representatives of organosulfur compounds in Allium species, including (+)-S-(propyl)-L-cysteine sulfoxide (Propiin), (+)-S-(1-propenyl)-L-cysteine sulfoxide (Isoalliin), (+)-S-methyl-L-cysteine sulfoxide (Methiin), and (+)-S-(2-propenyl)-L-cysteine sulfoxide (Alliin) (Freeman and Whenham 1975; Hashimoto et al. 1984) (Fig. 7.2). These compounds are characteristics of each species and are generated by chemical transformation and cleavage of odorless, S-alk(en)yl cysteine sulphoxide precursors by the enzymes alliinase and lachrymatory-factor synthase (Jones et al. 2004). While S-alk(en)yl cysteine sulphoxides are found in the cytosol of the mesophyll tissue, alliinase is located in the vacuole of the vascular bundle sheath (Lancaster and Collin 1981). Once tissue being damaged by crashing or cutting alliinase is released and contact with S-alk(en)yl cysteine sulphoxides to cleave the C–S bond and generate sulfenic acid which is rapidly converted to thiosulfinates by non-enzymatic self-condensation (Yoshimoto and Saito 2017). Methiin is present in most of the Allium species and some Brassicaceae, alliin is characteristic of garlic, isoalliin is characteristic of onion and chive, while propiin is characteristic of onion, but it can be found in a minor content in most of the Allium species. Although methiin is present in less than 20% of total precursors in A. cepa, A. sativum, A. ampeloprasum, A. proliferum, A. galanthum, and A. tuberosum, however, some Allium species have a high content of methiin, which make them inappropriate for human consumption due to the strong pungent smell (Kamenetsky and Rabinowitch 2006; Pratt 2010, Ramirez et al. 2017; Putnik et al. 2019).
Furthermore, chemotaxonomy of 40 Allium species from different subgenera revealed at least seven different chemotypes and showed specific arrays of volatile organosulfur compounds in the rhizomatous species (Storsberg et al. 2003; Kamenetsky and Rabinowitch 2006). This classification can contribute to a better selection of wild species for breeding experiments to improve taste, aroma, and medicinal properties of interspecific Allium hybrids. For instance, a recent study using chromosomal addition lines revealed an increase in organosulfur compounds, including gamma-glutamyl-PrenCS, S-2-carboxypropyl glutathione (2-CPGTH) and methiin, cycloalliin in A. fistulosum with extra chromosome 2A from shallot (Abdelrahman et al. 2019a).
Differences between cultivar and species in flavor characteristics mostly arose from variability in their sulfur uptake and metabolism, and the availability of sulfur is one of the factors that control the biosynthesis of each flavor precursor (Fritsch 2001; Storsberg et al. 2003; Kamenetsky and Rabinowitch 2006). The Allium plants synthesize organic sulfur compounds using the inorganic sulfate absorbed from the soil. Sulfate is converted into sulfite by adenosine 5ʹ-phosphosulfate reductase (EC 1.8.4.9), and the latter converted into sulfide by sulfite reductase enzyme (EC 1.8.7.1). Sulfide is incorporated into cysteine, which subsequently undergoes two conversions, glutamylation and glycosylation, to yield glutathione (Turnbull et al. 1980; Kodera et al. 2017). Although the biosynthetic pathway of the flavor precursors, including (+)-S-alk(en)yl cysteine sulfoxides and their γ-glutamyl peptide relatives, has been published (Lancaster and Shaw 1989), there is still ambiguity about several stages, and whether the same pathway is followed in all tissues. It has been proposed that the biosynthesis of the flavor precursors in Alliums started with S-alk(en)ylation of the cysteine in glutathione, followed by transpeptidation to remove the glycyl group, oxidation to the cysteine sulfoxides, and, finally, removal of the glutamyl group to yield cysteine sulfoxides (Lancaster and Shaw 1989; Lancaster et al. 1989; Block 1992; Prince et al. 1997). An alternative biosynthetic pathway ignores glutathione in favor of straight thioalk(en)ylation of O-acetyl serine or alk(en)ylation of cysteine, followed by oxidation to a sulphoxide. In both of the pathways, few of the proposed enzymes involved in the biosynthesis of S-alk(en)yl-L-cysteine sulfoxides from Alliums have not been identified. A recent subcellular localizations and kinetic properties of three γ-Glutamyl transpeptidases (GGT; EC 2.3.2.2) genes including AsGGT1, AsGGT2, and AsGGT3 isolated from garlic suggested that these genes may contribute differently to the biosynthesis of alliin in garlic (Yoshimoto et al. 2015). To date, several studies have been conducted to characterize and identify GGTs in Allium plants, for instance, AcGGT partially purified from onion showed high substrate specificity to γ-glutamyl compounds, a putative intermediates of S-alk(en)yl-L-cysteine sulfoxide biosynthesis, suggesting the involvement of AcGGT in the biosynthesis of S-alk(en)yl-L-cysteine sulfoxides in onion (Lancaster and Shaw 1994). A partial cDNA of AsGGT, which has high sequence homology to AcGGT, was isolated from garlic, and its expression profiles suggested that AsGGT may play a role in synthesizing S-alk(en)yl-L-cysteine sulfoxides in garlic cloves during cold storage (Cho et al. 2012). Future investigations of the in vivo functions of different GGT will offer a better understanding of the molecular mechanisms underlying the biosynthesis of alliin and other cysteine sulfoxide compounds in Allium, which can be applied to future metabolic engineering of crop plants.
The role of organosulfur compounds in Allium abiotic stress tolerance is still unclear; however, some few evidences reported that Allium species and landraces grown under stress conditions exhibited high level of organosulfur compounds. For example, a comparative targeted metabolite profiling and transcriptome landscapes of tropical shallot doubled haploid (stress-tolerant) and cultivated onion doubled haploid, and their F1 hybrid revealed several key genes and metabolites related to organosulfur were introgressed in abiotic stress response were upregulated shallot and F1 genotypes as compared onion (Abdelrahman et al. 2015). Also the additional chromosome from shallot to Japanese bunching onion induced organosulfur compound accumulation under summer conditions (Masamura et al. 2011). Similarly, shallot landraces derived from Indonesia possessed high levels of methiin and isoalliin in comparison with different onion varieties (Ariyanti et al. 2018). In addition, a comparative study of antioxidant activities and organosulfur compounds in garlic, elephant garlic, and onion demonstrated a significant positive correlation between organosulfur compounds and antioxidant capacity in Allium crops (Kim et al. 2018). Nevertheless, there are no direct studies that addressed the in-depth role of organosulfur compounds in Allium abiotic stress tolerance, which remain to be a future task.
7.3 Steroidal Saponins in Allium Species: Anticancer, Antimicrobial, and Biosynthesis Pathway
Although organosulfur compounds have been considered a key component of Allium plants’ medicinal properties, various researchers tend to attribute the prospective medicinal benefits of Allium plants to other constituents, such as polyphenolic compounds, especially flavonoids, steroidal saponins as well as sugars (Lanzotti 2005; Stajner et al. 2006; Lanzotti et al. 2012; Abdelrahman et al. 2017e). The genus Allium is a rich source of steroidal saponins, which can be classified into spirostanol, furostanol, and cholestane saponins based on their sapogenin structure (Challinor and De Voss 2013; Mostafa et al. 2013; Abdelrahman et al. 2017d). Apart from the Amaryllidaceae family, steroidal saponins are also broadly spread in other monocot families, such as Costaceae, Asparagaceae, Liliaceae, Dioscoreaceae, Melanthiaceae, and Smilacaceae. These saponin compounds have also been reported in some dicotyledonous angiosperms: Zygophyllaceae, Plantaginaceae, Solanaceae, and Fabaceae. The earliest reports on Allium saponins date back to the 1970s through the identification of alliogenin in the bulbs of A. giganteum (Khristulas et al. 1970) and diosgenin in A. albidum (Kereselidze et al. 1970), which was followed by first chemical survey of saponins from the Allium genus by Kravets in (Kravets et al. 1990), and Lanzotti in (Lanzotti 2005), (Kravets et al. 1990, Lanzotti 2005). Since then, a huge number of new saponin compounds have been revealed. The Allium saponins are mainly bi- or mono-desmosides; however, a tri-desmodic cholestane glycoside has been described in the bulbs of A. macleanii (Inoue et al. 1995). The sugar chain in Allium saponins consists of branched or linear chains made up most often of glucose, galactose, rhamnose, arabinose, and xylose units (Mostafa et al. 2013; Sobolewska et al. 2016).
Saponins are considered accountable for various pharmacological properties of several plants, and they are recognized as bioactive constituents of Allium species (Sobolewska et al. 2016). There have been several reports addressing the pharmacological activities of steroidal saponins, including cytotoxic, antithrombotic, antifungal, anti-inflammatory, and immunomodulatory effects (Sparg et al. 2004; Sun et al. 2009; Lanzotti et al. 2012; Abdelrahman et al. 2017e). Saponins are potential anticancer molecules, and the induction of apoptosis by saponins has been defined in several studies, including inhibition of cancer migration (Sun et al. 2010; Zhao et al. 2014) and proliferation (Beit-Yannai et al. 2011; Zhang et al. 2012). Steroidal saponins isolated from different Allium species displayed amazing cytotoxic activities against different animal and human cancer cell lines, such as 4T1 breast carcinoma, B16 melanoma, hepatocellular carcinoma HepG2, fibroblast 3T3-L1, and pheochromocytoma PC12 cell lines (Chen et al. 2009; Luo et al. 2011; Yu et al. 2015). In vitro examination of the cytotoxic activity of Cepa2 steroidal saponin, isolated from the dry roots of shallot against P3U1 myeloma cancer cell line showed its high efficiency as an anticancer with 91.13% reduction in P3U1 cell viability (Abdelrahman et al. 2017e). The reduction of cell viability was correlated with the increase in reactive oxygen species levels in Cepa2-treated P3U1 cells (Abdelrhaman et al. Abdelrahman et al. 2017e). Similarly, Tuberoside M isolated from the seeds of A. tuberosum and F-gitonin isolated from the fresh bulbs of A. jesdianum inhibited the cancer cells growth, with IC50 = 6.8 and 1.5 μg/mL, respectively (Sang et al. 2001; Mimaki et al. Mimaki et al. 1999). More recently, the cytotoxic substance of A. chinense saponins (ACSs) inhibited the proliferation, cell migration, and colony formation of 4T1 and B16 cells in a dose-dependent manner (Yu et al. 2015). These studies above provide clear evidence for the anticancer activities of the natural saponin compounds isolated from Allium plants, and a strong basis for in-depth investigations for the development of novel anticancer drugs.
With increasing concern about the negative impacts of climate change on the development of plant disease epidemics and altering the interactions between plant and pathogens, greater effort toward improving plant disease resistance became a mandate. Although many steroidal saponin compounds isolated from diverse plant species have been reported to have antifungal activity, unfortunately, only a few studies have been performed so far on Allium steroidal glycosides antifungal properties (Mostafa et al. 2013; Sobolewska et al. 2016). Antifungal activity of Allium saponins is controlled by both the number and structure of the sugar residue and sapogenin type. Generally, saponins with spirostanol skeleton exhibited higher antifungal activity than furostanols (Mostafa et al. 2013). Lanzotti et al. (2012) provided a strong evidence for the significant differences in the potency of saponin compounds belonging to spirostane relative to furostane groups. For instance, gitogenin 3-O-tetrasaccharide and gigenin 3-O-trisaccharide, isolated from the bulbs of A. sativum var. Voghiera, were more active against Trichoderma harzianum and Botrytis cinerea than furostanol voghierosides isolated from the same plant (Lanzotti et al. 2012). Also, the sprirostanol Aginoside isolated from A. nigrum at 400 ppm completely inhibited the growth of Botrytis squamosa and C. gloeosporioides, and partially inhibited F. oxysporum f. sp. cepae and F. oxysporum f. sp. radicis-lycopersici (Mostafa et al. 2013). The influence of the structure of the sugar chain on the observed antifungal activity of Alliospirosides A isolated from the roots of shallot, inhibited a wide range of plant pathogenic fungi, including Alternaria ssp., Botrytis ssp., Colletotrichum spp., Curvularia lunata, Epicoccum nigrum, and Fusarium ssp. (Teshima et al. 2013). However, Alliospirosides A activity against Fusarium pathogens was relatively low in comparison with other phytopathogens (Teshima et al. 2013). Despite a large number of saponin compounds being isolated from different Allium species, little efforts have been invested in their antifungal activity. One of the main reasons for such drawback is the limited amount of the isolated pure compounds which are mostly being consumed through the identification and chemical structure elucidation methods by mass spectrometry and nuclear magnetic resonance (NMR).
In plants, steroidal saponins are mostly synthesized from lanosterol and cycloartenol via cholesterol and sitosterol, respectively. However, the steroidal saponin biosynthesis pathway in Allium has not been reported yet. Differential expression analysis of Asparagus racemosus fruit, leaves, and roots showed that expression of the transcripts involved in steroidal saponin biosynthesis is mainly upregulated in the leaf and root tissues, whereas triterpene saponins was dominated in fruit and leaf tissues (Srivastava et al. 2018). In a recent study, Abdelrahman et al. (2017d) were able to isolate and identify Alliospiroside A saponin compound in A. fistulosum (FF) with additional chromosome 2A (FF2A) from shallot (AA) with potent role in defense mechanism against Fusarium pathogens. In addition, differential gene expression analyses of AA and FF2A as compared to FF (as a control) revealed a strong upregulation of the saponin downstream pathway, including glycosyltransferase, cytochrome P450, and beta-glucosidase in chromosome 2A (Abdelrahman et al. 2017d). An understanding of the biosynthesis-related genes and saponin compounds would facilitate the development of plants with unique saponin content and, subsequently, improved disease resistance.
7.4 Metabolomic and Transcriptomic Landscapes of Allium Crops Under Environmental Stress
The heavy yield losses in primary crops due to global warming and the increasing demand for food mean that there is a crucial need to improve food security (Abiala et al. 2018; Zhang et al. 2019). However, the development of abiotic stress-resilient crops requires an in-depth information about the biological processes that enable plants to survive in stressful environments, and this information can be achieved from “omic” studies, such as metabolomics, proteomics, transcriptomics, and genomics (Hirata et al. 2016; Abdelrahman et al. 2017b; Abdelrahman et al. 2018a, b; Galsurker et al. 2018; Wang et al. 2018). Unfortunately, there are limited studies addressing the Allium metabolome and transcriptome profiling in response to environmental stress, and thus the Allium international community needs further efforts in this regard. Transcriptome analysis between inner and outer scales of commercial brown onion cv. “Orlando” in response to the heat stress demonstrated that oxidation and lipid metabolism pathways, as well as cell-wall modification were highly expressed in the onion outer scale under heat stress (Galsurker et al. 2018). However, defense response-related genes such as those encoding antioxidative stress defense, heat shock proteins, or production of osmo-protectant metabolites were highly induced in the inner scale (Galsurker et al. 2018). These transcriptomic data led to a conceptual model that suggests consecutive processes for the development of desiccation and browning of the outer scale versus processes associated with defense response and heat tolerance in the inner scales (Galsurker et al. 2018). Transcriptome-based sequencing of cold-tolerant and cold-susceptible genotypes of onion under freezing and cold conditions indicated that several genes were significantly induced by freezing and cold stress in tolerant lines relative to susceptible genotype (Han et al. 2016). Among these transcript, genes encoding hypothetical proteins, zinc finger (ZIP) proteins, heat shock proteins (HSPs), and CBL-interacting protein kinase (CIPK), in addition to subset of transcription factors, particularly those that function as activators including dehydration-responsive element (DRE)-binding (DREB), CBL, MYB, bZIP, zinc finger of Arabidopsis thaliana (ZAT), HSPs and basic helix-loop-helix (bHLH) were drastically changed during freezing and cold conditions (Han et al. 2016). Similarly, genome-wide transcriptome profiling analysis of garlic under low temperature stress indicated that enzyme-encoding genes, which significantly enriched the pathway “proteasome,” are potentially involved in the garlic discoloration under low temperature stress, such as γ-glutamyltranspeptidase-, δ-aminolevulinic acid dehydratase-, and alliinase-encoding genes (Li et al. 2018). These stress-responsive genes are possibly responsible for the low-temperature-induced garlic discoloration (Li et al. 2018). Effects of salinity stress on the growth parameters and K+/Na+ ratio of Allium vegetables (Welsh onion and Wakegi) using diverse concentrations of seawater demonstrate stunting of plants; however, the rate of growth reduction under salinity stress varies widely among different Allium plants (Arakaki et al. 2014). The chlorophyll content as in term of SPAD values of the leaves of the Welsh onion decreased, whereas the SPAD value of the two types of Wakegi cultivars increased (Arakaki et al. 2014). In addition, the total sugar and phenolic contents increased significantly compared with the respective controls under seawater treatment (Arakaki et al. 2014). Environmental stress affects plant growth, thus identification of stress biomarkers is a major prerequisite for the breeding of stress-tolerant crops. In this regard, because of its high adaptability to subtropical and tropical environment, shallots are recognized as an important genetic resource for the breeding of common onion (Abdelrahman et al. 2015). Using liquid chromatography quadruple-mass spectrometer (LC-QqQ-MS), the bulb onion double haploid, shallot double haploid, and its F1 hybrid were evaluated. In total, 113 targeted metabolites were detected, and the principal component analysis and volcano plot analysis clearly showed genotype-specific metabolites, which can be used as metabolic markers of environmental tolerance (Abdelrahman et al. 2015). Similarly, integrated transcriptome and metabolome analysis of A. fistulosum with additional chromosome 5A from shallot revealed an accumulation of several flavonoid compounds which are majorly involved in abiotic and biotic stress tolerances (Abdelrahman et al. 2019a). Also the increase in flavonoid pool in A. fistulosum with additional chromosome 5A from shallot was consistent with the upregulation of many upstream and downstream flavonoid biosynthesis and regulatory genes (Abdelrahman et al. 2019a). The above results confirmed that shallot can be a potential genetic resource for the improvement of onion stress tolerance. Likewise, Zhang et al. (2018) used transcriptome analysis of two contrasting dark-red and white onion cultivars, revealing that both flavonoid 3ʹ,5ʹ-hydroxylase (F3ʹ,5ʹH) and dihydroflavonol 4-reductase (DFR) genes play major role in the biosynthesis of dark-red bulbs, and the expression levels of flavonol synthase (FLS) and DFR genes may act to block blue pigmentation. In addition, the positive variation in the F3ʹ,5ʹH/F3ʹH ratio also affects onion bulb color diversity (Zhang et al. 2018). A recent study using comparative transcriptome analysis of cold-tolerant and sensitive bulb onions provides further information regarding the transcriptional changes underlying cold and freezing tolerance mechanisms in addition to molecular markers that would facilitate gene mapping and genetic diversity analysis (Han et al. 2016).
7.5 Future Aspects for Allium Functional Genomics
Allium transcriptomics and metabolomics will elucidate characteristic metabolites and their biosynthesis or regulatory related genes within different accessions, landraces, and cultivars. The individual bio-resource-specific metabolic patterns can be used for molecular breeding of Allium crops while the broad metabolic profiles of Allium bioresources can be used for integrated omics approaches. Further integrated omics approaches, e.g., correlation analysis between transcriptome and metabolome, linkage mapping, can elucidate the gene-to-metabolite networks in environmental responses or stress. In this regard, Allium transcriptome database (Allium TDB; http://alliumtdb.kazusa.or.jp/) provides a comprehensive information of the transcriptome analysis in different Allium species that can be used for further genetic and molecular breeding studies. The integration of metabolomics and transcriptomics will provide insight into the molecular mechanism of Allium metabolite biosynthesis, which can be used for elucidation of the molecular architecture underlying environmental responses and stress tolerance in Allium.
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Abdelrahman, M. (2020). Allium Functional Genomic Development for Future Climatic Changes. In: Kole, C. (eds) Genomic Designing of Climate-Smart Vegetable Crops. Springer, Cham. https://doi.org/10.1007/978-3-319-97415-6_7
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