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Parallel Analysis of Global Garlic Gene Expression and Alliin Content

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Parallel Analysis of Global Garlic Gene Expression and Alliin Content Yang et al. BMC Plant Biology (2021) 21:174 https://doi.org/10.1186/s12870-021-02948-0 RESEARCH ARTICLE Open Access Parallel analysis of global garlic gene expression and alliin content following leaf wounding Xuqin Yang1†, Yiren Su1†, Jiaying Wu1, Wen Wan1, Huijian Chen2, Xiaoying Cao1, Junjuan Wang1, Zhong Zhang1, Youzhi Wang2, Deliang Ma2, G. J. Loake3 and Jihong Jiang1* Abstract Background: Allium sativum (garlic) is an economically important food source and medicinal plant rich in sulfides and other protective substances such as alliin, the precursor of allicin biosynthesis. Cysteine, serine and sulfur is the precursor of alliin biosynthesis. However, little is known about the alliin content under abiotic stress or the mechanism by which it is synthesized. Results: The findings revealed that the content of alliin was lowest in the garlic roots, and highest in the buds. Furthermore, alliin levels decreased in mature leaves following wounding. Transcriptome data generated over time after wounding further revealed significant up-regulation of genes integral to the biosynthetic pathways of cysteine and serine in mature garlic leaves. Conclusions: The findings suggest that differential expression of cysteine, serine and sulfide-related genes underlies the accumulation of alliin and its precursors in garlic, providing a basis for further analyses of alliin biosynthesis. Keywords: Garlic, Allium sativum, Transcriptomics, Alliin, Gene prediction Background buds in a characteristic clove shape, are the most Garlic (Allium sativum L.), a diploid (2n = 2x = 16) economically important [2]. A key feature of garlic is plant species and one of the most medicinally and the production of secondary metabolites rich in sul- economically important members of the Allium fur, such as S-methyl-L-cysteine sulfoxide (MCSO, genus, has been widely cultivated for more than 5000 methiin), S-propyl-L-cysteine sulfoxide (PCSO, pro- years [1–3]. Studies have shown a number of bio- piin), S-trans-1-propenyl-L-cysteine sulfoxide (PECSO, logical functions from strong antioxidant potential [4], isoalliin) and, most importantly, S-allyl-L-cysteine stabilization of blood pressure [5], reduced cancer risk sulfoxide (ACSO, alliin) [9]. These sulphur com- [6], cardiovascular protection [7], and reduced hyper- pounds are also taste precursors, regulating the fla- lipidemia [8], with the roots, bulbs, leaves and sprouts vour and odour of the developing bulbs [10]. Allicin, all possessing important agronomical traits. Of these, which is derived from alliin, is another sulfur com- the bulbs, which consist of several abnormal axillary pound and the key bioactive molecule in garlic [11, 12].Variousinvivoandinvitrostudieshavedemon- * Correspondence: [email protected] strated the anti-apoptosis and anti-oxidation potential †Xuqin Yang and Yiren Su contributed equally to this work. of allicin [13]. However, allicin is also extremely un- 1 The Key Laboratory of Biotechnology for Medicinal Plant of Jiangsu stable at room temperature due to its rapid decom- Province, School of Life Science, Jiangsu Normal University, Xuzhou 221116, Jiangsu, China position into diallyl disulfides and sulfur dioxide [14]. Full list of author information is available at the end of the article © The Author(s). 2021 Open Access 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://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Yang et al. BMC Plant Biology (2021) 21:174 Page 2 of 10 Allicin is produced from alliin, which is located in transposable elements. Which helps explain the evolu- the cytoplasm, via alliinase [15], which is located in tion of allicin biosynthesis-related genes. Four GSH1- the vacuole. Accordingly, when cells are broken or orthologous genes, one GSH2-orthologous gene and one damaged, allinase is released, inducing the conversion PCS-orthologous gene were also identified, expression of of alliin into allicin [16, 17]. which was up-regulated during garlic bulb development. Alliin is the most abundant non-protein sulfur- These genes are therefore potential candidates of the containing amino acid in fresh garlic, accounting for more alliin biosynthesis pathway. than 90% of its sulfur compounds [18]. Stable and odorless Although genome sequencing is an effective tool, it is molecule [19], alliin is of significant nutritional and medi- both time-consuming and costly. In contrast, transcrip- cinal value [20], exhibiting antioxidant [21]andanti- tome analysis has the advantages of high speed, low cost inflammatory [22] activity, promoting cardiovascular func- and the absence of limitations in terms of genome com- tion [23] and conveying beneficial effects on certain intes- plexity [33]. In recent years, transcriptomics has been tinal diseases [24]. Alliin is synthesized in the leaves then used in correlation analysis of different traits, aiding transferred to the bulbs [25, 26], during which process, the studies of genetic association, notably in complex poly- roots absorb sulfates from the soil and transport them to ploid species [34–36], such as Salvia miltiorrhiza [37], the leaves. These sulfates are then used to synthesis gluta- Pinellia ternata [38], and Cicer arietinum L. [39] Mean- thione in the chloroplasts, which is then transferred to the while, Jun [2] carried out transcriptome analyses of gar- developing bulb via the vascular system. Alliin stored in the lic bulbs, and identified 22 candidate transcripts with leaves is also transported to the sprouts, protecting them complex interactions. Mitrová [40] through transcrip- from attack by microorganisms and herbivores [27]. tome analysis also revealed the corresponding genetic Despite the importance of alliin in the commercial po- changes in allinase during the whole cycle, while re- tential of garlic, the details of alliin biosynthesis remain ported that the transcription of two particular enzymes largely unknown. Based on the results of radiotracer ex- was highest during sprouting. Moreover, Einat [30] com- periments and chemical analyses [28], it is thought that bined transcriptome and proteome analyses of garlic the alliin biosynthetic pathway involves cysteine. Briefly, flowers and pollen revealed potential molecular markers the pathway involves S-alk(en)ylation of the cysteine resi- for male fertility and sterility. Liu [41] also carried out due in glutathione, followed by the removal of the glycyl association mapping of three yield traits in the garlic group to form an intermediate γ-glutamyl-S-alk(en)yl-L- bulb: bulb weight, bulb diameterand garlic quantity, re- cysteine. By ASFMO1(AsFMO1 is a flavin-containing vealing 17 significantly correlated single nucleotide poly- monooxygenase, in garlic, which is responsible for the S- morphisms (SNPs). oxygenation reaction in the biosynthesis of alliin) catalytic However, despite the above studies, transcriptome get alliin. However, others also support the involvement of analysis of alliin biosynthesis in garlic leaves after the serine-thiol pathway: bonding of serine with Acetyl wounding have yet to be carried out. In this study, we CoA to produce O- Acetylserine followed by the conjuga- carried out transcriptome analysis of the key pathways tion of O-Acetylserine with the allyl thiol compound S- thought to be involved in alliin metabolism over time allylcysteine, and lastly, S-allylcysteine oxidation of ACSO. after wounding. The findings provide a basis for the While γ-serine acetyl transpeptidase is thought to catalyse mechanism of alliin biosynthesis under physical stress. the first step, S-cysteine acetyl transpeptidase catalyses step 2, resulting in the formation S-allyl cysteine [29]. Un- Results derstanding the biosynthetic pathways of both cysteine Measurement of alliin content and serine is therefore important in determining the path- To determine the differences in alliin content among the way of alliin biosynthesis. garlic cloves, inner buds, roots, and sprouts, a post- Garlic (2n = 2x = 16) has a large genome [30]. It is esti- column derivatization method using ninhydrin was mated to be 15.9G and sterile cultivars, and therefore, established. The findings revealed that the bulbs contain no classical breeding or genetic studies have been car- the highest level of alliin (1.474 mg.ml-1, DW), while the ried out [31]. As a result, and despite its agronomic im- roots contain the lowest (0.019 mg.ml-1, DW). portance, garlic remains largely undomesticated, Next, to determine the alliin content of the garlic hampering its commercial potential. Liu [32] recently re- leaves after wounding, damaged leaves were sampled at ported the
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