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Comprehensive Metabolite Profiling in Genetic Resources of Garlic

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Comprehensive Metabolite Profiling in Genetic Resources of Garlic molecules Article Comprehensive Metabolite Profiling in Genetic Resources of Garlic (Allium sativum L.) Collected from Different Geographical Regions Mostafa Abdelrahman 1,†, Sho Hirata 2,†, Takuya Mukae 3, Tomohiro Yamada 4, Yuji Sawada 5, Magdi El-Syaed 6, Yutaka Yamada 5, Muneo Sato 5, Masami Yokota Hirai 5 and Masayoshi Shigyo 3,* 1 Botany Department, Faculty of Science, Aswan University, Aswan 81528, Egypt; [email protected] 2 Laboratory of Agroecology, Faculty of Agriculture, Kyushu University, Kasuya, Fukuoka 811-2307, Japan; [email protected] 3 Laboratory of Vegetable Crop Science, Graduate School of Sciences and Technology for Innovation, College of Agriculture, Yamaguchi University Yamaguchi City, Yamaguchi 753-8515, Japan; [email protected] 4 Allium Unit, Division of Vegetable Breeding, Institute of Vegetable and Floriculture Science, National Agriculture and Food Research Organization (NARO), 360 Kusawa, Ano, Tsu, Mie 514-2392, Japan; [email protected] 5 RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan; [email protected] (Y.S.); [email protected] (Y.Y.); [email protected] (M.S.); [email protected] (M.Y.H.) 6 Molecular Biotechnology Program, Field of Advanced Basic Sciences, Galala University, New Galala City 43511, Egypt; [email protected] Citation: Abdelrahman, M.; Hirata, * Correspondence: [email protected]; Tel.: +81-839-335-842 S.; Mukae, T.; Yamada, T.; Sawada, Y.; † These authors contributed equally to this work. El-Syaed, M.; Yamada, Y.; Sato, M.; Hirai, M.Y.; Shigyo, M. Abstract: Garlic (Allium sativum) is the second most important Allium crop that has been used as a Comprehensive Metabolite Profiling vegetable and condiment from ancient times due to its characteristic flavor and taste. Although garlic in Genetic Resources of Garlic (Allium is a sterile plant that reproduces vegetatively through cloves, garlic shows high biodiversity, as well as sativum L.) Collected from Different phenotypic plasticity and environmental adaptation capacity. To determine the possible mechanism Geographical Regions. Molecules 2021, underlying this phenomenon and to provide new genetic materials for the development of a novel 26, 1415. https://doi.org/10.3390/ garlic cultivar with useful agronomic traits, the metabolic profiles in the leaf tissue of 30 garlic molecules26051415 accessions collected from different geographical regions, with a special focus on the Asian region, Academic Editors: Ifedayo were investigated using LC/MS. In addition, the total saponin and fructan contents in the roots and Victor Ogungbe, Masayoshi Shigyo cloves of the investigated garlic accessions were also evaluated. Total saponin and fructan contents and Mostafa Abdelrahman did not separate the garlic accessions based on their geographical origin, implying that saponin and fructan contents were clone-specific and agroclimatic changes have affected the quantitative Received: 2 January 2021 and qualitative levels of saponins in garlic over a long history of cultivation. Principal component Accepted: 25 February 2021 analysis (PCA) and dendrogram clustering of the LC/MS-based metabolite profiling showed two Published: 5 March 2021 major clusters. Specifically, many Japanese and Central Asia accessions were grouped in cluster I and showed high accumulations of flavonol glucosides, alliin, and methiin. On the other hand, Publisher’s Note: MDPI stays neutral garlic accessions grouped in cluster II exhibited a high accumulation of anthocyanin glucosides with regard to jurisdictional claims in and amino acids. Although most of the accessions were not separated based on country of origin, published maps and institutional affil- the Central Asia accessions were clustered in one group, implying that these accessions exhibited iations. distinct metabolic profiles. The present study provides useful information that can be used for germplasm selection and the development of new garlic varieties with beneficial biotic and abiotic stress-adaptive traits. Copyright: © 2021 by the authors. Keywords: garlic; saponins; fructan; metabolome profiles Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons 1. Introduction Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ Garlic (Allium sativum L.) is one of the most economically important species of the 4.0/). genus Allium that has been used from ancient times as traditional medicine due to its Molecules 2021, 26, 1415. https://doi.org/10.3390/molecules26051415 https://www.mdpi.com/journal/molecules Molecules 2021, 26, 1415 2 of 14 nutritional, antimicrobial, and antioxidant properties, as well as a spice and herb to heighten the flavor of the dishes and health quotient [1–3]. The total world garlic production in 2018 was 28.5 million tonnes (MT), of which, 26.1 MT were produced in Asia, 0.86 in Europe, 0.83 MT in the Americas, and 0.73 MT in Africa [4]. Currently, numerous garlic products, including garlic powder, garlic paste, picked garlic, garlic vinegar, and garlic slices, have become available in the food markets to suit the growing demands of consumers [5]. However, the geographical origin of cultivars, cultivation methods, environmental conditions, and food processing have significant effects on the quality of garlic and garlic products, especially the contents of organosulfur compounds, amino acids, sugars, and phenolics [6–8]. For example, using a high temperature during thermal processing decreased amino acid, allicin, and moisture contents of black garlic, whereas increases in the total phenolic, reducing sugar, and organic acid contents were observed, indicating that temperature had a significant influence on the quality and flavor of black garlic [7]. The center of origin for garlic is considered to be the northwestern side of the Tien Shan Mountains in Central Asia due to the discovery of some fertile clones of a primitive garlic type in this area [9], leading to new avenues of research on garlic breeding, genetics, and physiology. Garlic has a large diploid genome (2n = 2x = 16), with an estimated haploid size of 15.9 gigabase pairs, which is ~32 times greater than the rice (Oryza sativa) genome [10]. Garlic is a usually sterile plant and does not produce fertile seeds by sexual reproduction, and thus, clonal propagation by its cloves is the main cultivation method [11,12]. Although the peculiar garlic reproduction could lead to low genetic diversity [13], garlic shows surprisingly high biodiversity, as well as phenotypic plasticity and environmental adapta- tion capacity [14,15]. For example, garlic genotypes vary considerably in their ability to produce fertile pollen, leaf number, floral scape length and inflorescences, and receptive stigmas [11,16]. The reason for this large biodiversity in garlic is not fully understood, which could be partially attributed to the large genome with many multicopy genes and du- plications, including noncoding sequences and tandem repeats that have been accumulated through the history of domestication [17–19]. Garlic cultivars vary not only in their fertility but also in their chemical composi- tions, including organosulfur compounds, saponins, phenolic compounds, and polysac- charides [4,20,21]. In general, diallyl sulfide (DAS), diallyl thiosulfonate (allicin), diallyl trisulfide (DATS), diallyl disulfide (DADS), S-allyl-cysteine (SAC), and S-allyl-cysteine sulfoxide (alliin) are the main organosulfur compounds detected in garlic [22,23]. In addi- tion, the total amount of saponin in purple garlic was almost 40 times greater than that in white garlic, and several saponin compounds were only found in purple garlic [24]. More- over, β-resorcylic acid, followed by pyrogallol, gallic acid, rutin, protocatechuic acid, and quercetin, are the major phenolic compounds detected in different garlic cultivars [25]. The characterization of garlic germplasm has been largely based on phenotypic characteristics, but these can vary under various agroclimatic conditions [26]. Although garlic is produced in a wide geographic range, there have been few studies on the chemical compounds in garlic based on the geographical origin. Therefore, the objective of this study was to inves- tigate the metabolite profiles of 30 garlic accessions collected from different geographical regions using LC/MS. In addition, the total saponin and fructan contents, as well as the morphological traits (plant height, number of leaves, leaf width, and sheath diameter), were also evaluated. This study provides in-depth insight into the metabolite richness in different garlic accessions based on the geographical distribution, which could be useful information that enables us to understand the phenotypic plasticity and environmental adaption of garlic germplasm. 2. Results 2.1. Quantitative Analysis of Saponin and Fructan Contents in the Examined Garlic Accessions Saponin contents in garlic root tissues varied between 3.36 to 32.18 mg g−1 DW, and the average was 14.49 mg g−1 DW (Table S1, In the Supplementary Material). Garlic accessions Molecules 2021, 26, 1415 3 of 14 showed considerable variations in their saponin contents, regardless of their country of origin, indicating that the production of saponins in the examined garlic accessions was not influenced by the geographical distribution (Figure1A, Table S1). For example, five accessions, namely, EGY489, JPN_Taishu-san, SYR_No.5, JPN_Kikai-onodu, and
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