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Comparative Analysis of Flavonoid Metabolites in Foxtail Millet (Setaria Italica) with Different Eating Quality

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Comparative Analysis of Flavonoid Metabolites in Foxtail Millet (Setaria Italica) with Different Eating Quality life Article Comparative Analysis of Flavonoid Metabolites in Foxtail Millet (Setaria italica) with Different Eating Quality Yakun Zhang 1,†, Jianhua Gao 2,†, Qianru Qie 1, Yulu Yang 1, Siyu Hou 1, Xingchun Wang 2, Xukai Li 2,* and Yuanhuai Han 1,* 1 College of Agriculture, Shanxi Agricultural University, Jinzhong 030801, China; [email protected] (Y.Z.); [email protected] (Q.Q.); [email protected] (Y.Y.); [email protected] (S.H.) 2 College of Life Sciences, Shanxi Agricultural University, Jinzhong 030801, China; [email protected] (J.G.); [email protected] (X.W.) * Correspondence: [email protected] (X.L.); [email protected] (Y.H.) † These authors contributed equally to the paper. Abstract: Foxtail millet (Setaria italica) is an important minor cereal crop in China. The yellow color of the de-husked grain is the most direct aspect for evaluating the foxtail millet quality. The yellow pigment mainly includes carotenoids (lutein and zeaxanthin) and flavonoids. To reveal the diversity and specificity of flavonoids in foxtail millet, we chose three high eating quality and two poor eating quality varieties as research materials. A total of 116 flavonoid metabolites were identified based on Ultra Performance Liquid Chromatography-Electrospray Ionization-Tandem Mass Spectrometry (UPLC-ESI-MS/MS) system. The tested varieties contained similar levels of flavonoid metabolites, but with each variety accumulating its unique flavonoid metabolites. A total of 33 flavonoid metabolites were identified as significantly discrepant between high eating quality and poor eating quality varieties, which were mainly in the flavonoid biosynthesis pathway and one Citation: Zhang, Y.; Gao, J.; Qie, Q.; of its branches, the flavone and flavonol biosynthesis pathway. These results showed the diversified Yang, Y.; Hou, S.; Wang, X.; Li, X.; components of flavonoids accumulated in foxtail millets and laid the foundation for further research Han, Y. Comparative Analysis of on flavonoids and the breeding for high-quality foxtail millet varieties. Flavonoid Metabolites in Foxtail Millet (Setaria italica) with Different Keywords: foxtail millet; flavonoid metabolome; functional components; UPLC-ESI-MS/MS Eating Quality. Life 2021, 11, 578. https://doi.org/10.3390/life11060578 Academic Editor: Stefania Lamponi 1. Introduction Foxtail millet (Setaria italica (L.) P. Beauv), a member of the family of Poaceae, origi- Received: 25 May 2021 nated in the Yellow River basin in China more than 11,000 years ago [1]. Foxtail millet Accepted: 15 June 2021 plays a nutritional and functional role in the diet for many people [2]. It is nutritionally Published: 18 June 2021 comparable to some other major cereals. For example, it has a higher content of protein, lipids, and lower carbohydrate content than some cereals (wheat and maize) [3]. Compared Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in with rice, foxtail millet has double protein content, fourfold minerals and fat, and triple published maps and institutional affil- calcium [4]. Ample evidence showed that increasing the consumption of foxtail millet was iations. associated with a lower risk of diabetes [5]. Therefore, foxtail millet is gaining increasing attention among consumers. Generally, the yellow color of the de-husked grain is the most direct indicator for consumers to evaluate the millet quality. Many compounds, including carotenoids (lutein and zeaxanthin), flavonoids, are predominant yellow pigments in plants and are believed to confer nutritional and pharmacological benefits to plants. There have Copyright: © 2021 by the authors. been preliminary studies on carotenoids in foxtail millet [6,7]. However, a systematic Licensee MDPI, Basel, Switzerland. This article is an open access article understanding of flavonoid diversity in foxtail millet is still lacking. distributed under the terms and Foxtail millets are rich in flavonoids [8,9], a large group of natural products with conditions of the Creative Commons variable phenolic structures, containing flavone, flavanone, flavonols, isoflavone, antho- Attribution (CC BY) license (https:// cyanins, and so on. Flavonoids play essential roles in plants in forming the color and creativecommons.org/licenses/by/ flavor of flowers and fruits, and resistance against ultraviolet B (UV-B), diseases, and pests 4.0/). Life 2021, 11, 578. https://doi.org/10.3390/life11060578 https://www.mdpi.com/journal/life Life 2021, 11, 578 2 of 14 damages [10–12]. For example, the accumulation of flavonoids led to the deep yellow col- oration of red Chinese pears after methyl jasmonate (MeJA) treatment. It also affected the appearance of radishes with multiple colors [13,14]. Furthermore, flavonoids have potential benefits for human health, including antioxidation, anti-inflammatory, anti-cholinesterase, anticancer and heart diseases, and countering antibiotic resistance [15–17]. The flavonoid biosynthesis pathway has been well understood in Arabidopsis thaliana, Zea mays, and Petunia hybrida, providing a basis for studying flavonoids in foxtail millet [18,19]. Metabolomics has been introduced as a novel technology to analyze the microbial, plant, and animal metabolomes and is considered the bridge linking the genomes and the phenotypes [20]. The high sensitivity and fast scanning speed make ultra-performance liquid chromatography-tandem mass spectrometry (UPLC-MS/MS) a preferred method of component analysis, in which the multiple reaction monitoring (MRM) mode in triple quadrupole mass spectrometry (UPLC-QQQ-MS/MS) is often used to eliminate the in- fluence of matrix effects in quantitative analyses [21]. Various metabolites and the corre- sponding genetic characteristics in plants have been identified based on this metabolic path-based approach, such as the identification of glucosides in Arabidopsis leaves [22], the synthesis and regulation of flavonoids in rice [23], and the comparison of metabolism substances in plants [24]. This study aimed to characterize flavonoid metabolites in foxtail millets and explore the diversity of flavonoid metabolites among different varieties using UPLC-ESI-MS/MS. It is expected that our work could provide a basis for further understanding of the quality of foxtail millet and pave the way for the breeding of better varieties with high flavonoids. 2. Materials and Methods 2.1. Plant Materials Five foxtail millet varieties were selected as experimental materials, which were “Jingu21” (JG21), “Qinzhouhuang” (QZH), “Yugu1” (YG1), “Daobaqi” (DBQ) and “Niu- maobai” (NMB). JG21 is an elite variety from Shanxi province with excellent quality and the largest growing area in China. QZH is another outstanding variety bred from an elite landrace that originated from Qinxian County in Shanxi province. YG1 is an elite variety originating from Henan province in China, the most influential species in North China, and has a high-quality reference genome sequence [25]. Both DBQ and NMB are landrace with poor eating quality. All the foxtail millet varieties were planted in the experimental field of Shanxi Agricultural University (37.42 N, 112.59 E), Taigu, China, in May 2018 and harvested in October 2018 at full maturity. The region has a semiarid climate, with an average annual temperature of 11.91 ◦C and annual precipitation of 396.24 mm in 2018. 2.2. Photo Recording and Color Determination The husk of foxtail millet seeds was removed using small hulling separators. For each variety, we selected well-developed grains for the experiments. The de-husked millets were put into containers for taking photos. The colors of these millets were measured by a colorimeter (X-Rite VS450, Big Rapids, Michigan, USA). After determining the color, the freeze-dried seed was crushed using a mixer mill (Retsch MM400, Dusseldorf, North Rhine-Westphalia, Germany) with a zirconia bead for 1.5 min at 30 Hz. The powder was also photographed, and its color was measured. Three replicates were carried out. The values of color parameters “L,” “a,” and “b,” which represent the luminosity, redness, and yellowness, respectively, were collected. The color contribution index (CCI) values were calculated according to CCI = 1000 × a/(L × b) [26]. 2.3. Preparation and Extraction of Samples for Metabolomics Analysis The preparation and extraction of samples were performed as previously described [27]. One hundred mg foxtail millet powder was weighed and extracted overnight at 4 ◦C with 1.0 mL 70% aqueous methanol (including 0.1 mg/L lidocaine or 0.1 mg/L acyclovir) to ensure sufficient reaction. After that, the samples were centrifuged at 4 ◦C and 14,000 r Life 2021, 11, 578 3 of 14 for 5 min. The supernatant was collected and centrifuged again. Then, the water-soluble extracts were absorbed on a CNWBOND Carbon-GCB SPE Cartridge (ANPEL, Shanghai, China) and filtrated with SCAA-104 (ANPEL, 0.22 µm pore size, Shanghai, China), for standby application. 2.4. Ultra-High-Performance Liquid Chromatography (UPLC) Conditions The extracted samples were analyzed as described by Wang et al. [28]. A UPLC-ESI- MS/MS system (UPLC, Shim-pack UFLC SHIMADZU CBM30A system; MS, Applied Biosystems 6500 Q TRAP, Foster City, USA) equipped with a C18 chromatographic column (Waters ACQUITY UPLC HSS T3, 2.1 mm × 100 mm, 1.8 µm) was used for the analysis. The solvent systems contained mobile phase A (0.04% acetic acid in water) and mobile phase B (0.04% acetic acid in acetonitrile). The gradient program (Mobile phase A: Mobile phase B) was performed as follows: 95:5 (v/v) at 0 min, 5:95 (v/v) at 11.0 min, 5:95 (v/v) at 12.0 min, 95:5 (v/v) at 12.1 min, and 95:5 (v/v) at 15.0 min; flow rate 0.40 mL/min. The column temperature was kept at 40 ◦C, and the injection volume was set to 2 µL. The UPLC effluent was input into an ESI-triple quadrupole-linear ion trap (Q TRAP)-MS and analyzed further. 2.5. Electrospray-Triple Quadrupole-Linear Ion Trap Mass Spectrometry (ESI-Q TRAP-MS/MS) System The mass spectrometry (MS) followed the method described by Chen et al.
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