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Transcriptome Analysis Reveals the Protection Mechanism Of www.nature.com/scientificreports OPEN Transcriptome analysis reveals the protection mechanism of proanthocyanidins for Saccharomyces cerevisiae during wine fermentation Jingyuan Li1, Kaili Zhu1 & Hongwei Zhao2,3* Grape-derived proanthocyanidins could act as a protector against various environmental stresses for Saccharomyces cerevisiae during wine fermentation, resulting in the increased physiological activity, fermentation efciency and improved wine quality. In order to explore the possible protection mechanism of proanthocyanidins globally, RNA-seq analysis for wine yeast AWRI R2 cultivated with 0 g/L (group A), 0.1 g/L (group B), 1.0 g/L (group C) proanthocyanidins were applied in this study. Diferentially expressed genes were enriched into six metabolic pathways including vitamin B6, thiamine, amino acids, aminoacyl-tRNA, carbohydrate and steroid based on KEGG enrichment analysis. Four key genes (SNZ2, THI6, THI21 and THI80), participated in the biosynthesis of vitamin B6 and thiamine, were up-regulated signifcantly in proanthocyanidins treated yeast cells and the gene expression levels were verifed by RT-qPCR. Yeast cells supplemented with proanthocyanidins performed increased intracellular levels of vitamin B6 and thiamine and higher cell viability compared to the control group. In addition, the composition of intracellular fatty acids showed an obvious alternation in proanthocyanidins-treated yeast cells, in which the UFAs content increased whereas the SFA content decreased. In general, we provided an indirect protection efect of proanthocyanidins on the yeast cells to alleviate environmental stresses during wine fermentation. Te widely distributed phenolic substances in wine refer to a large group of chemical compounds that impact the sensory quality of red wine, such as color, favor and astringency1. A large number of studies have shown that these phenolic substances have also biological activities of interest to the consumers, such as antioxidant prop- erties, vascular protection and immune-modulatory efects2–5. For winemaking, these phenolic compounds are mainly extracted from grape skin, seed, and stem during the maceration and fermentation process6. Oenological practices, such as fermentation temperature, maceration time, storage period and yeast strains, are believed to impact the concentration and structure of these chemical compounds7–9. As the predominant fraction, proanthocyanidins (PAs) account for more than 50% of the total wine polyphe- nols, and have several important roles in the quality of red wine, such as the perception of astringency and taste, aroma release, and color stability, throughout the entire period of fermentation and storage of wine10,11. In addition, PAs could interact with other extracted phenolic compounds and even the fermentation strains, which have been proved to be crucial for the generation of new pigments, color and astringency modifcations12,13. It has been reported that the interaction of the polysaccharides released by yeast lees with wine polyphenols dur- ing aging were crucial for sensory qualities of wines11. Te extracted polyphenols could be adsorbed by yeast cells by forming the Van der Waals bonds and H-bonds during alcoholic fermentations, which might be a reasonable explanation that the yeasts cells could contribute to the modifcation of the color of the wine13. 1College of Food Science and Engineering, Qingdao Agricultural University, Qingdao, Shandong Province, 266109, China. 2College of Marine Science and Bioengineering, Qingdao University of Science and Technology, Qingdao, Shandong Province, 266042, China. 3Shandong Provincial Key Laboratory of Biochemical Engineering, Qingdao, Shandong Province, 266042, China. *email: [email protected] SCIENTIFIC REPORTS | (2020) 10:6676 | https://doi.org/10.1038/s41598-020-63631-2 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Q20 Q30 Sample length Reads Bases (%) (%) A1 147.32 40811558 6012389770 95.73 88.78 A2 147.38 62030546 9141997823 95.75 89.47 A3 147.53 60816138 8972430801 95.93 89.89 B1 147.45 67018594 9882123005 95.88 89.72 B2 147.49 55217110 8143748191 96.01 90.04 B3 147.41 66504646 9803127605 95.89 89.78 C1 147.18 52310564 7699225784 95.85 89.70 C2 147.28 55806604 8219088002 95.85 89.69 C3 147.21 63509302 9349372301 96.02 90.10 Table 1. Quality statistics of clean sequencing data. Q20, Q30 refer to the proportion of base calls with Phred scores >20 or 30 in the total bases. Higher scores ensured the base calling accuracy and data quality. Each group has three biological replicates. Saccharomyces cerevisiae, the preferred microorganism for wine making and bioethanol production, has been exposed simultaneously and sequentially to a variety of environmental stresses during the fermentation process, including high concentration of ethanol, hyperosmotic stress, heat shock, low pH and nutrients defciency14–16. Cells viability and fermentative behavior will be negatively afected by the stresses that in turn limit the wine pro- duction and quality17. In order to carry out wine fermentation properly, yeast cells should possess the capacity of rapid stress perceptions and responses to those stress conditions without substantial viability loss14. Terefore, to solve these problems, a number of previous studies have been performed in the aspects of robust strain isolation, genetic modifcation and fermentation process control18–21. It has been reported that phenolic compounds in wine act as a structure-dependent and dose-dependent manner to afect the physiological activities and fermentation performance of yeast and bacterial cells22–24. Our previous work showed that PAs could pose obvious enhancement on the metabolism and fermentation ef- ciency, which has been elucidated from the metabolic level such as the change of glucose transport, the energy and redox homeostasis as well as the activities of rate-limiting enzymes in glycolysis24,25. However, the possible molecular mechanisms of the efects of PAs on the yeast fermentation performance have not been fully stud- ied. Next-generation sequencing technologies enables the generation of genomic resources more efcient and cost-efective26. Terefore, in this study, we employed RNA-seq as the method to fnd the diferentially expressed key genes and then performed comprehensive and comparative bioinformatics analysis to globally explore the possible protective efects of PAs on the yeast cells during wine fermentation. Results Quality evaluation of sequencing reads. Quality evaluation of sequencing reads needed to be evaluated before the following bioinformatics analysis. As shown in Table 1, a total of 524025062 clean data were generated with an average length of 147 bp. Te total raw data was deposited in NCBI Gene Expression Omnibus (GEO) public archive database and the accession number is GSE141069. Phred quality score (Q score) was used as an index for the base calling accuracy and calculated by using the FastQC sofware (v0.10.1) based on Eq. (1): =− Qphred 10log10(e) (1) About 90% of the clean reads in each sample has Phred quality score >30, indicating that the base calling accuracy for each group was 99.9% and met the requirement for the next analysis (Table 1). Te Pearson correlation coefcients R2 were calculated to assess the reproducibility of gene expression values across biological replicates, as shown in Supplementary Fig. S1 to Supplementary Fig. S3, the average correla- tion R2 across the replicates for each group (A, B, C) were 0.969, 0.967 and 0.931, respectively, indicating that there were no considerable diferences between the biological replicates and the data could be used in following analysis. Diferential gene expression analysis. To identify diferentially expressed genes, transcriptome analysis was carried out for the yeast cells supplemented with 0 g/L (group A), 0.1 g/L (group B) and 1.0 g/L (group C) PAs, respectively. As shown in Fig. 1, 389, 1737 and 1566 DEGs were identifed by comparative analysis of transcrip- tome data of group A versus group B, group A versus group C and group B versus group C, respectively, indicating that PAs pose considerable efects on the gene expression level in the yeast cells. Moreover, a dose-dependent increase of DEGs was found in the data comparison (Fig. 2). With the increase of the concentration of PAs from 0.1 g/L to 1.0 g/L in the fermentation broth, more than 4 times of DEGs were identifed in the yeast cells. A total of 48 DEGs were found in all the three comparative groups, which might be considered as the key genes related to the PAs protection mechanism. GO enrichment analysis of the DEGs. To better understand the functions of the DEGs, gene annotation including homologous protein annotation was performed by using the gene ontology (GO) database. As shown in Fig. 3, the identifed DEGs could be classifed into three categories including biological process, cellular com- ponent and molecular function. SCIENTIFIC REPORTS | (2020) 10:6676 | https://doi.org/10.1038/s41598-020-63631-2 2 www.nature.com/scientificreports/ www.nature.com/scientificreports Figure 1. Venn diagrams of transcripts in the three comparative groups marked as group A versus group B, group A versus group C and group B versus group C, respectively. Figure 2. Up or down regulated DEGs in pairwise comparisons marked as group A versus group B, group A versus group C and group B versus group C, respectively. In the cellular component category, DEGs were mainly enriched in the terms related with the structure of cell membrane and organelle; In the biological process group, metabolic process and cellular process were the impor- tant functions, especially the thiamine and cellular amino acid metabolic pathways and tRNA aminoacylation process; catalytic activity, oxidoreductase activity and binding were the three main molecular functions of the identifed DEGs. In addition, an obvious positive correlation between the number of enriched DGEs and the concentration of PAs were found in the three biological functions. Especially in the thiamine metabolic process and tRNA aminoacylation, as the concentration of PAs was increased to 1.0 g/L, more than 6 times of the numbers of DGEs were enriched compared to that in the 0.1 g/L PAs-treated group.
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