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Integrated Metabolomics and Transcriptome Analyses Unveil Pathways Involved in Sugar Content and Rind Color of Two Sugarcane Varieties.

ABSTRACT: Metabolic composition can have potential impact on several vital agronomic traits, and metabolomics, which represents the bioactive compounds in plant tissues, is widely considered as a powerful approach for linking phenotype-genotype interactions. However, metabolites related to cane traits such as sugar content, rind color, and texture differences in different sugarcane cultivars using metabolome integrated with transcriptome remain largely inconclusive. In this study, metabolome integrated with transcriptome analyses were performed to identify and quantify metabolites composition, and have better insight into the molecular mechanisms underpinning the different cane traits, namely, brix, rind color, and textures in the stems (S) and leaves (L) of sugarcane varieties FN41 and 165402. We also identified metabolites and associated genes in the phenylpropanoid and flavonoid biosynthesis pathways, starch and sucrose metabolism. A total of 512 metabolites from 11 classes, with the vast majority (122) belonging to flavonoids were identified. Moreover, the relatively high amount of D-fructose 6-p, D-glucose6-p and glucose1-p detected in FN41L may have been transported and distributed by source and sink of the cane, and a majority of them reached the stem of sugarcane FN41L, thereby promoting the high accumulation of sugar in FN41S. Observations also revealed that genes such as C4H, CHS, F3H, F3'H, DFR, and FG2 in phenylpropanoid and flavonoid biosynthesis pathways were the major factors impacting the rind color and contrasting texture of FN41 and 165204. Further analysis revealed that weighted gene co-expression network analysis (WGCNA) hub genes and six transcription factors, namely, Tify and NAC, MYB-related, C2C2-Dof, WRKY, and bHLH play a key role in phenylpropanoid biosynthesis, flavone and flavonol biosynthesis, starch and sucrose metabolism. Additionally, metabolites such as L-phenylalanine, tyrosine, sinapaldehyde, pinobanksin, kaempferin, and nictoflorin were the potential drivers of phenotypic differences. Our finding also demonstrated that genes and metabolites in the starch and sucrose metabolism had a significant effect on cane sugar content. Overall, this study provided valuable insight into the molecular mechanisms underpinning high sugar accumulation and rind color in sugarcane, which we believe is important for future sugarcane breeding programs and the selection of high biomass varieties.

SUBMITTER: Yuan Z

PROVIDER: S-EPMC9244704 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundSugarcane (Saccharum officinarum) is one of the most valuable feedstocks for sugar production. In addition to the production of industrial raw materials such as alcohol, papermaking, the fiber of livestock feed, respectively, sugarcane can produce bioactive compounds such as anthocyanins. Elucidation of the anthocyanin biosynthesis pathway is critical for the molecular breeding of sugarcane varieties with favorable traits. We aimed to identify candidate genes involved in anthocyanin biosynthesis by transcriptomic and metabolomic analyses.ResultsThree varieties of sugarcane displaying different colors were used in this study: FN15 (greed rind), ROC22 (red rind), and Badila (purple rind). Sample materials were subjected to metabolomic analysis using UPLC-Q-TOF/MS and RNA-seq analysis. The metabolomic profiling results showed Cyanidin, Cyanidin (6'-malonylglucoside), Cyanidin O-glucoside, and Peonidin O-glucoside were the main components responsible for the rind color. Then, through RNA-seq analysis, we identified a total of 3137, 3302, 3014 differentially expressed genes (DEGs) between the rind and pith tissues for the corresponding varieties Badila rind, ROC22, and FN15. We then compared the expression levels of genes among the rind tissues from the three varieties. We identified 2901, 2821, and 3071 DEGs between Badila rind vs. ROC22 rind, Badila rind vs. FN15 rind, ROC22 rind vs. FN15 rind, respectively. We identified two enriched pathways, including phenylpropanoid biosynthesis and flavonoid biosynthesis. Sequencing similarity search identified a total of 50 unigenes belonging to 15 enzyme families as putative genes involved in anthocyanin biosynthesis in sugarcane rind. Seven of them were identified as candidate genes related to anthocyanin biosynthesis in the rind of sugarcane through co-localization analysis with the anthocyanin content in sugarcane. In total, 25 unigenes were selected and subjected to RT-qPCR analysis, and qRT-PCR results were consistent with those obtained with the RNA-Seq experiments.ConclusionsWe proposed a pathway for anthocyanin biosynthesis in sugarcane rind. This is the first report on the biosynthesis of anthocyanin in sugarcane using the combined transcriptomic and metabolomic methods. The results obtained from this study will lay the foundation for breeding purple pith sugarcane varieties with high anthocyanin contents.

Project description:Sugarcane is a major crop of the tropics cultivated mainly for its high sucrose content. The crop is genetically less explored due to its complex polyploid genome. Sucrose synthesis and accumulation are complex processes influenced by physiological, biochemical and genetic factors, and the growth environment. The recent focus on the crop for fibre and biofuel has led to a renewed interest on understanding the molecular basis of sucrose and biomass traits. This transcriptome study aimed to identify genes that are associated with and differentially regulated during sucrose synthesis and accumulation in the mature stage of sugarcane. Patterns of gene expression in high and low sugar genotypes as well as mature and immature culm tissues were studied using RNA-Seq of culm transcriptomes.In this study, 28 RNA-Seq libraries from 14 genotypes of sugarcane differing in their sucrose content were used for studying the transcriptional basis of sucrose accumulation. Differential gene expression studies were performed using SoGI (Saccharum officinarum Gene Index, 3.0), SAS (sugarcane assembled sequences) of sugarcane EST database (SUCEST) and SUGIT, a sugarcane Iso-Seq transcriptome database. In total, about 34,476 genes were found to be differentially expressed between high and low sugar genotypes with the SoGI database, 20,487 genes with the SAS database and 18,543 genes with the SUGIT database at FDR?<?0.01, using the Baggerley's test. Further, differential gene expression analyses were conducted between immature (top) and mature (bottom) tissues of the culm. The DEGs were functionally annotated using GO classification and the genes consistently associated with sucrose accumulation were identified.The large number of DEGs may be due to the large number of genes that influence sucrose content or are regulated by sucrose content. These results indicate that apart from being a primary metabolite and storage and transport sugar, sucrose may serve as a signalling molecule that regulates many aspects of growth and development in sugarcane. Further studies are needed to confirm if sucrose regulates the expression of the identified DEGs or vice versa. The DEGs identified in this study may lead to identification of genes/pathways regulating sucrose accumulation and/or regulated by sucrose levels in sugarcane. We propose identifying the master regulators of sucrose if any in the future.

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Integrated Metabolomics and Transcriptome Analyses Unveil Pathways Involved in Sugar Content and Rind Color of Two Sugarcane Varieties.

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