Skip to main content
Log in

Dynamic Changes of Transcriptome and Metabolites During Ripening of Alpinia Oxyphylla Fruit (AOF)

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Alpinia oxyphylla (Yizhi) is an economically valuable plant, not only used as edible fruit, but also as an important traditional medicinal material. However, there are few studies on fruit development and metabolic pathways. To elucidate the dynamic changes of metabolites and transcription levels during fruit development of A. oxyphylla, the four parts of A. oxyphylla fruit from different periods, including early fruit (EF), middle fruit (MF), late pericarp (LP) and late seed (LS) were collected. KEGG pathway analysis shows that DEGs in EF, MF, LP are involved in amino sugar and nucleotide sugar metabolism, starch and sucrose metabolism, and plant hormone signal transduction. However, at the late part of fruit development (LS), most of the DEGs between LS and LP were enriched in pyruvate metabolism, glycolysis/gluconeogenesis, tryptophan metabolism. We found that in the early and middle parts of fruit development (EF, MF), many differential metabolites were enriched in piperidine tropane and biosynthesis of secondary metabolites, pyridine alkaloid biosynthesis. In addition, important active components, such as nootkatone in A. oxyphylla fruits accumulated in the LS part, but did not show significant differences in the first three parts. Some key transcription factors that are significantly positively correlated with the maturation of AOF have also been identified. Together, our research provides new insights into the accumulation of metabolites and the dynamic changes of the transcriptome during fruit development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barri T, Dragsted LO (2013) UPLC-ESI-QTOF/MS and multivariate data analysis for blood plasma and serum metabolomics: effect of experimental artefacts and anticoagulant. Anal Chim Acta 768:118–128

    Article  CAS  PubMed  Google Scholar 

  • Chang YM, Chang HH, Wei-Wen K, Lin HJ, Yu-Lan Y, Vijaya PV, Chin-Chuan T, Chen RJ, Chang HN, Huang CY (2016) Anti-apoptotic and pro-survival effect of Alpinate Oxyphyllae Fructus (AOF) in a d-galactose-induced aging heart. Int J Mol Sci 17:466

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen X, Mao X, Huang J, Yang D, Wu J, Dong S, Lei K, Ge G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:316–322

    Article  Google Scholar 

  • Chen F, Li HL, Tan YF, Li YH, Lai WY, Guan WW, Zhang JQ, Zhao YS, Qin ZM (2014) Identification of known chemicals and their metabolites from Alpinia oxyphylla fruit extract in rat plasma using liquid chromatography/tandem mass spectrometry (LC-MS/MS) with selected reaction monitoring. J Pharm Biomed Anal 97:166–177

    Article  CAS  PubMed  Google Scholar 

  • Douglas CJ, Ellard M, Hauffe KD, Molitor E, Sá M, Reinold S, Subramaniam R, Williams F (1992) General phenylpropanoid metabolism: regulation by environmental and developmental signals. Springer, US

    Google Scholar 

  • Feng C, Li HL, Tan YF, Guan WW, Zhang JQ, Li YH, Zhao YS, Qin ZM (2014) Different accumulation profiles of multiple components between pericarp and seed of Alpinia oxyphylla capsular fruit as determined by UFLC-MS/MS. Molecules (basel, Switzerland) 19:4510

    Article  Google Scholar 

  • Geo P, Huang X, Liang F, Valentin A, Razvan S, Svetlana K, Yuandan L, Joseph W, Foo C, Babak P (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652

    Article  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang KK, Lin MN, Hsu YL, Lu IH, Pan IH, Yang JL (2019) Alpinia oxyphylla fruit extract ameliorates experimental autoimmune encephalomyelitis through the regulation of Th1/Th17 Cells. Evid Based Complem Alternat Mede 2019:1–15

    CAS  Google Scholar 

  • Jiang J, Ma S, Ye N, Ming J, Zhang J (2016) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59:86

    Article  CAS  Google Scholar 

  • Jie L, Wen-Hui W, Han-Shen Z, Lu-Yao L, Yu-Ting LU (2010) Study on chemical constituents of volatile oil from leaves and flowers of Dimocarpus longan Lour. in Guangxi by GC-MS. Chinese J Experim Tradit Med Formul

  • Lei H, Ding G, Guo B, Huang W, Zhang X, Sun Z, Shi X (2015) New Sesquiterpenoids and a Diterpenoid from Alpinia oxyphylla. Molecules 20:1551–1559

    Article  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323. BMC Bioinformat 12:93–99

    Article  CAS  Google Scholar 

  • Li YH, Feng C, Wang JF, Wang Y, Guo T (2013) Analysis of nine compounds from Alpinia oxyphylla fruit at different harvest time using UFLC-MS/MS and an extraction method optimized by orthogonal design. Chem Cent J 7:134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YH, Tan YF, Cai HD, Zhang JQ (2016) Metabonomic study of the fruits of Alpinia oxyphylla as an effective treatment for chronic renal injury in rats. J Pharmac Biomed Analysis 124:236–245

    Article  CAS  Google Scholar 

  • Megan JB, Wonkeun P, Philip JB, Joshua AU, Justin TP, Joshua R, Brian ES, Don CJ, Tc B (2013) KEGG pathway visualization of starch and sucrose associated differentially expressed transcripts

  • Na YJ, Lee PJ, Roh JD (2017) Anti-inflammatory and anti-oxidative effects of alpiniae oxyphyllae fructus hot aqueous extract in lipopolysaccharide (LPS)-stimulated macrophages. The Acupuncture 34:83–91

    Article  Google Scholar 

  • Park SY (2015) The relaxation effects of alpiniae oxyphyllae fructus on isolated corpus cavernosum smooth muscle. Korea J Herbol 30:71–79

    Article  Google Scholar 

  • Lin Q, Wang C, Dong W, Jiang Q, Wang D (2015) Transcriptome and metabolome analyses of sugar and organic acid metabolism in Ponkan (Citrus reticulata) fruit during fruit maturation. Gene. https://doi.org/10.1016/j.gene.2014.10.025

    Article  PubMed  Google Scholar 

  • Smith LR, Mahoney N, Molyneux RJ (2003) Synthesis and structure-phytotoxicity relationships of acetylenic phenols and chromene metabolites, and their analogues, from the grapevine pathogen Eutypa lata. J Nat Prod 66:169–176

    Article  CAS  PubMed  Google Scholar 

  • Wen Q, Li HL, Tan YF, Zhang XG, Qin ZM, Li W, Li YH, Zhang JQ, Chen F (2016) LC-MS/MS-based method for simultaneous quantification of known chemicals and metabolites of Alpiniae oxyphyllae Fructus extract in rat plasma and its application in a pharmacokinetic study. Analyt Methods. https://doi.org/10.1039/C5AY03389F

    Article  Google Scholar 

  • Wen-Bing LI, Chang-Jiang HU, Shan-Shan WU, Gao Y, Ling-Ying YU (2013) Study on urine reduction of fructus alpiniae oxyphyllae stir-frying with salt water in water-loading diuresis model rats. Chinese J Experim Tradition Med Formulae

  • Young M, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14–R14

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu C, Zhao X, Qi G, Bai Z, Yu W (2017) Integrated analysis of transcriptome and metabolites reveals an essential role of metabolic flux in starch accumulation under nitrogen starvation in duckweed. Biotechnol Biofuels. https://doi.org/10.1186/s13068-017-0851-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan M, Breitkopf SB, Yang X, Asara JM (2012) A positive/negative ion–switching, targeted mass spectrometry–based metabolomics platform for bodily fluids, cells, and fresh and fixed tissue. Nat Protoc 7:872–881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Zheng Y, Hu X, Hu X, Lv W, Lv D, Chen J, Wu M, Song Q, Shentu J (2018) Ethnopharmacological uses, phytochemistry, biological activities, and therapeutic applications of Alpinia oxyphylla Miquel: A review. J Ethnopharmacol. https://doi.org/10.1016/j.jep.2018.05.002

    Article  PubMed  Google Scholar 

  • Zhang S, Zhang A, Wu X, Zhu Z, Yang Z, Zhu Y, Zha D (2019) Transcriptome analysis revealed expression of genes related to anthocyanin biosynthesis in eggplant (Solanum melongena L.) under high-temperature stress. BMC Plant Biol 19:387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao C, Hua LN, Liu XF, Li YZ, Guo JX (2016) Sucrose synthase FaSS1 plays an important role in the regulation of strawberry fruit ripening. Plant Growth Regul 81:1–7

    Google Scholar 

  • Zhou D, Fu Y, Lai W, Zhang J (2016) Determination of heavy metals in Alpinia oxyphylla Miq. collected from different cultivation regions. J Anal Methods Chem 2016:1–6

    Article  CAS  Google Scholar 

  • Zhu M, Chen G, Shuang Z, Yun T, Wang Y, Dong T, Hu Z (2014) A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol 55:119–135

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

He authors acknowledgements the support from National Natural Science Foundation of China (No. 81660629 and No. 81560611).

Author information

Authors and Affiliations

Authors

Contributions

KP and BG designed the study, XY and SW collect samples needed for sequencing, JH and YL analyzed the transcriptome and metabolome dates, KP wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Bingmiao Gao.

Ethics declarations

Conflict of interest

The authors declare that have no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

12374_2022_9354_MOESM1_ESM.tif

Supplementary file1 (TIF 178290 KB) Figure S1 Analysis of GO enrichment of DEGs between four different developmental stages of AOF. BP: biological process, CC: cellular component, MF: molecular function

12374_2022_9354_MOESM2_ESM.tif

Supplementary file2 (TIF 66113 KB) Figure S2 KEGG pathway enrichment analysis of the annotated DEGs. The Y-axis indicates the KEGG pathway, the X-axis indicates the rich factor. The dot size indicates the number of DEGs of the pathway, and the dot colour indicates the q value

12374_2022_9354_MOESM3_ESM.tif

Supplementary file3 (TIF 138974 KB) Figure S3 Enrichment analysis of KEGG pathway of differential metabolites in different developmental stages of AOF

Supplementary file4 (TIF 27025 KB) Figure S4 qRT-PCR results of 10 genes

Supplementary file5 (DOCX 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pan, K., Yu, X., Wang, S. et al. Dynamic Changes of Transcriptome and Metabolites During Ripening of Alpinia Oxyphylla Fruit (AOF). J. Plant Biol. 65, 445–457 (2022). https://doi.org/10.1007/s12374-022-09354-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-022-09354-5

Keywords

Navigation