Transcriptomic and Free Monoterpene Analyses of Aroma Reveal That Isopentenyl Diphosphate Isomerase Inhibits Monoterpene Biosynthesis in Grape (Vitis Vinifera L.)

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2024 Jun 24

PMID 38914931

Authors

Tianchi Chen

Tao Xu

Jinnan Wang

Tianye Zhang

Jin Yang

Lixiao Feng

Tiefeng Song

Jian Yang

Yueyan Wu

Affiliations

Soon will be listed here.

Abstract

Background: Monoterpenes are among the most important volatile aromatic compounds contributing to the flavor and aroma of grapes and wine. However, the molecular basis of monoterpene biosynthesis has not yet been fully elucidated.

Results: In our study, transcriptomics and gas chromatography-mass spectrometry (GC-MS) were used to mine candidate genes and transcription factors involved in monoterpene biosynthesis between high-monoterpene and zero-monoterpene table grape cultivars. We found that monoterpene biosynthesis was positively correlated by the expression of five genes encoding 1-deoxy-D-xylulose-5-phosphate synthase (VvDXSs), one encoding 4-hydroxy-3-methylbut-2-enyl diphosphate reductase (VvHDR), three hydroxy-3-methylglutaryl-CoA synthases (VvHMGSs) and one mevalonate kinase (VvMVK), whereas the expression of one isopentenyl diphosphate isomerase (VvIDI) and one 3-hydroxy-3-methylglutaryl-CoA reductase (VvHMGR) negatively correlated monoterpene biosynthesis. Of these genes, VvIDI was selected to validate its function in monoterpene accumulation through a transient overexpression experiment, and was shown to inhibit the biosynthesis of grape linalool and α-terpineol. Meanwhile, we found that a 64-amino acid extension sequence at the N-terminus can guide the VvIDI protein to target the chloroplast.

Conclusions: The findings of this study should help to guide future functional analysis of key genes as well as mining the potential regulatory mechanism of monoterpene biosynthesis in grapes and grape products.

Citing Articles

Transcriptomic and metabolomic study of the biosynthetic pathways of bioactive components in Amomum tsaoko fruits.

Luo D, Zhang Y, Jin L, Wu X, Yang C, Zhang T BMC Plant Biol. 2025; 25(1):212.

PMID: 39966750 PMC: 11834249. DOI: 10.1186/s12870-025-06239-w.

References

Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q . Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One. 2008; 3(4):e1994. PMC: 2291561. DOI: 10.1371/journal.pone.0001994. View

Luo J, Brotchie J, Pang M, Marriott P, Howell K, Zhang P . Free terpene evolution during the berry maturation of five Vitis vinifera L. cultivars. Food Chem. 2019; 299:125101. DOI: 10.1016/j.foodchem.2019.125101. View

Ma D, Li G, Alejos-Gonzalez F, Zhu Y, Xue Z, Wang A . Overexpression of a type-I isopentenyl pyrophosphate isomerase of Artemisia annua in the cytosol leads to high arteannuin B production and artemisinin increase. Plant J. 2017; 91(3):466-479. DOI: 10.1111/tpj.13583. View

Okada K, Kasahara H, Yamaguchi S, Kawaide H, Kamiya Y, Nojiri H . Genetic evidence for the role of isopentenyl diphosphate isomerases in the mevalonate pathway and plant development in Arabidopsis. Plant Cell Physiol. 2008; 49(4):604-16. DOI: 10.1093/pcp/pcn032. View

Igata M, Islam M, Tada A, Takagi M, Kober A, Albarracin L . Transcriptome Modifications in Porcine Adipocytes via Toll-Like Receptors Activation. Front Immunol. 2019; 10:1180. PMC: 6549529. DOI: 10.3389/fimmu.2019.01180. View

Emanuelli F, Battilana J, Costantini L, Le Cunff L, Boursiquot J, This P . A candidate gene association study on muscat flavor in grapevine (Vitis vinifera L.). BMC Plant Biol. 2010; 10:241. PMC: 3095323. DOI: 10.1186/1471-2229-10-241. View

Xu Z, Ni J, Shah F, Wang Q, Wang Z, Wu L . Transcriptome analysis of pecan seeds at different developing stages and identification of key genes involved in lipid metabolism. PLoS One. 2018; 13(4):e0195913. PMC: 5919011. DOI: 10.1371/journal.pone.0195913. View

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S . MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013; 30(12):2725-9. PMC: 3840312. DOI: 10.1093/molbev/mst197. View

Martin D, Chiang A, Lund S, Bohlmann J . Biosynthesis of wine aroma: transcript profiles of hydroxymethylbutenyl diphosphate reductase, geranyl diphosphate synthase, and linalool/nerolidol synthase parallel monoterpenol glycoside accumulation in Gewürztraminer grapes. Planta. 2012; 236(3):919-29. DOI: 10.1007/s00425-012-1704-0. View

10.

Pankratov I, McQuinn R, Schwartz J, Bar E, Fei Z, Lewinsohn E . Fruit carotenoid-deficient mutants in tomato reveal a function of the plastidial isopentenyl diphosphate isomerase (IDI1) in carotenoid biosynthesis. Plant J. 2016; 88(1):82-94. DOI: 10.1111/tpj.13232. View

11.

Bruce B . Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol. 2000; 10(10):440-7. DOI: 10.1016/s0962-8924(00)01833-x. View

12.

Morcia C, Tumino G, Raimondi S, Schneider A, Terzi V . Muscat Flavor in Grapevine: A Digital PCR Assay to Track Allelic Variation in Gene. Genes (Basel). 2021; 12(5). PMC: 8156067. DOI: 10.3390/genes12050747. View

13.

Nakamura A, Shimada H, Masuda T, Ohta H, Takamiya K . Two distinct isopentenyl diphosphate isomerases in cytosol and plastid are differentially induced by environmental stresses in tobacco. FEBS Lett. 2001; 506(1):61-4. DOI: 10.1016/s0014-5793(01)02870-8. View

14.

Tian F, Yang D, Meng Y, Jin J, Gao G . PlantRegMap: charting functional regulatory maps in plants. Nucleic Acids Res. 2019; 48(D1):D1104-D1113. PMC: 7145545. DOI: 10.1093/nar/gkz1020. View

15.

Leng X, Wang P, Wang C, Zhu X, Li X, Li H . Genome-wide identification and characterization of genes involved in carotenoid metabolic in three stages of grapevine fruit development. Sci Rep. 2017; 7(1):4216. PMC: 5484692. DOI: 10.1038/s41598-017-04004-0. View

16.

Li M, Chen R, Gu H, Cheng D, Guo X, Shi C . Grape Small Auxin Upregulated RNA () 041 Is a Candidate Regulator of Berry Size in Grape. Int J Mol Sci. 2021; 22(21). PMC: 8584205. DOI: 10.3390/ijms222111818. View

17.

Chen C, Chen H, Zhang Y, Thomas H, Frank M, He Y . TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol Plant. 2020; 13(8):1194-1202. DOI: 10.1016/j.molp.2020.06.009. View

18.

Wang Y, Qiu C, Zhang F, Guo B, Miao Z, Sun X . Molecular cloning, expression profiling and functional analyses of a cDNA encoding isopentenyl diphosphate isomerase from Gossypium barbadense. Biosci Rep. 2008; 29(2):111-9. DOI: 10.1042/BSR20070052. View

19.

Qiu F, Wang X, Zheng Y, Wang H, Liu X, Su X . Full-Length Transcriptome Sequencing and Different Chemotype Expression Profile Analysis of Genes Related to Monoterpenoid Biosynthesis in . Int J Mol Sci. 2019; 20(24). PMC: 6941020. DOI: 10.3390/ijms20246230. View

20.

Panighel A, Flamini R . Applications of solid-phase microextraction and gas chromatography/mass spectrometry (SPME-GC/MS) in the study of grape and wine volatile compounds. Molecules. 2014; 19(12):21291-309. PMC: 6270909. DOI: 10.3390/molecules191221291. View