Peroxisomal Localisation of the Final Steps of the Mevalonic Acid Pathway in Planta

Overview

Journal Planta

Specialty Biology

Date 2011 Jun 10

PMID 21655959

Citations 54

Authors

Andrew J Simkin

Gregory Guirimand

Nicolas Papon

Vincent Courdavault

Insaf Thabet

Olivia Ginis

Sadok Bouzid

Nathalie Giglioli-Guivarch

Marc Clastre

Affiliations

Soon will be listed here.

Abstract

In plants, the mevalonic acid (MVA) pathway provides precursors for the formation of triterpenes, sesquiterpenes, phytosterols and primary metabolites important for cell integrity. Here, we have cloned the cDNA encoding enzymes catalysing the final three steps of the MVA pathway from Madagascar periwinkle (Catharanthus roseus), mevalonate kinase (MVK), 5-phosphomevalonate kinase (PMK) and mevalonate 5-diphosphate decarboxylase (MVD). These cDNA were shown to functionally complement MVA pathway deletion mutants in the yeast Saccharomyces cerevisiae. Transient transformations of C. roseus cells with yellow fluorescent protein (YFP)-fused constructs reveal that PMK and MVD are localised to the peroxisomes, while MVK was cytosolic. These compartmentalisation results were confirmed using the Arabidopsis thaliana MVK, PMK and MVD sequences fused to YFP. Based on these observations and the arguments raised here we conclude that the final steps of the plant MVA pathway are localised to the peroxisome.

Citing Articles

Expression Analysis and Functional Validation of DcTPSb1 in Terpene Synthesis of .

Jin Y, Zhou S, Du Z, Wang W, Chen Z Curr Issues Mol Biol. 2025; 47(1).

PMID: 39852140 PMC: 11763578. DOI: 10.3390/cimb47010025.

The interaction networks of small rubber particle proteins in the latex of reveal diverse functions in stress responses and secondary metabolism.

Wolters S, Laibach N, Riekotter J, Roelfs K, Muller B, Eirich J Front Plant Sci. 2024; 15:1498737.

PMID: 39735776 PMC: 11671276. DOI: 10.3389/fpls.2024.1498737.

Metabolic engineering of terpene metabolism in lavender.

Oseni O, Sajaditabar R, Mahmoud S Beni Suef Univ J Basic Appl Sci. 2024; 13(1):67.

PMID: 38988370 PMC: 11230991. DOI: 10.1186/s43088-024-00524-7.

The synthesis of papaya fruit flavor-related linalool was regulated by CpTPS18 and CpNAC56.

Yao Y, Fu W, Yu Y, Wan S, Zhang W, Ming R Plant Reprod. 2023; 37(3):295-308.

PMID: 37966580 DOI: 10.1007/s00497-023-00486-3.

Aromatic Terpenes and Their Biosynthesis in , and Conjecture on the Botanical Perfumer Mechanism.

Du Z, Yang X, Zhou S, Jin Y, Wang W, Xia K Curr Issues Mol Biol. 2023; 45(7):5305-5316.

PMID: 37504253 PMC: 10378317. DOI: 10.3390/cimb45070337.

References

Nelson B, Cai X, Nebenfuhr A . A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 2007; 51(6):1126-36. DOI: 10.1111/j.1365-313X.2007.03212.x. View

Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K, Holbrook D . In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol. 2009; 150(1):125-43. PMC: 2675712. DOI: 10.1104/pp.109.137703. View

van der Heijden R, Jacobs D, Snoeijer W, Hallard D, Verpoorte R . The Catharanthus alkaloids: pharmacognosy and biotechnology. Curr Med Chem. 2004; 11(5):607-28. DOI: 10.2174/0929867043455846. View

Hogenboom S, Tuyp J, Espeel M, Koster J, Wanders R, Waterham H . Phosphomevalonate kinase is a cytosolic protein in humans. J Lipid Res. 2004; 45(4):697-705. DOI: 10.1194/jlr.M300373-JLR200. View

Reumann S . Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol. 2004; 135(2):783-800. PMC: 514115. DOI: 10.1104/pp.103.035584. View

Hogenboom S, Tuyp J, Espeel M, Koster J, Wanders R, Waterham H . Mevalonate kinase is a cytosolic enzyme in humans. J Cell Sci. 2004; 117(Pt 4):631-9. DOI: 10.1242/jcs.00910. View

Rodriguez-Concepcion M, Boronat A . Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 2002; 130(3):1079-89. PMC: 1540259. DOI: 10.1104/pp.007138. View

Hemmerlin A, Hoeffler J, Meyer O, Tritsch D, Kagan I, Grosdemange-Billiard C . Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J Biol Chem. 2003; 278(29):26666-76. DOI: 10.1074/jbc.M302526200. View

Olivier L, Kovacs W, Masuda K, Keller G, Krisans S . Identification of peroxisomal targeting signals in cholesterol biosynthetic enzymes. AA-CoA thiolase, hmg-coa synthase, MPPD, and FPP synthase. J Lipid Res. 2000; 41(12):1921-35. View

10.

Dewick P . The biosynthesis of C5-C25 terpenoid compounds. Nat Prod Rep. 2002; 19(2):181-222. DOI: 10.1039/b002685i. View

11.

Sando T, Takaoka C, Mukai Y, Yamashita A, Hattori M, Ogasawara N . Cloning and characterization of mevalonate pathway genes in a natural rubber producing plant, Hevea brasiliensis. Biosci Biotechnol Biochem. 2008; 72(8):2049-60. DOI: 10.1271/bbb.80165. View

12.

Cordier H, Karst F, Berges T . Heterologous expression in Saccharomyces cerevisiae of an Arabidopsis thaliana cDNA encoding mevalonate diphosphate decarboxylase. Plant Mol Biol. 1999; 39(5):953-67. DOI: 10.1023/a:1006181720100. View

13.

Tian G, Mohanty A, Chary S, Li S, Paap B, Drakakaki G . High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol. 2004; 135(1):25-38. PMC: 429330. DOI: 10.1104/pp.104.040139. View

14.

Schrader M, Fahimi H . The peroxisome: still a mysterious organelle. Histochem Cell Biol. 2008; 129(4):421-40. PMC: 2668598. DOI: 10.1007/s00418-008-0396-9. View

15.

Hsieh M, Chang C, Hsu S, Chen J . Chloroplast localization of methylerythritol 4-phosphate pathway enzymes and regulation of mitochondrial genes in ispD and ispE albino mutants in Arabidopsis. Plant Mol Biol. 2008; 66(6):663-73. DOI: 10.1007/s11103-008-9297-5. View

16.

Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli G . Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell. 2007; 19(10):3170-93. PMC: 2174697. DOI: 10.1105/tpc.107.050989. View

17.

Hayashi H, De Bellis L, Hayashi Y, Nito K, Kato A, Hayashi M . Molecular characterization of an Arabidopsis acyl-coenzyme a synthetase localized on glyoxysomal membranes. Plant Physiol. 2002; 130(4):2019-26. PMC: 166713. DOI: 10.1104/pp.012955. View

18.

Luo B, Norris C, Bolstad E, Knecht D, Grant D . Protein quaternary structure and expression levels contribute to peroxisomal-targeting-sequence-1-mediated peroxisomal import of human soluble epoxide hydrolase. J Mol Biol. 2008; 380(1):31-41. PMC: 2515390. DOI: 10.1016/j.jmb.2008.04.064. View

19.

Pan X, Yuan D, Xiang D, Wang X, Sookhai-Mahadeo S, Bader J . A robust toolkit for functional profiling of the yeast genome. Mol Cell. 2004; 16(3):487-96. DOI: 10.1016/j.molcel.2004.09.035. View

20.

Lamberto I, Percudani R, Gatti R, Folli C, Petrucco S . Conserved alternative splicing of Arabidopsis transthyretin-like determines protein localization and S-allantoin synthesis in peroxisomes. Plant Cell. 2010; 22(5):1564-74. PMC: 2899872. DOI: 10.1105/tpc.109.070102. View