The subcellular localization of two isopentenyl diphosphate isomerases in rice suggests a role for the endoplasmic reticulum in isoprenoid biosynthesis.

Publisher: Springer Country of Publication: Germany NLM ID: 9880970 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-203X (Electronic) Linking ISSN: 07217714 NLM ISO Abbreviation: Plant Cell Rep Subsets: MEDLINE

Original Publication: Berlin ; New York : Springer, 1981-

Carbon-Carbon Double Bond Isomerases/*metabolism ; Endoplasmic Reticulum/*enzymology ; Hemiterpenes/*metabolism ; Oryza/*enzymology ; Terpenes/*metabolism; Carbon-Carbon Double Bond Isomerases/genetics ; Carotenoids/metabolism ; Chlorophyll/metabolism ; Endoplasmic Reticulum/metabolism ; Gene Expression Regulation, Plant ; Hemiterpenes/genetics ; Mevalonic Acid/metabolism ; Mitochondria/metabolism ; Organophosphorus Compounds/metabolism ; Oryza/genetics ; Oryza/metabolism ; Peroxisomes/metabolism ; Plant Leaves/metabolism ; Plants, Genetically Modified/cytology ; Plants, Genetically Modified/genetics ; Plants, Genetically Modified/metabolism ; Plastids/metabolism

Key Message: Both OsIPPI1 and OsIPPI2 enzymes are found in the endoplasmic reticulum, providing novel important insights into the role of this compartment in the synthesis of MVA pathway isoprenoids. Isoprenoids are synthesized from the precursor's isopentenyl diphosphate (IPP) and dimethylallyl diphosphosphate (DMAPP), which are interconverted by the enzyme isopentenyl diphosphate isomerase (IPPI). Many plants express multiple isoforms of IPPI, the only enzyme shared by the mevalonate (MVA) and non-mevalonate (MEP) pathways, but little is known about their specific roles. Rice (Oryza sativa) has two IPPI isoforms (OsIPPI1 and OsIPPI2). We, therefore, carried out a comprehensive comparison of IPPI gene expression, protein localization, and isoprenoid biosynthesis in this species. We found that OsIPPI1 mRNA was more abundant than OsIPPI2 mRNA in all tissues, and its expression in de-etiolated leaves mirrored the accumulation of phytosterols, suggesting a key role in the synthesis of MVA pathway isoprenoids. We investigated the subcellular localization of both isoforms by constitutively expressing them as fusions with synthetic green fluorescent protein. Both proteins localized to the endoplasmic reticulum (ER) as well as peroxisomes and mitochondria, whereas only OsIPPI2 was detected in plastids, due to an N-terminal transit peptide which is not present in OsIPPI1. Despite the plastidial location of OsIPPI2, the expression of OsIPPI2 mRNA did not mirror the accumulation of chlorophylls or carotenoids, indicating that OsIPPI2 may be a redundant component of the MEP pathway. The detection of both OsIPPI isoforms in the ER indicates that DMAPP can be synthesized de novo in this compartment. Our work shows that the ER plays an as yet unknown role in the synthesis of MVA-derived isoprenoids, with important implications for the metabolic engineering of isoprenoid biosynthesis in higher plants.

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31870278 National Natural Science Foundation of China; RTI2018-097613-B-I00 Ministerio de Economía y Competitividad; PGC2018-097655-B-I00 Ministerio de Economía y Competitividad; 613513 European Union Framework Program DISCO; OC-2015-1-19780 European Cooperation in Science and Technology project EUROCAROTEN; 20190201013JC the International Science & Technology Cooperation Project from Jilin Provincial Science & Technology Department, China

Keywords: Carotenoids; Dimethylallyl diphosphosphate; Endoplasmic reticulum; Gene expression; Isopentenyl diphosphate isomerase; Rice (Oryza sativa)

0 (Hemiterpenes)
0 (Organophosphorus Compounds)
0 (Terpenes)
1406-65-1 (Chlorophyll)
358-72-5 (3,3-dimethylallyl pyrophosphate)
36-88-4 (Carotenoids)
EC 5.3.3.- (Carbon-Carbon Double Bond Isomerases)
EC 5.3.3.2 (isopentenyldiphosphate delta-isomerase)
S5UOB36OCZ (Mevalonic Acid)

Date Created: 20191104 Date Completed: 20200626 Latest Revision: 20220412

20250114

10.1007/s00299-019-02479-x

31679061