A single arabidopsis gene encodes two differentially targeted geranylgeranyl diphosphate synthase isoforms

M. Águila Ruiz-Sola, M.V. Barja, David Manzano, Briardo Llorente, Bert Schipper, Jules Beekwilder, Manuel Rodriguez-Concepcion

Research output: Contribution to journalArticleAcademicpeer-review

6 Citations (Scopus)

Abstract

A wide diversity of isoprenoids is produced in different plant compartments. Most groups of isoprenoids synthesized in plastids, and some produced elsewhere in the plant cell derive from geranylgeranyl diphosphate (GGPP) synthesized by GGPP synthase (GGPPS) enzymes. In Arabidopsis (Arabidopsis thaliana), five genes appear to encode GGPPS isoforms localized in plastids (two), the endoplasmic reticulum (two), and mitochondria (one). However, the loss of function of the plastid-targeted GGPPS11 isoform (referred to as G11) is sufficient to cause lethality. Here, we show that the absence of a strong transcription initiation site in the G11 gene results in the production of transcripts of different lengths. The longer transcripts encode an isoform with a functional plastid import sequence that produces GGPP for the major groups of photosynthesis-related plastidial isoprenoids. However, shorter transcripts are also produced that lack the first translation initiation codon and rely on a second in-frame ATG codon to produce an enzymatically active isoform lacking this N-terminal domain. This short enzyme localizes in the cytosol and is essential for embryo development. Our results confirm that the production of differentially targeted enzyme isoforms from the same gene is a central mechanism to control the biosynthesis of isoprenoid precursors in different plant cell compartments.

LanguageEnglish
Pages1393-1402
JournalPlant Physiology
Volume172
Issue number3
DOIs
Publication statusPublished - 2016

Fingerprint

Farnesyltranstransferase
isoprenoids
Arabidopsis
Plastids
plastids
Terpenes
Protein Isoforms
Genes
Plant Cells
genes
enzymes
Enzymes
start codon
cytosol
codons
endoplasmic reticulum
Initiator Codon
imports
translation (genetics)
Transcription Initiation Site

Cite this

Águila Ruiz-Sola, M. ; Barja, M.V. ; Manzano, David ; Llorente, Briardo ; Schipper, Bert ; Beekwilder, Jules ; Rodriguez-Concepcion, Manuel. / A single arabidopsis gene encodes two differentially targeted geranylgeranyl diphosphate synthase isoforms. In: Plant Physiology. 2016 ; Vol. 172, No. 3. pp. 1393-1402.
@article{2c0d93198d58453cbc1b484534307e9b,
title = "A single arabidopsis gene encodes two differentially targeted geranylgeranyl diphosphate synthase isoforms",
abstract = "A wide diversity of isoprenoids is produced in different plant compartments. Most groups of isoprenoids synthesized in plastids, and some produced elsewhere in the plant cell derive from geranylgeranyl diphosphate (GGPP) synthesized by GGPP synthase (GGPPS) enzymes. In Arabidopsis (Arabidopsis thaliana), five genes appear to encode GGPPS isoforms localized in plastids (two), the endoplasmic reticulum (two), and mitochondria (one). However, the loss of function of the plastid-targeted GGPPS11 isoform (referred to as G11) is sufficient to cause lethality. Here, we show that the absence of a strong transcription initiation site in the G11 gene results in the production of transcripts of different lengths. The longer transcripts encode an isoform with a functional plastid import sequence that produces GGPP for the major groups of photosynthesis-related plastidial isoprenoids. However, shorter transcripts are also produced that lack the first translation initiation codon and rely on a second in-frame ATG codon to produce an enzymatically active isoform lacking this N-terminal domain. This short enzyme localizes in the cytosol and is essential for embryo development. Our results confirm that the production of differentially targeted enzyme isoforms from the same gene is a central mechanism to control the biosynthesis of isoprenoid precursors in different plant cell compartments.",
author = "{{\'A}guila Ruiz-Sola}, M. and M.V. Barja and David Manzano and Briardo Llorente and Bert Schipper and Jules Beekwilder and Manuel Rodriguez-Concepcion",
year = "2016",
doi = "10.1104/pp.16.01392",
language = "English",
volume = "172",
pages = "1393--1402",
journal = "Plant Physiology",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "3",

}

Águila Ruiz-Sola, M, Barja, MV, Manzano, D, Llorente, B, Schipper, B, Beekwilder, J & Rodriguez-Concepcion, M 2016, 'A single arabidopsis gene encodes two differentially targeted geranylgeranyl diphosphate synthase isoforms', Plant Physiology, vol. 172, no. 3, pp. 1393-1402. https://doi.org/10.1104/pp.16.01392

A single arabidopsis gene encodes two differentially targeted geranylgeranyl diphosphate synthase isoforms. / Águila Ruiz-Sola, M.; Barja, M.V.; Manzano, David; Llorente, Briardo; Schipper, Bert; Beekwilder, Jules; Rodriguez-Concepcion, Manuel.

In: Plant Physiology, Vol. 172, No. 3, 2016, p. 1393-1402.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - A single arabidopsis gene encodes two differentially targeted geranylgeranyl diphosphate synthase isoforms

AU - Águila Ruiz-Sola, M.

AU - Barja, M.V.

AU - Manzano, David

AU - Llorente, Briardo

AU - Schipper, Bert

AU - Beekwilder, Jules

AU - Rodriguez-Concepcion, Manuel

PY - 2016

Y1 - 2016

N2 - A wide diversity of isoprenoids is produced in different plant compartments. Most groups of isoprenoids synthesized in plastids, and some produced elsewhere in the plant cell derive from geranylgeranyl diphosphate (GGPP) synthesized by GGPP synthase (GGPPS) enzymes. In Arabidopsis (Arabidopsis thaliana), five genes appear to encode GGPPS isoforms localized in plastids (two), the endoplasmic reticulum (two), and mitochondria (one). However, the loss of function of the plastid-targeted GGPPS11 isoform (referred to as G11) is sufficient to cause lethality. Here, we show that the absence of a strong transcription initiation site in the G11 gene results in the production of transcripts of different lengths. The longer transcripts encode an isoform with a functional plastid import sequence that produces GGPP for the major groups of photosynthesis-related plastidial isoprenoids. However, shorter transcripts are also produced that lack the first translation initiation codon and rely on a second in-frame ATG codon to produce an enzymatically active isoform lacking this N-terminal domain. This short enzyme localizes in the cytosol and is essential for embryo development. Our results confirm that the production of differentially targeted enzyme isoforms from the same gene is a central mechanism to control the biosynthesis of isoprenoid precursors in different plant cell compartments.

AB - A wide diversity of isoprenoids is produced in different plant compartments. Most groups of isoprenoids synthesized in plastids, and some produced elsewhere in the plant cell derive from geranylgeranyl diphosphate (GGPP) synthesized by GGPP synthase (GGPPS) enzymes. In Arabidopsis (Arabidopsis thaliana), five genes appear to encode GGPPS isoforms localized in plastids (two), the endoplasmic reticulum (two), and mitochondria (one). However, the loss of function of the plastid-targeted GGPPS11 isoform (referred to as G11) is sufficient to cause lethality. Here, we show that the absence of a strong transcription initiation site in the G11 gene results in the production of transcripts of different lengths. The longer transcripts encode an isoform with a functional plastid import sequence that produces GGPP for the major groups of photosynthesis-related plastidial isoprenoids. However, shorter transcripts are also produced that lack the first translation initiation codon and rely on a second in-frame ATG codon to produce an enzymatically active isoform lacking this N-terminal domain. This short enzyme localizes in the cytosol and is essential for embryo development. Our results confirm that the production of differentially targeted enzyme isoforms from the same gene is a central mechanism to control the biosynthesis of isoprenoid precursors in different plant cell compartments.

U2 - 10.1104/pp.16.01392

DO - 10.1104/pp.16.01392

M3 - Article

VL - 172

SP - 1393

EP - 1402

JO - Plant Physiology

T2 - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 3

ER -