Distribution and Functions of Monodehydroascorbate Reductases in Plants: Comprehensive Reverse Genetic Analysis of <i>Arabidopsis thaliana</i> Enzymes

Monodehydroascorbate reductase (MDAR) is an enzyme involved in ascorbate recycling. <i>Arabidopsis thaliana</i> has five <i>MDAR</i> genes that encode two cytosolic, one cytosolic/peroxisomal, one peroxisomal membrane-attached, and one chloroplastic/mitochondrial isoform. In...

Full description

Bibliographic Details
Main Authors: Mio Tanaka, Ryuki Takahashi, Akane Hamada, Yusuke Terai, Takahisa Ogawa, Yoshihiro Sawa, Takahiro Ishikawa, Takanori Maruta
Format: Article
Language:English
Published: MDPI AG 2021-10-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/10/11/1726
_version_ 1797511409890754560
author Mio Tanaka
Ryuki Takahashi
Akane Hamada
Yusuke Terai
Takahisa Ogawa
Yoshihiro Sawa
Takahiro Ishikawa
Takanori Maruta
author_facet Mio Tanaka
Ryuki Takahashi
Akane Hamada
Yusuke Terai
Takahisa Ogawa
Yoshihiro Sawa
Takahiro Ishikawa
Takanori Maruta
author_sort Mio Tanaka
collection DOAJ
description Monodehydroascorbate reductase (MDAR) is an enzyme involved in ascorbate recycling. <i>Arabidopsis thaliana</i> has five <i>MDAR</i> genes that encode two cytosolic, one cytosolic/peroxisomal, one peroxisomal membrane-attached, and one chloroplastic/mitochondrial isoform. In contrast, tomato plants possess only three enzymes, lacking the cytosol-specific enzymes. Thus, the number and distribution of MDAR isoforms differ according to plant species. Moreover, the physiological significance of MDARs remains poorly understood. In this study, we classify plant MDARs into three classes: class I, chloroplastic/mitochondrial enzymes; class II, peroxisomal membrane-attached enzymes; and class III, cytosolic/peroxisomal enzymes. The cytosol-specific isoforms form a subclass of class III and are conserved only in Brassicaceae plants. With some exceptions, all land plants and a charophyte algae, <i>Klebsormidium flaccidum</i>, contain all three classes. Using reverse genetic analysis of <i>Arabidopsis thaliana</i> mutants lacking one or more isoforms, we provide new insight into the roles of MDARs; for example, (1) the lack of two isoforms in a specific combination results in lethality, and (2) the role of MDARs in ascorbate redox regulation in leaves can be largely compensated by other systems. Based on these findings, we discuss the distribution and function of MDAR isoforms in land plants and their cooperation with other recycling systems.
first_indexed 2024-03-10T05:44:53Z
format Article
id doaj.art-2425bec247c0408dae49fa228278c941
institution Directory Open Access Journal
issn 2076-3921
language English
last_indexed 2024-03-10T05:44:53Z
publishDate 2021-10-01
publisher MDPI AG
record_format Article
series Antioxidants
spelling doaj.art-2425bec247c0408dae49fa228278c9412023-11-22T22:12:48ZengMDPI AGAntioxidants2076-39212021-10-011011172610.3390/antiox10111726Distribution and Functions of Monodehydroascorbate Reductases in Plants: Comprehensive Reverse Genetic Analysis of <i>Arabidopsis thaliana</i> EnzymesMio Tanaka0Ryuki Takahashi1Akane Hamada2Yusuke Terai3Takahisa Ogawa4Yoshihiro Sawa5Takahiro Ishikawa6Takanori Maruta7Graduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue 690-8504, Shimane, JapanDepartment of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue 690-8504, Shimane, JapanGraduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue 690-8504, Shimane, JapanDepartment of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue 690-8504, Shimane, JapanGraduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue 690-8504, Shimane, JapanDepartment of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue 690-8504, Shimane, JapanGraduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue 690-8504, Shimane, JapanGraduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue 690-8504, Shimane, JapanMonodehydroascorbate reductase (MDAR) is an enzyme involved in ascorbate recycling. <i>Arabidopsis thaliana</i> has five <i>MDAR</i> genes that encode two cytosolic, one cytosolic/peroxisomal, one peroxisomal membrane-attached, and one chloroplastic/mitochondrial isoform. In contrast, tomato plants possess only three enzymes, lacking the cytosol-specific enzymes. Thus, the number and distribution of MDAR isoforms differ according to plant species. Moreover, the physiological significance of MDARs remains poorly understood. In this study, we classify plant MDARs into three classes: class I, chloroplastic/mitochondrial enzymes; class II, peroxisomal membrane-attached enzymes; and class III, cytosolic/peroxisomal enzymes. The cytosol-specific isoforms form a subclass of class III and are conserved only in Brassicaceae plants. With some exceptions, all land plants and a charophyte algae, <i>Klebsormidium flaccidum</i>, contain all three classes. Using reverse genetic analysis of <i>Arabidopsis thaliana</i> mutants lacking one or more isoforms, we provide new insight into the roles of MDARs; for example, (1) the lack of two isoforms in a specific combination results in lethality, and (2) the role of MDARs in ascorbate redox regulation in leaves can be largely compensated by other systems. Based on these findings, we discuss the distribution and function of MDAR isoforms in land plants and their cooperation with other recycling systems.https://www.mdpi.com/2076-3921/10/11/1726ascorbate recyclingmonodehydroascorbate reductasedehydroascorbate reductaselight stress<i>Arabidopsis thaliana</i>
spellingShingle Mio Tanaka
Ryuki Takahashi
Akane Hamada
Yusuke Terai
Takahisa Ogawa
Yoshihiro Sawa
Takahiro Ishikawa
Takanori Maruta
Distribution and Functions of Monodehydroascorbate Reductases in Plants: Comprehensive Reverse Genetic Analysis of <i>Arabidopsis thaliana</i> Enzymes
Antioxidants
ascorbate recycling
monodehydroascorbate reductase
dehydroascorbate reductase
light stress
<i>Arabidopsis thaliana</i>
title Distribution and Functions of Monodehydroascorbate Reductases in Plants: Comprehensive Reverse Genetic Analysis of <i>Arabidopsis thaliana</i> Enzymes
title_full Distribution and Functions of Monodehydroascorbate Reductases in Plants: Comprehensive Reverse Genetic Analysis of <i>Arabidopsis thaliana</i> Enzymes
title_fullStr Distribution and Functions of Monodehydroascorbate Reductases in Plants: Comprehensive Reverse Genetic Analysis of <i>Arabidopsis thaliana</i> Enzymes
title_full_unstemmed Distribution and Functions of Monodehydroascorbate Reductases in Plants: Comprehensive Reverse Genetic Analysis of <i>Arabidopsis thaliana</i> Enzymes
title_short Distribution and Functions of Monodehydroascorbate Reductases in Plants: Comprehensive Reverse Genetic Analysis of <i>Arabidopsis thaliana</i> Enzymes
title_sort distribution and functions of monodehydroascorbate reductases in plants comprehensive reverse genetic analysis of i arabidopsis thaliana i enzymes
topic ascorbate recycling
monodehydroascorbate reductase
dehydroascorbate reductase
light stress
<i>Arabidopsis thaliana</i>
url https://www.mdpi.com/2076-3921/10/11/1726
work_keys_str_mv AT miotanaka distributionandfunctionsofmonodehydroascorbatereductasesinplantscomprehensivereversegeneticanalysisofiarabidopsisthalianaienzymes
AT ryukitakahashi distributionandfunctionsofmonodehydroascorbatereductasesinplantscomprehensivereversegeneticanalysisofiarabidopsisthalianaienzymes
AT akanehamada distributionandfunctionsofmonodehydroascorbatereductasesinplantscomprehensivereversegeneticanalysisofiarabidopsisthalianaienzymes
AT yusuketerai distributionandfunctionsofmonodehydroascorbatereductasesinplantscomprehensivereversegeneticanalysisofiarabidopsisthalianaienzymes
AT takahisaogawa distributionandfunctionsofmonodehydroascorbatereductasesinplantscomprehensivereversegeneticanalysisofiarabidopsisthalianaienzymes
AT yoshihirosawa distributionandfunctionsofmonodehydroascorbatereductasesinplantscomprehensivereversegeneticanalysisofiarabidopsisthalianaienzymes
AT takahiroishikawa distributionandfunctionsofmonodehydroascorbatereductasesinplantscomprehensivereversegeneticanalysisofiarabidopsisthalianaienzymes
AT takanorimaruta distributionandfunctionsofmonodehydroascorbatereductasesinplantscomprehensivereversegeneticanalysisofiarabidopsisthalianaienzymes