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Title: Peroxisomes: versatile organelles with diverse roles in plants

Abstract

Peroxisomes are small, ubiquitous organelles that are delimited by a single membrane and lack genetic material. However, these simple-structured organelles are highly versatile in morphology, abundance and protein content in response to various developmental and environmental cues. In plants, peroxisomes are essential for growth and development and perform diverse metabolic functions, many of which are carried out coordinately by peroxisomes and other organelles physically interacting with peroxisomes. Recent studies have added greatly to our knowledge of peroxisomes, addressing areas such as the diverse proteome, regulation of division and protein import, pexophagy, matrix protein degradation, solute transport, signaling, redox homeostasis and various metabolic and physiological functions. This review summarizes our current understanding of plant peroxisomes, focusing on recent discoveries. Current problems and future efforts required to better understand these organelles are also discussed. Here, an improved understanding of peroxisomes will be important not only to the understanding of eukaryotic cell biology and metabolism, but also to agricultural efforts aimed at improving crop performance and defense.

Authors:
 [1];  [1];  [1]; ORCiD logo [2]
  1. Zhejiang Univ. Hangzhou (China)
  2. Michigan State Univ., East Lansing, MI (United States)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1734850
Alternate Identifier(s):
OSTI ID: 1566900
Grant/Contract Number:  
FG02-91ER20021; FG02‐91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 225; Journal Issue: 4; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; division; inter‐organellar interaction; metabolism; peroxisome protein import; peroxisomes; pexophagy; proteome; β‐oxidation

Citation Formats

Pan, Ronghui, Liu, Jun, Wang, Saisai, and Hu, Jianping. Peroxisomes: versatile organelles with diverse roles in plants. United States: N. p., 2019. Web. doi:10.1111/nph.16134.
Pan, Ronghui, Liu, Jun, Wang, Saisai, & Hu, Jianping. Peroxisomes: versatile organelles with diverse roles in plants. United States. https://doi.org/10.1111/nph.16134
Pan, Ronghui, Liu, Jun, Wang, Saisai, and Hu, Jianping. Fri . "Peroxisomes: versatile organelles with diverse roles in plants". United States. https://doi.org/10.1111/nph.16134. https://www.osti.gov/servlets/purl/1734850.
@article{osti_1734850,
title = {Peroxisomes: versatile organelles with diverse roles in plants},
author = {Pan, Ronghui and Liu, Jun and Wang, Saisai and Hu, Jianping},
abstractNote = {Peroxisomes are small, ubiquitous organelles that are delimited by a single membrane and lack genetic material. However, these simple-structured organelles are highly versatile in morphology, abundance and protein content in response to various developmental and environmental cues. In plants, peroxisomes are essential for growth and development and perform diverse metabolic functions, many of which are carried out coordinately by peroxisomes and other organelles physically interacting with peroxisomes. Recent studies have added greatly to our knowledge of peroxisomes, addressing areas such as the diverse proteome, regulation of division and protein import, pexophagy, matrix protein degradation, solute transport, signaling, redox homeostasis and various metabolic and physiological functions. This review summarizes our current understanding of plant peroxisomes, focusing on recent discoveries. Current problems and future efforts required to better understand these organelles are also discussed. Here, an improved understanding of peroxisomes will be important not only to the understanding of eukaryotic cell biology and metabolism, but also to agricultural efforts aimed at improving crop performance and defense.},
doi = {10.1111/nph.16134},
journal = {New Phytologist},
number = 4,
volume = 225,
place = {United States},
year = {Fri Aug 23 00:00:00 EDT 2019},
month = {Fri Aug 23 00:00:00 EDT 2019}
}

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Starch Deficiency Enhances Lipid Biosynthesis and Turnover in Leaves
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  • Yu, Linhui; Fan, Jilian; Yan, Chengshi
  • Plant Physiology, Vol. 178, Issue 1
  • DOI: 10.1104/pp.18.00539

Cadmium induces reactive oxygen species‐dependent pexophagy in Arabidopsis leaves
journal, May 2019

  • Calero‐Muñoz, Nieves; Exposito‐Rodriguez, Marino; Collado‐Arenal, Aurelio M.
  • Plant, Cell & Environment, Vol. 42, Issue 9
  • DOI: 10.1111/pce.13597

Modulation of Guard Cell Turgor and Drought Tolerance by a Peroxisomal Acetate–Malate Shunt
journal, October 2018


The Peroxisome Deficient Arabidopsis Mutant sse1 Exhibits Impaired Fatty Acid Synthesis
journal, June 2004

  • Lin, Yun; Cluette-Brown, Joanne E.; Goodman, Howard M.
  • Plant Physiology, Vol. 135, Issue 2
  • DOI: 10.1104/pp.103.036772

A genetic framework for H2O2 induced cell death in Arabidopsis thaliana
journal, October 2015


Chaperone and Protease Functions of LON Protease 2 Modulate the Peroxisomal Transition and Degradation with Autophagy
journal, February 2014

  • Goto-Yamada, Shino; Mano, Shoji; Nakamori, Chihiro
  • Plant and Cell Physiology, Vol. 55, Issue 3
  • DOI: 10.1093/pcp/pcu017

Gene-Specific Involvement of β -Oxidation in Wound-Activated Responses in Arabidopsis
journal, May 2004

  • Castillo, M. Cruz; Martínez, Cristina; Buchala, Antony
  • Plant Physiology, Vol. 135, Issue 1
  • DOI: 10.1104/pp.104.039925

Kinase MPK17 and the Peroxisome Division Factor PMD1 Influence Salt-induced Peroxisome Proliferation
journal, September 2017

  • Frick, Elizabeth M.; Strader, Lucia C.
  • Plant Physiology, Vol. 176, Issue 1
  • DOI: 10.1104/pp.17.01019

Autophagy regulates glucose-mediated root meristem activity by modulating ROS production in Arabidopsis
journal, September 2018


The Arabidopsis E3 Ubiquitin Ligase SP1 Targets to Chloroplasts, Peroxisomes, and Mitochondria
journal, January 2018


Peroxisome biogenesis, protein targeting mechanisms and PEX gene functions in plants
journal, May 2016

  • Cross, Laura L.; Ebeed, Heba Talat; Baker, Alison
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1863, Issue 5
  • DOI: 10.1016/j.bbamcr.2015.09.027

chy1 , an Arabidopsis Mutant with Impaired β-Oxidation, Is Defective in a Peroxisomal β-Hydroxyisobutyryl-CoA Hydrolase
journal, June 2001

  • Zolman, Bethany K.; Monroe-Augustus, Melanie; Thompson, Beth
  • Journal of Biological Chemistry, Vol. 276, Issue 33
  • DOI: 10.1074/jbc.M104679200

OsPEX11, a Peroxisomal Biogenesis Factor 11, Contributes to Salt Stress Tolerance in Oryza sativa
journal, September 2016


Plant peroxisomes: A nitro-oxidative cocktail
journal, April 2017


Peroxisomes in plant reproduction and seed-related development: Peroxisomes in reproduction, seeds and seedlings
journal, February 2019

  • Pan, Ronghui; Liu, Jun; Hu, Jianping
  • Journal of Integrative Plant Biology, Vol. 61, Issue 7
  • DOI: 10.1111/jipb.12765

Plant Peroxisomes: Biogenesis and Function
journal, June 2012


Metabolic Interplay between Peroxisomes and Other Subcellular Organelles Including Mitochondria and the Endoplasmic Reticulum
journal, January 2016

  • Wanders, Ronald J. A.; Waterham, Hans R.; Ferdinandusse, Sacha
  • Frontiers in Cell and Developmental Biology, Vol. 3
  • DOI: 10.3389/fcell.2015.00083

Re‐evaluation of physical interaction between plant peroxisomes and other organelles using live‐cell imaging techniques
journal, May 2019

  • Oikawa, Kazusato; Hayashi, Makoto; Hayashi, Yasuko
  • Journal of Integrative Plant Biology
  • DOI: 10.1111/jipb.12805

The Arabidopsis catalase triple mutant reveals important roles of catalases and peroxisome-derived signaling in plant development
journal, June 2018

  • Su, Tong; Wang, Pingping; Li, Huijuan
  • Journal of Integrative Plant Biology, Vol. 60, Issue 7
  • DOI: 10.1111/jipb.12649

A peroxisomal carrier delivers NAD+ and contributes to optimal fatty acid degradation during storage oil mobilization: Peroxisomal NAD import
journal, October 2011


Peroxisome Biogenesis and Function
journal, January 2009

  • Kaur, Navneet; Reumann, Sigrun; Hu, Jianping
  • The Arabidopsis Book, Vol. 7
  • DOI: 10.1199/tab.0123

Plant peroxisomes at the crossroad of NO and H 2 O 2 metabolism
journal, April 2019

  • Corpas, Francisco J.; del Río, Luis A.; Palma, José M.
  • Journal of Integrative Plant Biology
  • DOI: 10.1111/jipb.12772

The Arabidopsis DELAYED DEHISCENCE1 Gene Encodes an Enzyme in the Jasmonic Acid Synthesis Pathway
journal, July 2000

  • Sanders, Paul M.; Lee, Pei Yun; Biesgen, Christian
  • The Plant Cell, Vol. 12, Issue 7
  • DOI: 10.1105/tpc.12.7.1041

Peroxisomes Extend Peroxules in a Fast Response to Stress via a Reactive Oxygen Species-Mediated Induction of the Peroxin PEX11a
journal, May 2016

  • Rodríguez-Serrano, María; Romero-Puertas, María C.; Sanz-Fernández, María
  • Plant Physiology, Vol. 171, Issue 3
  • DOI: 10.1104/pp.16.00648

Peroxisomal APX knockdown triggers antioxidant mechanisms favourable for coping with high photorespiratory H 2 O 2 induced by CAT deficiency in rice : pAPX KD rice displays high H
journal, August 2014

  • Sousa, Rachel H. V.; Carvalho, Fabricio E. L.; Ribeiro, Carol W.
  • Plant, Cell & Environment, Vol. 38, Issue 3
  • DOI: 10.1111/pce.12409

Hydrogen sulfide: A novel component in Arabidopsis peroxisomes which triggers catalase inhibition
journal, April 2019

  • Corpas, Francisco J.; Barroso, Juan B.; González‐Gordo, Salvador
  • Journal of Integrative Plant Biology
  • DOI: 10.1111/jipb.12779

OPEN GLUME1: a key enzyme reducing the precursor of JA, participates in carbohydrate transport of lodicules during anthesis in rice
journal, November 2017


Disparate peroxisome‐related defects in Arabidopsis pex6 and pex26 mutants link peroxisomal retrotranslocation and oil body utilization
journal, August 2017

  • Gonzalez, Kim L.; Fleming, Wendell A.; Kao, Yun‐Ting
  • The Plant Journal, Vol. 92, Issue 1
  • DOI: 10.1111/tpj.13641

Catalase and ascorbate peroxidase—representative H2O2-detoxifying heme enzymes in plants
journal, August 2016

  • Anjum, Naser A.; Sharma, Pallavi; Gill, Sarvajeet S.
  • Environmental Science and Pollution Research, Vol. 23, Issue 19
  • DOI: 10.1007/s11356-016-7309-6

Control of sexuality by the sk1 -encoded UDP-glycosyltransferase of maize
journal, October 2016

  • Hayward, Andrew P.; Moreno, Maria A.; Howard, Thomas P.
  • Science Advances, Vol. 2, Issue 10
  • DOI: 10.1126/sciadv.1600991

Acyl-CoA measurements in plants suggest a role in regulating various cellular processes
journal, November 2002

  • Graham, I. A.; Li, Y.; Larson, T. R.
  • Biochemical Society Transactions, Vol. 30, Issue 6
  • DOI: 10.1042/bst0301095

Identification of Novel Plant Peroxisomal Targeting Signals by a Combination of Machine Learning Methods and in Vivo Subcellular Targeting Analyses
journal, April 2011

  • Lingner, Thomas; Kataya, Amr R.; Antonicelli, Gerardo E.
  • The Plant Cell, Vol. 23, Issue 4
  • DOI: 10.1105/tpc.111.084095

The life of the peroxisome: from birth to death
journal, December 2014


Genetic Interactions between PEROXIN12 and Other Peroxisome-Associated Ubiquitination Components
journal, September 2016

  • Kao, Yun-Ting; Fleming, Wendell A.; Ventura, Meredith J.
  • Plant Physiology, Vol. 172, Issue 3
  • DOI: 10.1104/pp.16.01211

E3 ubiquitin ligase SP1 regulates peroxisome biogenesis in Arabidopsis
journal, October 2016

  • Pan, Ronghui; Satkovich, John; Hu, Jianping
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 46
  • DOI: 10.1073/pnas.1613530113

Proteome Analysis of Arabidopsis Leaf Peroxisomes Reveals Novel Targeting Peptides, Metabolic Pathways, and Defense Mechanisms
journal, October 2007

  • Reumann, Sigrun; Babujee, Lavanya; Ma, Changle
  • The Plant Cell, Vol. 19, Issue 10
  • DOI: 10.1105/tpc.107.050989

Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks
journal, June 2015

  • Sandalio, L. M.; Romero-Puertas, M. C.
  • Annals of Botany, Vol. 116, Issue 4
  • DOI: 10.1093/aob/mcv074

Sucrose Production Mediated by Lipid Metabolism Suppresses the Physical Interaction of Peroxisomes and Oil Bodies during Germination of Arabidopsis thaliana
journal, July 2016

  • Cui, Songkui; Hayashi, Yasuko; Otomo, Masayoshi
  • Journal of Biological Chemistry, Vol. 291, Issue 38
  • DOI: 10.1074/jbc.M116.748814

Catalase and NO CATALASE ACTIVITY1 Promote Autophagy-Dependent Cell Death in Arabidopsis
journal, November 2013


Arabidopsis LON2 Is Necessary for Peroxisomal Function and Sustained Matrix Protein Import
journal, September 2009


A peroxisomal thioesterase plays auxiliary roles in plant β‐oxidative benzoic acid metabolism
journal, February 2018

  • Adebesin, Funmilayo; Widhalm, Joshua R.; Lynch, Joseph H.
  • The Plant Journal, Vol. 93, Issue 5
  • DOI: 10.1111/tpj.13818

Lack of GLYCOLATE OXIDASE1, but Not GLYCOLATE OXIDASE2, Attenuates the Photorespiratory Phenotype of CATALASE2-Deficient Arabidopsis
journal, May 2016

  • Kerchev, Pavel; Waszczak, Cezary; Lewandowska, Aleksandra
  • Plant Physiology, Vol. 171, Issue 3
  • DOI: 10.1104/pp.16.00359

New Insights into Plant Isoprenoid Metabolism
journal, September 2012

  • Pulido, Pablo; Perello, Catalina; Rodriguez-Concepcion, Manuel
  • Molecular Plant, Vol. 5, Issue 5
  • DOI: 10.1093/mp/sss088

Arabidopsis Forkhead‐Associated Domain Protein 3 negatively regulates peroxisome division
journal, June 2017

  • Desai, Mintu; Pan, Ronghui; Hu, Jianping
  • Journal of Integrative Plant Biology, Vol. 59, Issue 7
  • DOI: 10.1111/jipb.12542

Dual specificities of the glyoxysomal/peroxisomal processing protease Deg15 in higher plants
journal, June 2007

  • Helm, M.; Luck, C.; Prestele, J.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 27
  • DOI: 10.1073/pnas.0704733104

Dynamics of peroxisome abundance: a tale of division and proliferation
journal, December 2009


Organ-specific quality control of plant peroxisomes is mediated by autophagy
journal, January 2014

  • Yoshimoto, K.; Shibata, M.; Kondo, M.
  • Journal of Cell Science, Vol. 127, Issue 6
  • DOI: 10.1242/jcs.139709

Novel Glyoxysomal Protein Kinase, GPK1, Identified by Proteomic Analysis of Glyoxysomes in Etiolated Cotyledons of Arabidopsis thaliana
journal, October 2003

  • Fukao, Yoichiro; Hayashi, Makoto; Hara-Nishimura, Ikuko
  • Plant and Cell Physiology, Vol. 44, Issue 10
  • DOI: 10.1093/pcp/pcg145

Highly Oxidized Peroxisomes Are Selectively Degraded via Autophagy in Arabidopsis
journal, December 2013

  • Shibata, Michitaro; Oikawa, Kazusato; Yoshimoto, Kohki
  • The Plant Cell, Vol. 25, Issue 12
  • DOI: 10.1105/tpc.113.116947

Plant and Animal Glycolate Oxidases Have a Common Eukaryotic Ancestor and Convergently Duplicated to Evolve Long-Chain 2-Hydroxy Acid Oxidases
journal, January 2014

  • Esser, Christian; Kuhn, Anke; Groth, Georg
  • Molecular Biology and Evolution, Vol. 31, Issue 5
  • DOI: 10.1093/molbev/msu041

A vesicle carrier that mediates peroxisome protein traffic from the endoplasmic reticulum
journal, November 2010

  • Lam, S. K.; Yoda, N.; Schekman, R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 50
  • DOI: 10.1073/pnas.1013397107

The Arabidopsis DELAYED DEHISCENCE1 Gene Encodes an Enzyme in the Jasmonic Acid Synthesis Pathway
journal, July 2000

  • Sanders, Paul M.; Lee, Pei Yun; Biesgen, Christian
  • The Plant Cell, Vol. 12, Issue 7
  • DOI: 10.2307/3871254

Terpenoid Metabolism
journal, July 1995

  • McGarvey, Douglas J.; Croteau, Rodney
  • The Plant Cell, Vol. 7, Issue 7
  • DOI: 10.2307/3870054

ATG8-Binding UIM Proteins Define a New Class of Autophagy Adaptors and Receptors
journal, March 2022