ABA-Mediated ROS in Mitochondria Regulate Root Meristem Activity by Controlling PLETHORA Expression in Arabidopsis

Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An aba overly sensitive mutant, abo8-1, which is defective in a pentatricopeptide repeat (PPR) prote...

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Published inPLoS genetics Vol. 10; no. 12; p. e1004791
Main Authors Yang, Li, Zhang, Jing, He, Junna, Qin, Yingying, Hua, Deping, Duan, Ying, Chen, Zhizhong, Gong, Zhizhong
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.12.2014
Public Library of Science (PLoS)
Subjects
Abscisic acid
Abscisic Acid - pharmacology
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Biology and Life Sciences
Botanical research
Cloning
Electron Transport Complex I - genetics
Electron Transport Complex I - metabolism
Ethanol
Gene expression
Genetic aspects
Genetic research
Genotype
Glycerol
Growth hormones
Health aspects
Homeostasis
Introns
Meristem - genetics
Meristem - metabolism
Mitochondria
Mitochondria - metabolism
Phenotype
Plant Development
Plant growth
Plant Roots - genetics
Plant Roots - metabolism
Promoter Regions, Genetic
Proteins
Reactive oxygen species
Reactive Oxygen Species - metabolism
RNA Splicing
Signal Transduction
Transcription Factors - genetics
Transcription Factors - metabolism
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Abstract Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An aba overly sensitive mutant, abo8-1, which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in mitochondrial complex I, accumulates more ROS in root tips than the wild type, and the ROS accumulation is further enhanced by ABA treatment. The ABO8 mutation reduces root meristem activity, which can be enhanced by ABA treatment and reversibly recovered by addition of certain concentrations of the reducing agent GSH. As indicated by low ProDR5:GUS expression, auxin accumulation/signaling was reduced in abo8-1. We also found that ABA inhibits the expression of PLETHORA1 (PLT1) and PLT2, and that root growth is more sensitive to ABA in the plt1 and plt2 mutants than in the wild type. The expression of PLT1 and PLT2 is significantly reduced in the abo8-1 mutant. Overexpression of PLT2 in an inducible system can largely rescue root apical meristem (RAM)-defective phenotype of abo8-1 with and without ABA treatment. These results suggest that ABA-promoted ROS in the mitochondria of root tips are important retrograde signals that regulate root meristem activity by controlling auxin accumulation/signaling and PLT expression in Arabidopsis.
AbstractList Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An aba overly sensitive mutant, abo8-1, which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in mitochondrial complex I, accumulates more ROS in root tips than the wild type, and the ROS accumulation is further enhanced by ABA treatment. The ABO8 mutation reduces root meristem activity, which can be enhanced by ABA treatment and reversibly recovered by addition of certain concentrations of the reducing agent GSH. As indicated by low ProDR5:GUS expression, auxin accumulation/signaling was reduced in abo8-1. We also found that ABA inhibits the expression of PLETHORA1 (PLT1) and PLT2, and that root growth is more sensitive to ABA in the plt1 and plt2 mutants than in the wild type. The expression of PLT1 and PLT2 is significantly reduced in the abo8-1 mutant. Overexpression of PLT2 in an inducible system can largely rescue root apical meristem (RAM)-defective phenotype of abo8-1 with and without ABA treatment. These results suggest that ABA-promoted ROS in the mitochondria of root tips are important retrograde signals that regulate root meristem activity by controlling auxin accumulation/signaling and PLT expression in Arabidopsis.
  Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An aba overly sensitive mutant, abo8-1, which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in mitochondrial complex I, accumulates more ROS in root tips than the wild type, and the ROS accumulation is further enhanced by ABA treatment. The ABO8 mutation reduces root meristem activity, which can be enhanced by ABA treatment and reversibly recovered by addition of certain concentrations of the reducing agent GSH. As indicated by low ProDR5:GUS expression, auxin accumulation/signaling was reduced in abo8-1. We also found that ABA inhibits the expression of PLETHORA1 (PLT1) and PLT2, and that root growth is more sensitive to ABA in the plt1 and plt2 mutants than in the wild type. The expression of PLT1 and PLT2 is significantly reduced in the abo8-1 mutant. Overexpression of PLT2 in an inducible system can largely rescue root apical meristem (RAM)-defective phenotype of abo8-1 with and without ABA treatment. These results suggest that ABA-promoted ROS in the mitochondria of root tips are important retrograde signals that regulate root meristem activity by controlling auxin accumulation/signaling and PLT expression in Arabidopsis.
Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An ab a o verly sensitive mutant, abo8-1 , which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in mitochondrial complex I, accumulates more ROS in root tips than the wild type, and the ROS accumulation is further enhanced by ABA treatment. The ABO8 mutation reduces root meristem activity, which can be enhanced by ABA treatment and reversibly recovered by addition of certain concentrations of the reducing agent GSH. As indicated by low ProDR5:GUS expression, auxin accumulation/signaling was reduced in abo8-1 . We also found that ABA inhibits the expression of PLETHORA1 ( PLT1 ) and PLT2 , and that root growth is more sensitive to ABA in the plt1 and plt2 mutants than in the wild type. The expression of PLT1 and PLT2 is significantly reduced in the abo8-1 mutant. Overexpression of PLT2 in an inducible system can largely rescue root apical meristem (RAM)-defective phenotype of abo8-1 with and without ABA treatment. These results suggest that ABA-promoted ROS in the mitochondria of root tips are important retrograde signals that regulate root meristem activity by controlling auxin accumulation/signaling and PLT expression in Arabidopsis . Abscisic acid (ABA) plays crucial roles in plant growth and development, and also in plant responses to abiotic and biotic stresses. ABA can stimulate the production of reactive oxygen species (ROS) that act as signals in low concentrations, but as cell-damaging agents in high concentrations. A mutation in ABO8 , encoding a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3, leads to hypersensitivity to ABA in root growth, and root tips of the abo8-1 mutants accumulate more ROS than those of the wild type; this accumulation of ROS in abo8-1 root tips is enhanced by ABA treatment. We also found that auxin signaling and/or accumulation is greatly reduced in root tips of the abo8-1 mutants. Addition of the reducing agent GSH to the growth medium partially recovers the root hypersensitivity to ABA, and also the ABA-inhibited expression of PLT1/2 in abo8-1 . Furthermore, the inducible expression of PLT2 largely rescues the root growth defect of abo8-1 with and without ABA treatment. Our results reveal the important roles of ROS in regulating root meristem activity in the ABA signaling pathway.
Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An aba overly sensitive mutant, abo8-1, which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in mitochondrial complex I, accumulates more ROS in root tips than the wild type, and the ROS accumulation is further enhanced by ABA treatment. The ABO8 mutation reduces root meristem activity, which can be enhanced by ABA treatment and reversibly recovered by addition of certain concentrations of the reducing agent GSH. As indicated by low ProDR5:GUS expression, auxin accumulation/signaling was reduced in abo8-1. We also found that ABA inhibits the expression of PLETHORA1 (PLT1) and PLT2, and that root growth is more sensitive to ABA in the plt1 and plt2 mutants than in the wild type. The expression of PLT1 and PLT2 is significantly reduced in the abo8-1 mutant. Overexpression of PLT2 in an inducible system can largely rescue root apical meristem (RAM)-defective phenotype of abo8-1 with and without ABA treatment. These results suggest that ABA-promoted ROS in the mitochondria of root tips are important retrograde signals that regulate root meristem activity by controlling auxin accumulation/signaling and PLT expression in Arabidopsis.Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An aba overly sensitive mutant, abo8-1, which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in mitochondrial complex I, accumulates more ROS in root tips than the wild type, and the ROS accumulation is further enhanced by ABA treatment. The ABO8 mutation reduces root meristem activity, which can be enhanced by ABA treatment and reversibly recovered by addition of certain concentrations of the reducing agent GSH. As indicated by low ProDR5:GUS expression, auxin accumulation/signaling was reduced in abo8-1. We also found that ABA inhibits the expression of PLETHORA1 (PLT1) and PLT2, and that root growth is more sensitive to ABA in the plt1 and plt2 mutants than in the wild type. The expression of PLT1 and PLT2 is significantly reduced in the abo8-1 mutant. Overexpression of PLT2 in an inducible system can largely rescue root apical meristem (RAM)-defective phenotype of abo8-1 with and without ABA treatment. These results suggest that ABA-promoted ROS in the mitochondria of root tips are important retrograde signals that regulate root meristem activity by controlling auxin accumulation/signaling and PLT expression in Arabidopsis.
Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS regulate plant growth is not well known. An aba overly sensitive mutant, abo8-7, which is defective in a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3 in mitochondrial complex I, accumulates more ROS in root tips than the wild type, and the ROS accumulation is further enhanced by ABA treatment. The ABO8 mutation reduces root meristem activity, which can be enhanced by ABA treatment and reversibly recovered by addition of certain concentrations of the reducing agent GSH. As indicated by low ProDR5:GUS expression, auxin accumulation/signaling was reduced in abo8-7. We also found that ABA inhibits the expression of PLETHORA7 (PLT7) and PLT2, and that root growth is more sensitive to ABA in the plt7 and plt2 mutants than in the wild type. The expression of PLT7 and PLT2 is significantly reduced in the abo8-7 mutant. Overexpression of PLT2 in an inducible system can largely rescue root apical meristem (RAM)-defective phenotype of abo8-7 with and without ABA treatment. These results suggest that ABA-promoted ROS in the mitochondria of root tips are important retrograde signals that regulate root meristem activity by controlling auxin accumulation/signaling and PLT expression in Arabidopsis.
Audience Academic
Author Zhang, Jing
Duan, Ying
Hua, Deping
Chen, Zhizhong
Yang, Li
Qin, Yingying
He, Junna
Gong, Zhizhong
AuthorAffiliation 1 State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, China
2 National Center for Plant Gene Research, Beijing, China
National University of Singapore and Temasek Life Sciences Laboratory, Singapore
AuthorAffiliation_xml – name: National University of Singapore and Temasek Life Sciences Laboratory, Singapore
– name: 2 National Center for Plant Gene Research, Beijing, China
– name: 1 State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, China
Author_xml – sequence: 1
  givenname: Li
  surname: Yang
  fullname: Yang, Li
– sequence: 2
  givenname: Jing
  surname: Zhang
  fullname: Zhang, Jing
– sequence: 3
  givenname: Junna
  surname: He
  fullname: He, Junna
– sequence: 4
  givenname: Yingying
  surname: Qin
  fullname: Qin, Yingying
– sequence: 5
  givenname: Deping
  surname: Hua
  fullname: Hua, Deping
– sequence: 6
  givenname: Ying
  surname: Duan
  fullname: Duan, Ying
– sequence: 7
  givenname: Zhizhong
  surname: Chen
  fullname: Chen, Zhizhong
– sequence: 8
  givenname: Zhizhong
  surname: Gong
  fullname: Gong, Zhizhong
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25522358$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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2014 Yang et al 2014 Yang et al
2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 10(12): e1004791. doi:10.1371/journal.pgen.1004791
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The authors have declared that no competing interests exist.
Conceived and designed the experiments: LY ZG. Performed the experiments: LY JZ JH YQ DH YD. Analyzed the data: LY JZ ZG. Contributed reagents/materials/analysis tools: ZC ZG. Wrote the paper: LY ZG.
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Snippet Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which ROS...
  Although research has determined that reactive oxygen species (ROS) function as signaling molecules in plant development, the molecular mechanism by which...
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StartPage e1004791
SubjectTerms Abscisic acid
Abscisic Acid - pharmacology
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Biology and Life Sciences
Botanical research
Cloning
Electron Transport Complex I - genetics
Electron Transport Complex I - metabolism
Ethanol
Gene expression
Genetic aspects
Genetic research
Genotype
Glycerol
Growth hormones
Health aspects
Homeostasis
Introns
Meristem - genetics
Meristem - metabolism
Mitochondria
Mitochondria - metabolism
Phenotype
Plant Development
Plant growth
Plant Roots - genetics
Plant Roots - metabolism
Promoter Regions, Genetic
Proteins
Reactive oxygen species
Reactive Oxygen Species - metabolism
RNA Splicing
Signal Transduction
Transcription Factors - genetics
Transcription Factors - metabolism
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Title ABA-Mediated ROS in Mitochondria Regulate Root Meristem Activity by Controlling PLETHORA Expression in Arabidopsis
URI https://www.ncbi.nlm.nih.gov/pubmed/25522358
https://www.proquest.com/docview/1639975346
https://pubmed.ncbi.nlm.nih.gov/PMC4270459
https://doaj.org/article/8355c1298ab0417499266b861bbbe2e0
http://dx.doi.org/10.1371/journal.pgen.1004791
Volume 10
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