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New perspectives on the plant PARP family: Arabidopsis PARP3 is inactive, and PARP1 exhibits predominant poly (ADP-ribose) polymerase activity in response to DNA damage

BACKGROUND: Poly (ADP-ribosyl) ation (PARylation) is an important posttranslational modification that regulates DNA repair, gene transcription, stress responses and developmental processes in multicellular organisms. Poly (ADP-ribose) polymerase (PARP) catalyzes PARylation by consecutively adding AD...

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Autores principales: Gu, Zongying, Pan, Weiyang, Chen, Wei, Lian, Qichao, Wu, Qiao, Lv, Zeyu, Cheng, Xuan, Ge, Xiaochun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6701155/
https://www.ncbi.nlm.nih.gov/pubmed/31426748
http://dx.doi.org/10.1186/s12870-019-1958-9
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author Gu, Zongying
Pan, Weiyang
Chen, Wei
Lian, Qichao
Wu, Qiao
Lv, Zeyu
Cheng, Xuan
Ge, Xiaochun
author_facet Gu, Zongying
Pan, Weiyang
Chen, Wei
Lian, Qichao
Wu, Qiao
Lv, Zeyu
Cheng, Xuan
Ge, Xiaochun
author_sort Gu, Zongying
collection PubMed
description BACKGROUND: Poly (ADP-ribosyl) ation (PARylation) is an important posttranslational modification that regulates DNA repair, gene transcription, stress responses and developmental processes in multicellular organisms. Poly (ADP-ribose) polymerase (PARP) catalyzes PARylation by consecutively adding ADP-ribose moieties from NAD(+) to the amino acid receptor residues on target proteins. Arabidopsis has three canonical PARP members, and two of these members, AtPARP1 and AtPARP2, have been demonstrated to be bona fide poly (ADP-ribose) polymerases and to regulate DNA repair and stress response processes. However, it remains unknown whether AtPARP3, a member that is highly expressed in seeds, has similar biochemical activity to that of AtPARP1 and AtPARP2. Additionally, although both the phylogenetic relationships and structural similarities indicate that AtPARP1 and AtPARP2 correspond to animal PARP1 and PARP2, respectively, two previous studies have indicated that AtPARP2, and not AtPARP1, accounts for most of the PARP activity in Arabidopsis, which is contrary to the knowledge that PARP1 is the predominant PARP in animals. RESULTS: In this study, we obtained both in vitro and in vivo evidence demonstrating that AtPARP3 does not act as a typical PARP in Arabidopsis. Domain swapping and point mutation assays indicated that AtPARP3 has lost NAD(+)-binding capability and is inactive. In addition, our results showed that AtPARP1 was responsible for most of the PARP enzymatic activity in response to the DNA damage-inducing agents zeocin and methyl methanesulfonate (MMS) and was more rapidly activated than AtPARP2, which supports that AtPARP1 remains the predominant PARP member in Arabidopsis. AtPARP1 might first become activated by binding to damaged sites, and AtPARP2 is then poly (ADP-ribosyl) ated by AtPARP1 in vivo. CONCLUSIONS: Collectively, our biochemical and genetic analysis results strongly support the notion that AtPARP3 has lost poly (ADP-ribose) polymerase activity in plants and performs different functions from those of AtPARP1 and AtPARP2. AtPARP1, instead of AtPARP2, plays the predominant role in PAR synthesis in both seeds and seedlings. These data bring new insights into our understanding of the physiological functions of plant PARP family members. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1958-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-67011552019-08-26 New perspectives on the plant PARP family: Arabidopsis PARP3 is inactive, and PARP1 exhibits predominant poly (ADP-ribose) polymerase activity in response to DNA damage Gu, Zongying Pan, Weiyang Chen, Wei Lian, Qichao Wu, Qiao Lv, Zeyu Cheng, Xuan Ge, Xiaochun BMC Plant Biol Research Article BACKGROUND: Poly (ADP-ribosyl) ation (PARylation) is an important posttranslational modification that regulates DNA repair, gene transcription, stress responses and developmental processes in multicellular organisms. Poly (ADP-ribose) polymerase (PARP) catalyzes PARylation by consecutively adding ADP-ribose moieties from NAD(+) to the amino acid receptor residues on target proteins. Arabidopsis has three canonical PARP members, and two of these members, AtPARP1 and AtPARP2, have been demonstrated to be bona fide poly (ADP-ribose) polymerases and to regulate DNA repair and stress response processes. However, it remains unknown whether AtPARP3, a member that is highly expressed in seeds, has similar biochemical activity to that of AtPARP1 and AtPARP2. Additionally, although both the phylogenetic relationships and structural similarities indicate that AtPARP1 and AtPARP2 correspond to animal PARP1 and PARP2, respectively, two previous studies have indicated that AtPARP2, and not AtPARP1, accounts for most of the PARP activity in Arabidopsis, which is contrary to the knowledge that PARP1 is the predominant PARP in animals. RESULTS: In this study, we obtained both in vitro and in vivo evidence demonstrating that AtPARP3 does not act as a typical PARP in Arabidopsis. Domain swapping and point mutation assays indicated that AtPARP3 has lost NAD(+)-binding capability and is inactive. In addition, our results showed that AtPARP1 was responsible for most of the PARP enzymatic activity in response to the DNA damage-inducing agents zeocin and methyl methanesulfonate (MMS) and was more rapidly activated than AtPARP2, which supports that AtPARP1 remains the predominant PARP member in Arabidopsis. AtPARP1 might first become activated by binding to damaged sites, and AtPARP2 is then poly (ADP-ribosyl) ated by AtPARP1 in vivo. CONCLUSIONS: Collectively, our biochemical and genetic analysis results strongly support the notion that AtPARP3 has lost poly (ADP-ribose) polymerase activity in plants and performs different functions from those of AtPARP1 and AtPARP2. AtPARP1, instead of AtPARP2, plays the predominant role in PAR synthesis in both seeds and seedlings. These data bring new insights into our understanding of the physiological functions of plant PARP family members. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1958-9) contains supplementary material, which is available to authorized users. BioMed Central 2019-08-19 /pmc/articles/PMC6701155/ /pubmed/31426748 http://dx.doi.org/10.1186/s12870-019-1958-9 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Gu, Zongying
Pan, Weiyang
Chen, Wei
Lian, Qichao
Wu, Qiao
Lv, Zeyu
Cheng, Xuan
Ge, Xiaochun
New perspectives on the plant PARP family: Arabidopsis PARP3 is inactive, and PARP1 exhibits predominant poly (ADP-ribose) polymerase activity in response to DNA damage
title New perspectives on the plant PARP family: Arabidopsis PARP3 is inactive, and PARP1 exhibits predominant poly (ADP-ribose) polymerase activity in response to DNA damage
title_full New perspectives on the plant PARP family: Arabidopsis PARP3 is inactive, and PARP1 exhibits predominant poly (ADP-ribose) polymerase activity in response to DNA damage
title_fullStr New perspectives on the plant PARP family: Arabidopsis PARP3 is inactive, and PARP1 exhibits predominant poly (ADP-ribose) polymerase activity in response to DNA damage
title_full_unstemmed New perspectives on the plant PARP family: Arabidopsis PARP3 is inactive, and PARP1 exhibits predominant poly (ADP-ribose) polymerase activity in response to DNA damage
title_short New perspectives on the plant PARP family: Arabidopsis PARP3 is inactive, and PARP1 exhibits predominant poly (ADP-ribose) polymerase activity in response to DNA damage
title_sort new perspectives on the plant parp family: arabidopsis parp3 is inactive, and parp1 exhibits predominant poly (adp-ribose) polymerase activity in response to dna damage
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6701155/
https://www.ncbi.nlm.nih.gov/pubmed/31426748
http://dx.doi.org/10.1186/s12870-019-1958-9
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