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Genome-Wide Identification and Function of Aquaporin Genes During Dormancy and Sprouting Periods of Kernel-Using Apricot (Prunus armeniaca L.)

Aquaporins (AQPs) are essential channel proteins that play a major role in plant growth and development, regulate plant water homeostasis, and transport uncharged solutes across biological membranes. In this study, 33 AQP genes were systematically identified from the kernel-using apricot (Prunus arm...

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Autores principales: Li, Shaofeng, Wang, Lin, Zhang, Yaoxiang, Zhu, Gaopu, Zhu, Xuchun, Xia, Yongxiu, Li, Jianbo, Gao, Xu, Wang, Shaoli, Zhang, Jianhui, Wuyun, Ta-na, Mo, Wenjuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8520955/
https://www.ncbi.nlm.nih.gov/pubmed/34671366
http://dx.doi.org/10.3389/fpls.2021.690040
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author Li, Shaofeng
Wang, Lin
Zhang, Yaoxiang
Zhu, Gaopu
Zhu, Xuchun
Xia, Yongxiu
Li, Jianbo
Gao, Xu
Wang, Shaoli
Zhang, Jianhui
Wuyun, Ta-na
Mo, Wenjuan
author_facet Li, Shaofeng
Wang, Lin
Zhang, Yaoxiang
Zhu, Gaopu
Zhu, Xuchun
Xia, Yongxiu
Li, Jianbo
Gao, Xu
Wang, Shaoli
Zhang, Jianhui
Wuyun, Ta-na
Mo, Wenjuan
author_sort Li, Shaofeng
collection PubMed
description Aquaporins (AQPs) are essential channel proteins that play a major role in plant growth and development, regulate plant water homeostasis, and transport uncharged solutes across biological membranes. In this study, 33 AQP genes were systematically identified from the kernel-using apricot (Prunus armeniaca L.) genome and divided into five subfamilies based on phylogenetic analyses. A total of 14 collinear blocks containing AQP genes between P. armeniaca and Arabidopsis thaliana were identified by synteny analysis, and 30 collinear blocks were identified between P. armeniaca and P. persica. Gene structure and conserved functional motif analyses indicated that the PaAQPs exhibit a conserved exon-intron pattern and that conserved motifs are present within members of each subfamily. Physiological mechanism prediction based on the aromatic/arginine selectivity filter, Froger’s positions, and three-dimensional (3D) protein model construction revealed marked differences in substrate specificity between the members of the five subfamilies of PaAQPs. Promoter analysis of the PaAQP genes for conserved regulatory elements suggested a greater abundance of cis-elements involved in light, hormone, and stress responses, which may reflect the differences in expression patterns of PaAQPs and their various functions associated with plant development and abiotic stress responses. Gene expression patterns of PaAQPs showed that PaPIP1-3, PaPIP2-1, and PaTIP1-1 were highly expressed in flower buds during the dormancy and sprouting stages of P. armeniaca. A PaAQP coexpression network showed that PaAQPs were coexpressed with 14 cold resistance genes and with 16 cold stress-associated genes. The expression pattern of 70% of the PaAQPs coexpressed with cold stress resistance genes was consistent with the four periods [Physiological dormancy (PD), ecological dormancy (ED), sprouting period (SP), and germination stage (GS)] of flower buds of P. armeniaca. Detection of the transient expression of GFP-tagged PaPIP1-1, PaPIP2-3, PaSIP1-3, PaXIP1-2, PaNIP6-1, and PaTIP1-1 revealed that the fusion proteins localized to the plasma membrane. Predictions of an A. thaliana ortholog-based protein–protein interaction network indicated that PaAQP proteins had complex relationships with the cold tolerance pathway, PaNIP6-1 could interact with WRKY6, PaTIP1-1 could interact with TSPO, and PaPIP2-1 could interact with ATHATPLC1G. Interestingly, overexpression of PaPIP1-3 and PaTIP1-1 increased the cold tolerance of and protein accumulation in yeast. Compared with wild-type plants, PaPIP1-3- and PaTIP1-1-overexpressing (OE) Arabidopsis plants exhibited greater tolerance to cold stress, as evidenced by better growth and greater antioxidative enzyme activities. Overall, our study provides insights into the interaction networks, expression patterns, and functional analysis of PaAQP genes in P. armeniaca L. and contributes to the further functional characterization of PaAQPs.
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spelling pubmed-85209552021-10-19 Genome-Wide Identification and Function of Aquaporin Genes During Dormancy and Sprouting Periods of Kernel-Using Apricot (Prunus armeniaca L.) Li, Shaofeng Wang, Lin Zhang, Yaoxiang Zhu, Gaopu Zhu, Xuchun Xia, Yongxiu Li, Jianbo Gao, Xu Wang, Shaoli Zhang, Jianhui Wuyun, Ta-na Mo, Wenjuan Front Plant Sci Plant Science Aquaporins (AQPs) are essential channel proteins that play a major role in plant growth and development, regulate plant water homeostasis, and transport uncharged solutes across biological membranes. In this study, 33 AQP genes were systematically identified from the kernel-using apricot (Prunus armeniaca L.) genome and divided into five subfamilies based on phylogenetic analyses. A total of 14 collinear blocks containing AQP genes between P. armeniaca and Arabidopsis thaliana were identified by synteny analysis, and 30 collinear blocks were identified between P. armeniaca and P. persica. Gene structure and conserved functional motif analyses indicated that the PaAQPs exhibit a conserved exon-intron pattern and that conserved motifs are present within members of each subfamily. Physiological mechanism prediction based on the aromatic/arginine selectivity filter, Froger’s positions, and three-dimensional (3D) protein model construction revealed marked differences in substrate specificity between the members of the five subfamilies of PaAQPs. Promoter analysis of the PaAQP genes for conserved regulatory elements suggested a greater abundance of cis-elements involved in light, hormone, and stress responses, which may reflect the differences in expression patterns of PaAQPs and their various functions associated with plant development and abiotic stress responses. Gene expression patterns of PaAQPs showed that PaPIP1-3, PaPIP2-1, and PaTIP1-1 were highly expressed in flower buds during the dormancy and sprouting stages of P. armeniaca. A PaAQP coexpression network showed that PaAQPs were coexpressed with 14 cold resistance genes and with 16 cold stress-associated genes. The expression pattern of 70% of the PaAQPs coexpressed with cold stress resistance genes was consistent with the four periods [Physiological dormancy (PD), ecological dormancy (ED), sprouting period (SP), and germination stage (GS)] of flower buds of P. armeniaca. Detection of the transient expression of GFP-tagged PaPIP1-1, PaPIP2-3, PaSIP1-3, PaXIP1-2, PaNIP6-1, and PaTIP1-1 revealed that the fusion proteins localized to the plasma membrane. Predictions of an A. thaliana ortholog-based protein–protein interaction network indicated that PaAQP proteins had complex relationships with the cold tolerance pathway, PaNIP6-1 could interact with WRKY6, PaTIP1-1 could interact with TSPO, and PaPIP2-1 could interact with ATHATPLC1G. Interestingly, overexpression of PaPIP1-3 and PaTIP1-1 increased the cold tolerance of and protein accumulation in yeast. Compared with wild-type plants, PaPIP1-3- and PaTIP1-1-overexpressing (OE) Arabidopsis plants exhibited greater tolerance to cold stress, as evidenced by better growth and greater antioxidative enzyme activities. Overall, our study provides insights into the interaction networks, expression patterns, and functional analysis of PaAQP genes in P. armeniaca L. and contributes to the further functional characterization of PaAQPs. Frontiers Media S.A. 2021-10-04 /pmc/articles/PMC8520955/ /pubmed/34671366 http://dx.doi.org/10.3389/fpls.2021.690040 Text en Copyright © 2021 Li, Wang, Zhang, Zhu, Zhu, Xia, Li, Gao, Wang, Zhang, Wuyun and Mo. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Li, Shaofeng
Wang, Lin
Zhang, Yaoxiang
Zhu, Gaopu
Zhu, Xuchun
Xia, Yongxiu
Li, Jianbo
Gao, Xu
Wang, Shaoli
Zhang, Jianhui
Wuyun, Ta-na
Mo, Wenjuan
Genome-Wide Identification and Function of Aquaporin Genes During Dormancy and Sprouting Periods of Kernel-Using Apricot (Prunus armeniaca L.)
title Genome-Wide Identification and Function of Aquaporin Genes During Dormancy and Sprouting Periods of Kernel-Using Apricot (Prunus armeniaca L.)
title_full Genome-Wide Identification and Function of Aquaporin Genes During Dormancy and Sprouting Periods of Kernel-Using Apricot (Prunus armeniaca L.)
title_fullStr Genome-Wide Identification and Function of Aquaporin Genes During Dormancy and Sprouting Periods of Kernel-Using Apricot (Prunus armeniaca L.)
title_full_unstemmed Genome-Wide Identification and Function of Aquaporin Genes During Dormancy and Sprouting Periods of Kernel-Using Apricot (Prunus armeniaca L.)
title_short Genome-Wide Identification and Function of Aquaporin Genes During Dormancy and Sprouting Periods of Kernel-Using Apricot (Prunus armeniaca L.)
title_sort genome-wide identification and function of aquaporin genes during dormancy and sprouting periods of kernel-using apricot (prunus armeniaca l.)
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8520955/
https://www.ncbi.nlm.nih.gov/pubmed/34671366
http://dx.doi.org/10.3389/fpls.2021.690040
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