Genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of TOPLESS gene family members in tomato

Members of the TOPLESS gene family emerged recently as key players in gene repression in several mechanisms, especially in auxin perception. The TOPLESS genes constitute, in ‘higher-plant’ genomes, a small multigenic family comprising four to 11 members. In this study, this family was investigated i...

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Main Authors: Hao, Yanwei, Wang, Xinyu, Li, Xian, Bassa, Carole, Mila, Isabelle, Audran, Corinne, Maza, Elie, Li, Zhengguo, Bouzayen, Mondher, van der Rest, Benoit, Zouine, Mohamed
Format: Online
Language:English
Published: Oxford University Press 2014
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3935560/
id pubmed-3935560
recordtype oai_dc
spelling pubmed-39355602014-02-26 Genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of TOPLESS gene family members in tomato Hao, Yanwei Wang, Xinyu Li, Xian Bassa, Carole Mila, Isabelle Audran, Corinne Maza, Elie Li, Zhengguo Bouzayen, Mondher van der Rest, Benoit Zouine, Mohamed Research Paper Members of the TOPLESS gene family emerged recently as key players in gene repression in several mechanisms, especially in auxin perception. The TOPLESS genes constitute, in ‘higher-plant’ genomes, a small multigenic family comprising four to 11 members. In this study, this family was investigated in tomato, a model plant for Solanaceae species and fleshy fruits. Six open reading frames predicted to encode topless-like proteins (SlTPLs) containing the canonical domains (LisH, CTLH, and two WD40 repeats) were identified in the tomato genome. Nuclear localization was confirmed for all members of the SlTPL family with the exception SlTPL6, which localized at the cytoplasm and was excluded from the nucleus. SlTPL genes displayed distinctive expression patterns in different tomato organs, with SlTPL1 showing the highest levels of transcript accumulation in all tissues tested except in ripening fruit where SlTPL3 and SlTPL4 were the most prominently expressed. To gain insight into the specificity of the different TOPLESS paralogues, a protein–protein interaction map between TOPLESS and auxin/indole-3-acetic acid (Aux/IAA) proteins was built using a yeast two-hybrid approach. The PPI map enabled the distinction of two patterns: TOPLESS isoforms interacting with the majority of Aux/IAA, and isoforms with limited capacity for interaction with these protein partners. Interestingly, evolutionary analyses of the TOPLESS gene family revealed that the highly expressed isoforms (SlTPL1, SlTPL3, and SlTPL4) corresponded to the three TPL-related genes undergoing the strongest purifying selection, while the selection was much weaker for SlTPL6, which was expressed at a low level and encoded a protein lacking the capacity to interact with Aux/IAAs. Oxford University Press 2014-03 2014-01-07 /pmc/articles/PMC3935560/ /pubmed/24399174 http://dx.doi.org/10.1093/jxb/ert440 Text en © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Hao, Yanwei
Wang, Xinyu
Li, Xian
Bassa, Carole
Mila, Isabelle
Audran, Corinne
Maza, Elie
Li, Zhengguo
Bouzayen, Mondher
van der Rest, Benoit
Zouine, Mohamed
spellingShingle Hao, Yanwei
Wang, Xinyu
Li, Xian
Bassa, Carole
Mila, Isabelle
Audran, Corinne
Maza, Elie
Li, Zhengguo
Bouzayen, Mondher
van der Rest, Benoit
Zouine, Mohamed
Genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of TOPLESS gene family members in tomato
author_facet Hao, Yanwei
Wang, Xinyu
Li, Xian
Bassa, Carole
Mila, Isabelle
Audran, Corinne
Maza, Elie
Li, Zhengguo
Bouzayen, Mondher
van der Rest, Benoit
Zouine, Mohamed
author_sort Hao, Yanwei
title Genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of TOPLESS gene family members in tomato
title_short Genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of TOPLESS gene family members in tomato
title_full Genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of TOPLESS gene family members in tomato
title_fullStr Genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of TOPLESS gene family members in tomato
title_full_unstemmed Genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of TOPLESS gene family members in tomato
title_sort genome-wide identification, phylogenetic analysis, expression profiling, and protein–protein interaction properties of topless gene family members in tomato
description Members of the TOPLESS gene family emerged recently as key players in gene repression in several mechanisms, especially in auxin perception. The TOPLESS genes constitute, in ‘higher-plant’ genomes, a small multigenic family comprising four to 11 members. In this study, this family was investigated in tomato, a model plant for Solanaceae species and fleshy fruits. Six open reading frames predicted to encode topless-like proteins (SlTPLs) containing the canonical domains (LisH, CTLH, and two WD40 repeats) were identified in the tomato genome. Nuclear localization was confirmed for all members of the SlTPL family with the exception SlTPL6, which localized at the cytoplasm and was excluded from the nucleus. SlTPL genes displayed distinctive expression patterns in different tomato organs, with SlTPL1 showing the highest levels of transcript accumulation in all tissues tested except in ripening fruit where SlTPL3 and SlTPL4 were the most prominently expressed. To gain insight into the specificity of the different TOPLESS paralogues, a protein–protein interaction map between TOPLESS and auxin/indole-3-acetic acid (Aux/IAA) proteins was built using a yeast two-hybrid approach. The PPI map enabled the distinction of two patterns: TOPLESS isoforms interacting with the majority of Aux/IAA, and isoforms with limited capacity for interaction with these protein partners. Interestingly, evolutionary analyses of the TOPLESS gene family revealed that the highly expressed isoforms (SlTPL1, SlTPL3, and SlTPL4) corresponded to the three TPL-related genes undergoing the strongest purifying selection, while the selection was much weaker for SlTPL6, which was expressed at a low level and encoded a protein lacking the capacity to interact with Aux/IAAs.
publisher Oxford University Press
publishDate 2014
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3935560/
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