Cargando…

PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity

BACKGROUND: Floral organs are specified by MADS-domain transcription factors that act in a combinatorial manner, as summarized in the (A)BCE model. However, this evolutionarily conserved model is in contrast to a remarkable amount of morphological diversity in flowers. One of the mechanisms suggeste...

Descripción completa

Detalles Bibliográficos
Autores principales: de Bruijn, Suzanne, Zhao, Tao, Muiño, Jose M., Schranz, Eric M., Angenent, Gerco C., Kaufmann, Kerstin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6303913/
https://www.ncbi.nlm.nih.gov/pubmed/30577806
http://dx.doi.org/10.1186/s12870-018-1574-0
_version_ 1783382255605907456
author de Bruijn, Suzanne
Zhao, Tao
Muiño, Jose M.
Schranz, Eric M.
Angenent, Gerco C.
Kaufmann, Kerstin
author_facet de Bruijn, Suzanne
Zhao, Tao
Muiño, Jose M.
Schranz, Eric M.
Angenent, Gerco C.
Kaufmann, Kerstin
author_sort de Bruijn, Suzanne
collection PubMed
description BACKGROUND: Floral organs are specified by MADS-domain transcription factors that act in a combinatorial manner, as summarized in the (A)BCE model. However, this evolutionarily conserved model is in contrast to a remarkable amount of morphological diversity in flowers. One of the mechanisms suggested to contribute to this diversity is duplication of floral MADS-domain transcription factors. Although gene duplication is often followed by loss of one of the copies, sometimes both copies are retained. If both copies are retained they will initially be redundant, providing freedom for one of the paralogs to change function. Here, we examine the evolutionary fate and functional consequences of a transposition event at the base of the Brassicales that resulted in the duplication of the floral regulator PISTILLATA (PI), using Tarenaya hassleriana (Cleomaceae) as a model system. RESULTS: The transposition of a genomic region containing a PI gene led to two paralogs which are located at different positions in the genome. The original PI copy is syntenic in position with most angiosperms, whereas the transposed copy is syntenic with the PI genes in Brassicaceae. The two PI paralogs of T. hassleriana have very similar expression patterns. However, they may have diverged in function, as only one of these PI proteins was able to act heterologously in the first whorl of A. thaliana flowers. We also observed differences in protein complex formation between the two paralogs, and the two paralogs exhibit subtle differences in DNA-binding specificity. Sequence analysis indicates that most of the protein sequence divergence between the two T. hassleriana paralogs emerged in a common ancestor of the Cleomaceae and the Brassicaceae. CONCLUSIONS: We found that the PI paralogs in T. hassleriana have similar expression patterns, but may have diverged at the level of protein function. Data suggest that most protein sequence divergence occurred rapidly, prior to the origin of the Brassicaceae and Cleomaceae. It is tempting to speculate that the interaction specificities of the Brassicaceae-specific PI proteins are different compared to the PI found in other angiosperms. This could lead to PI regulating partly different genes in the Brassicaceae, and ultimately might result in change floral in morphology. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1574-0) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6303913
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-63039132018-12-31 PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity de Bruijn, Suzanne Zhao, Tao Muiño, Jose M. Schranz, Eric M. Angenent, Gerco C. Kaufmann, Kerstin BMC Plant Biol Research Article BACKGROUND: Floral organs are specified by MADS-domain transcription factors that act in a combinatorial manner, as summarized in the (A)BCE model. However, this evolutionarily conserved model is in contrast to a remarkable amount of morphological diversity in flowers. One of the mechanisms suggested to contribute to this diversity is duplication of floral MADS-domain transcription factors. Although gene duplication is often followed by loss of one of the copies, sometimes both copies are retained. If both copies are retained they will initially be redundant, providing freedom for one of the paralogs to change function. Here, we examine the evolutionary fate and functional consequences of a transposition event at the base of the Brassicales that resulted in the duplication of the floral regulator PISTILLATA (PI), using Tarenaya hassleriana (Cleomaceae) as a model system. RESULTS: The transposition of a genomic region containing a PI gene led to two paralogs which are located at different positions in the genome. The original PI copy is syntenic in position with most angiosperms, whereas the transposed copy is syntenic with the PI genes in Brassicaceae. The two PI paralogs of T. hassleriana have very similar expression patterns. However, they may have diverged in function, as only one of these PI proteins was able to act heterologously in the first whorl of A. thaliana flowers. We also observed differences in protein complex formation between the two paralogs, and the two paralogs exhibit subtle differences in DNA-binding specificity. Sequence analysis indicates that most of the protein sequence divergence between the two T. hassleriana paralogs emerged in a common ancestor of the Cleomaceae and the Brassicaceae. CONCLUSIONS: We found that the PI paralogs in T. hassleriana have similar expression patterns, but may have diverged at the level of protein function. Data suggest that most protein sequence divergence occurred rapidly, prior to the origin of the Brassicaceae and Cleomaceae. It is tempting to speculate that the interaction specificities of the Brassicaceae-specific PI proteins are different compared to the PI found in other angiosperms. This could lead to PI regulating partly different genes in the Brassicaceae, and ultimately might result in change floral in morphology. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1574-0) contains supplementary material, which is available to authorized users. BioMed Central 2018-12-22 /pmc/articles/PMC6303913/ /pubmed/30577806 http://dx.doi.org/10.1186/s12870-018-1574-0 Text en © The Author(s). 2018 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
de Bruijn, Suzanne
Zhao, Tao
Muiño, Jose M.
Schranz, Eric M.
Angenent, Gerco C.
Kaufmann, Kerstin
PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_full PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_fullStr PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_full_unstemmed PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_short PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_sort pistillata paralogs in tarenaya hassleriana have diverged in interaction specificity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6303913/
https://www.ncbi.nlm.nih.gov/pubmed/30577806
http://dx.doi.org/10.1186/s12870-018-1574-0
work_keys_str_mv AT debruijnsuzanne pistillataparalogsintarenayahasslerianahavedivergedininteractionspecificity
AT zhaotao pistillataparalogsintarenayahasslerianahavedivergedininteractionspecificity
AT muinojosem pistillataparalogsintarenayahasslerianahavedivergedininteractionspecificity
AT schranzericm pistillataparalogsintarenayahasslerianahavedivergedininteractionspecificity
AT angenentgercoc pistillataparalogsintarenayahasslerianahavedivergedininteractionspecificity
AT kaufmannkerstin pistillataparalogsintarenayahasslerianahavedivergedininteractionspecificity