PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity

Abstract 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...

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Main Authors: Suzanne de Bruijn, Tao Zhao, Jose M. Muiño, Eric M. Schranz, Gerco C. Angenent, Kerstin Kaufmann
Format: Article
Language:English
Published: BMC 2018-12-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-018-1574-0
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author Suzanne de Bruijn
Tao Zhao
Jose M. Muiño
Eric M. Schranz
Gerco C. Angenent
Kerstin Kaufmann
author_facet Suzanne de Bruijn
Tao Zhao
Jose M. Muiño
Eric M. Schranz
Gerco C. Angenent
Kerstin Kaufmann
author_sort Suzanne de Bruijn
collection DOAJ
description Abstract 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.
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spelling doaj.art-03da130c9c8c4f859ec26b0909a083822022-12-21T18:16:07ZengBMCBMC Plant Biology1471-22292018-12-0118111810.1186/s12870-018-1574-0PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificitySuzanne de Bruijn0Tao Zhao1Jose M. Muiño2Eric M. Schranz3Gerco C. Angenent4Kerstin Kaufmann5Laboratory of Molecular Biology, Wageningen UniversityBiosystematics Group, Wageningen UniversityInstitute for Biology, Systems Biology of Gene Regulation, Humboldt-Universität zu BerlinBiosystematics Group, Wageningen UniversityLaboratory of Molecular Biology, Wageningen UniversityInstitute for Biology, Plant Cell and Molecular Biology, Humboldt-Universität zu BerlinAbstract 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.http://link.springer.com/article/10.1186/s12870-018-1574-0PISTILLATAFlower developmentGene duplicationsParalogsMADSTarenaya
spellingShingle Suzanne de Bruijn
Tao Zhao
Jose M. Muiño
Eric M. Schranz
Gerco C. Angenent
Kerstin Kaufmann
PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
BMC Plant Biology
PISTILLATA
Flower development
Gene duplications
Paralogs
MADS
Tarenaya
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 PISTILLATA
Flower development
Gene duplications
Paralogs
MADS
Tarenaya
url http://link.springer.com/article/10.1186/s12870-018-1574-0
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