Evolution of the SPATULA/ALCATRAZ gene lineage and expression analyses in the basal eudicot, Bocconia frutescens L. (Papaveraceae)

Abstract Background SPATULA (SPT) and ALCATRAZ (ALC) are recent paralogs that belong to the large bHLH transcription factor family. Orthologs of these genes have been found in all core eudicots, whereas pre-duplication genes, named paleoSPATULA/ALCATRAZ, have been found in basal eudicots, monocots,...

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Main Authors: Cecilia Zumajo-Cardona, Barbara Ann Ambrose, Natalia Pabón-Mora
Format: Article
Language:English
Published: BMC 2017-03-01
Series:EvoDevo
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13227-017-0068-8
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spelling doaj-15c29a8f8e044e8c97f6610b969a903d2020-11-24T21:15:30ZengBMCEvoDevo2041-91392017-03-018111810.1186/s13227-017-0068-8Evolution of the SPATULA/ALCATRAZ gene lineage and expression analyses in the basal eudicot, Bocconia frutescens L. (Papaveraceae)Cecilia Zumajo-Cardona0Barbara Ann Ambrose1Natalia Pabón-Mora2Instituto de Biología, Universidad de AntioquiaNew York Botanical GardenInstituto de Biología, Universidad de AntioquiaAbstract Background SPATULA (SPT) and ALCATRAZ (ALC) are recent paralogs that belong to the large bHLH transcription factor family. Orthologs of these genes have been found in all core eudicots, whereas pre-duplication genes, named paleoSPATULA/ALCATRAZ, have been found in basal eudicots, monocots, basal angiosperms and gymnosperms. Nevertheless, functional studies have only been performed in Arabidopsis thaliana, where SPT and ALC are partially redundant in carpel and valve margin development and ALC has a unique role in the dehiscence zone. Further analyses of pre-duplication genes are necessary to assess the functional evolution of this gene lineage. Results We isolated additional paleoSPT/ALC genes from Aristolochia fimbriata, Bocconia frutescens, Cattleya trianae and Hypoxis decumbens from our transcriptome libraries and performed phylogenetic analyses. We identified the previously described bHLH domain in all analyzed sequences and also new conserved motifs using the MEME suite. Finally, we analyzed the expression of three paleoSPT/ALC genes (BofrSPT1/2/3) from Bocconia frutescens, a basal eudicot in the Papaveraceae. To determine the developmental stages at which these genes were expressed, pre- and post-anthesis carpels and fruits of B. frutescens were collected, sectioned, stained, and examined using light microscopy. Using in situ hybridization we detected that BofrSPT1/2/3 genes are expressed in floral buds, early sepal initiation, stamens and carpel primordia and later during fruit development in the dehiscence zone of the opercular fruit. Conclusions Our expression results, in comparison with those available for core eudicots, suggest conserved roles of members of the SPT/ALC gene lineage across eudicots in the specification of carpel margins and the dehiscence zone of the mature fruits. Although there is some redundancy between ALC and SPT, these gene clades seem to have undergone some degree of sub-functionalization in the core eudicots, likely by changes in cis regulatory regions and to some extent in coding sequences, at least in Brassicaceae. Our results also indicate that in Bocconia frutescens, paleoSPT/ALC genes may play a role in early floral organ specification that was subsequently lost in core eudicot lineages.http://link.springer.com/article/10.1186/s13227-017-0068-8ALCATRAZBasal eudicotsBocconia frutescensFruit developmentpaleoSPT/ALCPapaveraceae
collection DOAJ
language English
format Article
sources DOAJ
author Cecilia Zumajo-Cardona
Barbara Ann Ambrose
Natalia Pabón-Mora
spellingShingle Cecilia Zumajo-Cardona
Barbara Ann Ambrose
Natalia Pabón-Mora
Evolution of the SPATULA/ALCATRAZ gene lineage and expression analyses in the basal eudicot, Bocconia frutescens L. (Papaveraceae)
EvoDevo
ALCATRAZ
Basal eudicots
Bocconia frutescens
Fruit development
paleoSPT/ALC
Papaveraceae
author_facet Cecilia Zumajo-Cardona
Barbara Ann Ambrose
Natalia Pabón-Mora
author_sort Cecilia Zumajo-Cardona
title Evolution of the SPATULA/ALCATRAZ gene lineage and expression analyses in the basal eudicot, Bocconia frutescens L. (Papaveraceae)
title_short Evolution of the SPATULA/ALCATRAZ gene lineage and expression analyses in the basal eudicot, Bocconia frutescens L. (Papaveraceae)
title_full Evolution of the SPATULA/ALCATRAZ gene lineage and expression analyses in the basal eudicot, Bocconia frutescens L. (Papaveraceae)
title_fullStr Evolution of the SPATULA/ALCATRAZ gene lineage and expression analyses in the basal eudicot, Bocconia frutescens L. (Papaveraceae)
title_full_unstemmed Evolution of the SPATULA/ALCATRAZ gene lineage and expression analyses in the basal eudicot, Bocconia frutescens L. (Papaveraceae)
title_sort evolution of the spatula/alcatraz gene lineage and expression analyses in the basal eudicot, bocconia frutescens l. (papaveraceae)
publisher BMC
series EvoDevo
issn 2041-9139
publishDate 2017-03-01
description Abstract Background SPATULA (SPT) and ALCATRAZ (ALC) are recent paralogs that belong to the large bHLH transcription factor family. Orthologs of these genes have been found in all core eudicots, whereas pre-duplication genes, named paleoSPATULA/ALCATRAZ, have been found in basal eudicots, monocots, basal angiosperms and gymnosperms. Nevertheless, functional studies have only been performed in Arabidopsis thaliana, where SPT and ALC are partially redundant in carpel and valve margin development and ALC has a unique role in the dehiscence zone. Further analyses of pre-duplication genes are necessary to assess the functional evolution of this gene lineage. Results We isolated additional paleoSPT/ALC genes from Aristolochia fimbriata, Bocconia frutescens, Cattleya trianae and Hypoxis decumbens from our transcriptome libraries and performed phylogenetic analyses. We identified the previously described bHLH domain in all analyzed sequences and also new conserved motifs using the MEME suite. Finally, we analyzed the expression of three paleoSPT/ALC genes (BofrSPT1/2/3) from Bocconia frutescens, a basal eudicot in the Papaveraceae. To determine the developmental stages at which these genes were expressed, pre- and post-anthesis carpels and fruits of B. frutescens were collected, sectioned, stained, and examined using light microscopy. Using in situ hybridization we detected that BofrSPT1/2/3 genes are expressed in floral buds, early sepal initiation, stamens and carpel primordia and later during fruit development in the dehiscence zone of the opercular fruit. Conclusions Our expression results, in comparison with those available for core eudicots, suggest conserved roles of members of the SPT/ALC gene lineage across eudicots in the specification of carpel margins and the dehiscence zone of the mature fruits. Although there is some redundancy between ALC and SPT, these gene clades seem to have undergone some degree of sub-functionalization in the core eudicots, likely by changes in cis regulatory regions and to some extent in coding sequences, at least in Brassicaceae. Our results also indicate that in Bocconia frutescens, paleoSPT/ALC genes may play a role in early floral organ specification that was subsequently lost in core eudicot lineages.
topic ALCATRAZ
Basal eudicots
Bocconia frutescens
Fruit development
paleoSPT/ALC
Papaveraceae
url http://link.springer.com/article/10.1186/s13227-017-0068-8
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