How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae.

Comparative gene expression studies are invaluable for predicting how existing genetic pathways may be modified or redeployed to produce novel and variable phenotypes. Fruits are ecologically important organs because of their impact on plant fitness and seed dispersal, modifications in which results...

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Main Authors: Shane Carey, Kerrin Mendler, Jocelyn C Hall
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0209535
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spelling doaj-75349f96c80b4d2bb65d712f540541602021-03-03T20:34:11ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-01147e020953510.1371/journal.pone.0209535How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae.Shane CareyKerrin MendlerJocelyn C HallComparative gene expression studies are invaluable for predicting how existing genetic pathways may be modified or redeployed to produce novel and variable phenotypes. Fruits are ecologically important organs because of their impact on plant fitness and seed dispersal, modifications in which results in morphological variation across species. A novel fruit type in the Brassicaceae known as heteroarthrocarpy enables distinct dispersal methods in a single fruit through segmentation via a lateral joint and variable dehiscence at maturity. Given the close relationship to Arabidopsis, species that exhibit heteroarthrocarpy are powerful models to elucidate how differences in gene expression of a fruit patterning pathway may result in novel fruit types. Transcriptomes of distal, joint, and proximal regions from Erucaria erucarioides and Cakile lanceolata were analyzed to elucidate within fruit and between species differences in whole transcriptome, gene ontology, and fruit patterning expression profiles. Whole transcriptome expression profiles vary between fruit regions in patterns that are consistent with fruit anatomy. These transcriptomic variances do not correlate with changes in gene ontology, as they remain generally stable within and between both species. Upstream regulators in the fruit patterning pathway, FILAMENTOUS FLOWER and YABBY3, are expressed in the distal and proximal regions of E. erucarioides, but not in the joint, implicating alterations in the pathway in heteroarthrocarpic fruits. Downstream gene, INDEHISCENT, is significantly upregulated in the abscissing joint region of C. lanceolata, which suggests repurposing of valve margin genes for novel joint disarticulation in an otherwise indehiscent fruit. In summary, these data are consistent with modifications in fruit patterning genes producing heteroarthrocarpic fruits through different components of the pathway relative to other indehiscent, non-heteroarthrocarpic, species within the family. Our understanding of fruit development in Arabidopsis is now extended to atypical siliques within the Brassicaceae, facilitating future studies on seed shattering in important Brassicaceous crops and pernicious weeds.https://doi.org/10.1371/journal.pone.0209535
collection DOAJ
language English
format Article
sources DOAJ
author Shane Carey
Kerrin Mendler
Jocelyn C Hall
spellingShingle Shane Carey
Kerrin Mendler
Jocelyn C Hall
How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae.
PLoS ONE
author_facet Shane Carey
Kerrin Mendler
Jocelyn C Hall
author_sort Shane Carey
title How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae.
title_short How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae.
title_full How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae.
title_fullStr How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae.
title_full_unstemmed How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae.
title_sort how to build a fruit: transcriptomics of a novel fruit type in the brassiceae.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2019-01-01
description Comparative gene expression studies are invaluable for predicting how existing genetic pathways may be modified or redeployed to produce novel and variable phenotypes. Fruits are ecologically important organs because of their impact on plant fitness and seed dispersal, modifications in which results in morphological variation across species. A novel fruit type in the Brassicaceae known as heteroarthrocarpy enables distinct dispersal methods in a single fruit through segmentation via a lateral joint and variable dehiscence at maturity. Given the close relationship to Arabidopsis, species that exhibit heteroarthrocarpy are powerful models to elucidate how differences in gene expression of a fruit patterning pathway may result in novel fruit types. Transcriptomes of distal, joint, and proximal regions from Erucaria erucarioides and Cakile lanceolata were analyzed to elucidate within fruit and between species differences in whole transcriptome, gene ontology, and fruit patterning expression profiles. Whole transcriptome expression profiles vary between fruit regions in patterns that are consistent with fruit anatomy. These transcriptomic variances do not correlate with changes in gene ontology, as they remain generally stable within and between both species. Upstream regulators in the fruit patterning pathway, FILAMENTOUS FLOWER and YABBY3, are expressed in the distal and proximal regions of E. erucarioides, but not in the joint, implicating alterations in the pathway in heteroarthrocarpic fruits. Downstream gene, INDEHISCENT, is significantly upregulated in the abscissing joint region of C. lanceolata, which suggests repurposing of valve margin genes for novel joint disarticulation in an otherwise indehiscent fruit. In summary, these data are consistent with modifications in fruit patterning genes producing heteroarthrocarpic fruits through different components of the pathway relative to other indehiscent, non-heteroarthrocarpic, species within the family. Our understanding of fruit development in Arabidopsis is now extended to atypical siliques within the Brassicaceae, facilitating future studies on seed shattering in important Brassicaceous crops and pernicious weeds.
url https://doi.org/10.1371/journal.pone.0209535
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