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The pennycress (Thlaspi arvense L.) nectary: structural and transcriptomic characterization

BACKGROUND: Pennycress [Thlaspi arvense L (Brassicaceae)] is being domesticated as a renewable biodiesel feedstock that also provides crucial ecosystems services, including as a nutritional resource for pollinators. However, its flowers produce significantly less nectar than other crop relatives in...

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Autores principales: Thomas, Jason B., Hampton, Marshall E., Dorn, Kevin M., David Marks, M., Carter, Clay J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5686818/
https://www.ncbi.nlm.nih.gov/pubmed/29137608
http://dx.doi.org/10.1186/s12870-017-1146-8
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author Thomas, Jason B.
Hampton, Marshall E.
Dorn, Kevin M.
David Marks, M.
Carter, Clay J.
author_facet Thomas, Jason B.
Hampton, Marshall E.
Dorn, Kevin M.
David Marks, M.
Carter, Clay J.
author_sort Thomas, Jason B.
collection PubMed
description BACKGROUND: Pennycress [Thlaspi arvense L (Brassicaceae)] is being domesticated as a renewable biodiesel feedstock that also provides crucial ecosystems services, including as a nutritional resource for pollinators. However, its flowers produce significantly less nectar than other crop relatives in the Brassicaceae. This study was undertaken to understand the basic biology of the pennycress nectary as an initial step toward the possibility of enhancing nectar output from its flowers. RESULTS: Pennycress flowers contain four equivalent nectaries located extrastaminally at the base of the insertion sites of short and long stamens. Like other Brassicaceae, the nectaries have open stomates on their surface, which likely serve as the sites of nectar secretion. The nectaries produce four distinct nectar droplets that accumulate in concave structures at the base of each of the four petals. To understand the molecular biology of the pennycress nectary, RNA was isolated from ‘immature’ (pre-secretory) and ‘mature’ (secretory) nectaries and subjected to RNA-seq. Approximately 184 M paired-end reads (368 M total reads) were de novo assembled into a total of 16,074 independent contigs, which mapped to 12,335 unique genes in the pennycress genome. Nearly 3700 genes were found to be differentially expressed between immature and mature nectaries and subjected to gene ontology and metabolic pathway analyses. Lastly, in silico analyses identified 158 pennycress orthologs to Arabidopsis genes with known enriched expression in nectaries. These nectary-enriched expression patterns were verified for select pennycress loci by semi-quantitative RT-PCR. CONCLUSIONS: Pennycress nectaries are unique relative to those of other agriculturally important Brassicaceae, as they contain four equivalent nectaries that present their nectar in specialized cup-shaped structures at the base of the petals. In spite of these morphological differences, the genes underlying the regulation and production of nectar appear to be largely conserved between pennycress and Arabidopsis thaliana. These results provide a starting point for using forward and reverse genetics approaches to enhance nectar synthesis and secretion in pennycress. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-017-1146-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-56868182017-11-21 The pennycress (Thlaspi arvense L.) nectary: structural and transcriptomic characterization Thomas, Jason B. Hampton, Marshall E. Dorn, Kevin M. David Marks, M. Carter, Clay J. BMC Plant Biol Research Article BACKGROUND: Pennycress [Thlaspi arvense L (Brassicaceae)] is being domesticated as a renewable biodiesel feedstock that also provides crucial ecosystems services, including as a nutritional resource for pollinators. However, its flowers produce significantly less nectar than other crop relatives in the Brassicaceae. This study was undertaken to understand the basic biology of the pennycress nectary as an initial step toward the possibility of enhancing nectar output from its flowers. RESULTS: Pennycress flowers contain four equivalent nectaries located extrastaminally at the base of the insertion sites of short and long stamens. Like other Brassicaceae, the nectaries have open stomates on their surface, which likely serve as the sites of nectar secretion. The nectaries produce four distinct nectar droplets that accumulate in concave structures at the base of each of the four petals. To understand the molecular biology of the pennycress nectary, RNA was isolated from ‘immature’ (pre-secretory) and ‘mature’ (secretory) nectaries and subjected to RNA-seq. Approximately 184 M paired-end reads (368 M total reads) were de novo assembled into a total of 16,074 independent contigs, which mapped to 12,335 unique genes in the pennycress genome. Nearly 3700 genes were found to be differentially expressed between immature and mature nectaries and subjected to gene ontology and metabolic pathway analyses. Lastly, in silico analyses identified 158 pennycress orthologs to Arabidopsis genes with known enriched expression in nectaries. These nectary-enriched expression patterns were verified for select pennycress loci by semi-quantitative RT-PCR. CONCLUSIONS: Pennycress nectaries are unique relative to those of other agriculturally important Brassicaceae, as they contain four equivalent nectaries that present their nectar in specialized cup-shaped structures at the base of the petals. In spite of these morphological differences, the genes underlying the regulation and production of nectar appear to be largely conserved between pennycress and Arabidopsis thaliana. These results provide a starting point for using forward and reverse genetics approaches to enhance nectar synthesis and secretion in pennycress. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-017-1146-8) contains supplementary material, which is available to authorized users. BioMed Central 2017-11-14 /pmc/articles/PMC5686818/ /pubmed/29137608 http://dx.doi.org/10.1186/s12870-017-1146-8 Text en © The Author(s). 2017 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
Thomas, Jason B.
Hampton, Marshall E.
Dorn, Kevin M.
David Marks, M.
Carter, Clay J.
The pennycress (Thlaspi arvense L.) nectary: structural and transcriptomic characterization
title The pennycress (Thlaspi arvense L.) nectary: structural and transcriptomic characterization
title_full The pennycress (Thlaspi arvense L.) nectary: structural and transcriptomic characterization
title_fullStr The pennycress (Thlaspi arvense L.) nectary: structural and transcriptomic characterization
title_full_unstemmed The pennycress (Thlaspi arvense L.) nectary: structural and transcriptomic characterization
title_short The pennycress (Thlaspi arvense L.) nectary: structural and transcriptomic characterization
title_sort pennycress (thlaspi arvense l.) nectary: structural and transcriptomic characterization
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5686818/
https://www.ncbi.nlm.nih.gov/pubmed/29137608
http://dx.doi.org/10.1186/s12870-017-1146-8
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