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Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)

BACKGROUND: Polyploidy has played a major role in angiosperm evolution. Previous studies have examined polyploid phenotypes in comparison to their extant progenitors, but not in context of predicted progenitor phenotypes at allopolyploid origin. In addition, differences in the trends of polyploid ve...

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Autores principales: McCarthy, Elizabeth W., Landis, Jacob B., Kurti, Amelda, Lawhorn, Amber J., Chase, Mark W., Knapp, Sandra, Le Comber, Steven C., Leitch, Andrew R., Litt, Amy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6486959/
https://www.ncbi.nlm.nih.gov/pubmed/31029077
http://dx.doi.org/10.1186/s12870-019-1771-5
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author McCarthy, Elizabeth W.
Landis, Jacob B.
Kurti, Amelda
Lawhorn, Amber J.
Chase, Mark W.
Knapp, Sandra
Le Comber, Steven C.
Leitch, Andrew R.
Litt, Amy
author_facet McCarthy, Elizabeth W.
Landis, Jacob B.
Kurti, Amelda
Lawhorn, Amber J.
Chase, Mark W.
Knapp, Sandra
Le Comber, Steven C.
Leitch, Andrew R.
Litt, Amy
author_sort McCarthy, Elizabeth W.
collection PubMed
description BACKGROUND: Polyploidy has played a major role in angiosperm evolution. Previous studies have examined polyploid phenotypes in comparison to their extant progenitors, but not in context of predicted progenitor phenotypes at allopolyploid origin. In addition, differences in the trends of polyploid versus diploid evolution have not been investigated. We use ancestral character-state reconstructions to estimate progenitor phenotype at allopolyploid origin to determine patterns of polyploid evolution leading to morphology of the extant species. We also compare trends in diploid versus allopolyploid evolution to determine if polyploidy modifies floral evolutionary patterns. RESULTS: Predicting the ancestral phenotype of a nascent allopolyploid from reconstructions of diploid phenotypes at the time of polyploid formation generates different phenotype predictions than when extant diploid phenotypes are used, the outcome of which can alter conclusions about polyploid evolution; however, most analyses yield the same results. Using ancestral reconstructions of diploid floral phenotypes indicate that young polyploids evolve shorter, wider corolla tubes, but older polyploids and diploids do not show any detectable evolutionary trends. Lability of the traits examined (floral shape, corolla tube length, and corolla tube width) differs across young and older polyploids and diploids. Corolla length is more evolutionarily labile in older polyploids and diploids. Polyploids do not display unique suites of floral characters based on both morphological and color traits, but some suites of characters may be evolving together and seem to have arisen multiple times within Nicotiana, perhaps due to the influence of pollinators. CONCLUSIONS: Young polyploids display different trends in floral evolution (shorter, wider corolla tubes, which may result in more generalist pollination) than older polyploids and diploids, suggesting that patterns of divergence are impacted by the early consequences of allopolyploidy, perhaps arising from genomic shock and/or subsequent genome stabilization associated with diploidization. Convergent evolution in floral morphology and color in Nicotiana can be consistent with pollinator preferences, suggesting that pollinators may have shaped floral evolution in Nicotiana. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1771-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-64869592019-05-06 Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae) McCarthy, Elizabeth W. Landis, Jacob B. Kurti, Amelda Lawhorn, Amber J. Chase, Mark W. Knapp, Sandra Le Comber, Steven C. Leitch, Andrew R. Litt, Amy BMC Plant Biol Research Article BACKGROUND: Polyploidy has played a major role in angiosperm evolution. Previous studies have examined polyploid phenotypes in comparison to their extant progenitors, but not in context of predicted progenitor phenotypes at allopolyploid origin. In addition, differences in the trends of polyploid versus diploid evolution have not been investigated. We use ancestral character-state reconstructions to estimate progenitor phenotype at allopolyploid origin to determine patterns of polyploid evolution leading to morphology of the extant species. We also compare trends in diploid versus allopolyploid evolution to determine if polyploidy modifies floral evolutionary patterns. RESULTS: Predicting the ancestral phenotype of a nascent allopolyploid from reconstructions of diploid phenotypes at the time of polyploid formation generates different phenotype predictions than when extant diploid phenotypes are used, the outcome of which can alter conclusions about polyploid evolution; however, most analyses yield the same results. Using ancestral reconstructions of diploid floral phenotypes indicate that young polyploids evolve shorter, wider corolla tubes, but older polyploids and diploids do not show any detectable evolutionary trends. Lability of the traits examined (floral shape, corolla tube length, and corolla tube width) differs across young and older polyploids and diploids. Corolla length is more evolutionarily labile in older polyploids and diploids. Polyploids do not display unique suites of floral characters based on both morphological and color traits, but some suites of characters may be evolving together and seem to have arisen multiple times within Nicotiana, perhaps due to the influence of pollinators. CONCLUSIONS: Young polyploids display different trends in floral evolution (shorter, wider corolla tubes, which may result in more generalist pollination) than older polyploids and diploids, suggesting that patterns of divergence are impacted by the early consequences of allopolyploidy, perhaps arising from genomic shock and/or subsequent genome stabilization associated with diploidization. Convergent evolution in floral morphology and color in Nicotiana can be consistent with pollinator preferences, suggesting that pollinators may have shaped floral evolution in Nicotiana. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1771-5) contains supplementary material, which is available to authorized users. BioMed Central 2019-04-27 /pmc/articles/PMC6486959/ /pubmed/31029077 http://dx.doi.org/10.1186/s12870-019-1771-5 Text en © The Author(s). 2019 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
McCarthy, Elizabeth W.
Landis, Jacob B.
Kurti, Amelda
Lawhorn, Amber J.
Chase, Mark W.
Knapp, Sandra
Le Comber, Steven C.
Leitch, Andrew R.
Litt, Amy
Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)
title Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)
title_full Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)
title_fullStr Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)
title_full_unstemmed Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)
title_short Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)
title_sort early consequences of allopolyploidy alter floral evolution in nicotiana (solanaceae)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6486959/
https://www.ncbi.nlm.nih.gov/pubmed/31029077
http://dx.doi.org/10.1186/s12870-019-1771-5
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