Cargando…

Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)

Background and Aims The coexistence of hermaphrodites and female-sterile individuals, or androdioecy, has been documented in only a handful of plants and animals. This study reports its existence in the plant species Cardamine amara (Brassicaceae), in which female-sterile individuals have shorter pi...

Descripción completa

Detalles Bibliográficos
Autores principales: Tedder, Andrew, Helling, Matthias, Pannell, John R., Shimizu-Inatsugi, Rie, Kawagoe, Tetsuhiro, van Campen, Julia, Sese, Jun, Shimizu, Kentaro K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4373288/
https://www.ncbi.nlm.nih.gov/pubmed/25776435
http://dx.doi.org/10.1093/aob/mcv006
_version_ 1782363317340209152
author Tedder, Andrew
Helling, Matthias
Pannell, John R.
Shimizu-Inatsugi, Rie
Kawagoe, Tetsuhiro
van Campen, Julia
Sese, Jun
Shimizu, Kentaro K.
author_facet Tedder, Andrew
Helling, Matthias
Pannell, John R.
Shimizu-Inatsugi, Rie
Kawagoe, Tetsuhiro
van Campen, Julia
Sese, Jun
Shimizu, Kentaro K.
author_sort Tedder, Andrew
collection PubMed
description Background and Aims The coexistence of hermaphrodites and female-sterile individuals, or androdioecy, has been documented in only a handful of plants and animals. This study reports its existence in the plant species Cardamine amara (Brassicaceae), in which female-sterile individuals have shorter pistils than seed-producing hermaphrodites. Methods Morphological analysis, in situ manual pollination, microsatellite genotyping and differential gene expression analysis using Arabidopsis microarrays were used to delimit variation between female-sterile individuals and hermaphrodites. Key Results Female sterility in C. amara appears to be caused by disrupted ovule development. It was associated with a 2.4- to 2.9-fold increase in clonal propagation. This made the pollen number of female-sterile genets more than double that of hermaphrodite genets, which fulfils a condition of co-existence predicted by simple androdioecy theories. When female-sterile individuals were observed in wild androdioecious populations, their ramet frequencies ranged from 5 to 54 %; however, their genet frequencies ranged from 11 to 29 %, which is consistent with the theoretically predicted upper limit of 50 %. Conclusions The results suggest that a combination of sexual reproduction and increased asexual proliferation by female-sterile individuals probably explains the invasion and maintenance of female sterility in otherwise hermaphroditic populations. To our knowledge, this is the first report of the coexistence of female sterility and hermaphrodites in the Brassicaceae.
format Online
Article
Text
id pubmed-4373288
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-43732882015-03-26 Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae) Tedder, Andrew Helling, Matthias Pannell, John R. Shimizu-Inatsugi, Rie Kawagoe, Tetsuhiro van Campen, Julia Sese, Jun Shimizu, Kentaro K. Ann Bot Original Articles Background and Aims The coexistence of hermaphrodites and female-sterile individuals, or androdioecy, has been documented in only a handful of plants and animals. This study reports its existence in the plant species Cardamine amara (Brassicaceae), in which female-sterile individuals have shorter pistils than seed-producing hermaphrodites. Methods Morphological analysis, in situ manual pollination, microsatellite genotyping and differential gene expression analysis using Arabidopsis microarrays were used to delimit variation between female-sterile individuals and hermaphrodites. Key Results Female sterility in C. amara appears to be caused by disrupted ovule development. It was associated with a 2.4- to 2.9-fold increase in clonal propagation. This made the pollen number of female-sterile genets more than double that of hermaphrodite genets, which fulfils a condition of co-existence predicted by simple androdioecy theories. When female-sterile individuals were observed in wild androdioecious populations, their ramet frequencies ranged from 5 to 54 %; however, their genet frequencies ranged from 11 to 29 %, which is consistent with the theoretically predicted upper limit of 50 %. Conclusions The results suggest that a combination of sexual reproduction and increased asexual proliferation by female-sterile individuals probably explains the invasion and maintenance of female sterility in otherwise hermaphroditic populations. To our knowledge, this is the first report of the coexistence of female sterility and hermaphrodites in the Brassicaceae. Oxford University Press 2015-04 2015-03-16 /pmc/articles/PMC4373288/ /pubmed/25776435 http://dx.doi.org/10.1093/aob/mcv006 Text en © The Author 2015. Published by Oxford University Press on behalf of the Annals of Botany Company http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Tedder, Andrew
Helling, Matthias
Pannell, John R.
Shimizu-Inatsugi, Rie
Kawagoe, Tetsuhiro
van Campen, Julia
Sese, Jun
Shimizu, Kentaro K.
Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)
title Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)
title_full Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)
title_fullStr Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)
title_full_unstemmed Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)
title_short Female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of Cardamine amara (Brassicaceae)
title_sort female sterility associated with increased clonal propagation suggests a unique combination of androdioecy and asexual reproduction in populations of cardamine amara (brassicaceae)
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4373288/
https://www.ncbi.nlm.nih.gov/pubmed/25776435
http://dx.doi.org/10.1093/aob/mcv006
work_keys_str_mv AT tedderandrew femalesterilityassociatedwithincreasedclonalpropagationsuggestsauniquecombinationofandrodioecyandasexualreproductioninpopulationsofcardamineamarabrassicaceae
AT hellingmatthias femalesterilityassociatedwithincreasedclonalpropagationsuggestsauniquecombinationofandrodioecyandasexualreproductioninpopulationsofcardamineamarabrassicaceae
AT pannelljohnr femalesterilityassociatedwithincreasedclonalpropagationsuggestsauniquecombinationofandrodioecyandasexualreproductioninpopulationsofcardamineamarabrassicaceae
AT shimizuinatsugirie femalesterilityassociatedwithincreasedclonalpropagationsuggestsauniquecombinationofandrodioecyandasexualreproductioninpopulationsofcardamineamarabrassicaceae
AT kawagoetetsuhiro femalesterilityassociatedwithincreasedclonalpropagationsuggestsauniquecombinationofandrodioecyandasexualreproductioninpopulationsofcardamineamarabrassicaceae
AT vancampenjulia femalesterilityassociatedwithincreasedclonalpropagationsuggestsauniquecombinationofandrodioecyandasexualreproductioninpopulationsofcardamineamarabrassicaceae
AT sesejun femalesterilityassociatedwithincreasedclonalpropagationsuggestsauniquecombinationofandrodioecyandasexualreproductioninpopulationsofcardamineamarabrassicaceae
AT shimizukentarok femalesterilityassociatedwithincreasedclonalpropagationsuggestsauniquecombinationofandrodioecyandasexualreproductioninpopulationsofcardamineamarabrassicaceae