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Plant adaptive radiation mediated by polyploid plasticity in transcriptomes


Shimizu-Inatsugi, Rie; Terada, Aika; Hirose, Kyosuke; Kudoh, Hiroshi; Sese, Jun; Shimizu, Kentaro K (2016). Plant adaptive radiation mediated by polyploid plasticity in transcriptomes. Molecular Ecology:1-35.

Abstract

The habitats of polyploid species are generally distinct from their parental species. Stebbins described polyploids as “general purpose genotypes,” which can tolerate a wide range of environmental conditions. However, little is known about its molecular basis because of the complexity of polyploid genomes. We hypothesized that allopolyploid species might utilize the expression patterns of both parents depending on environments (polyploid plasticity hypothesis). We focused on hydrological niche segregation along fine-scale soil-moisture and waterlogging gradients. Two diploid species, Cardamine amara and C. hirsuta, grew best in submerged and unsubmerged conditions, respectively, consistent with their natural habitats. Interestingly, the allotetraploid C. flexuosa derived from them grew similarly in fluctuating as well as submerged and unsubmerged conditions, consistent with its wide environmental tolerance. A similar pattern was found in another species trio: allotetraploid C. scutata and its parents. Using the close relatedness of Cardamine and Arabidopsis, we quantified genome-wide expression patterns following dry and wet treatments using an Arabidopsis microarray. Hierarchical clustering analysis revealed that the expression pattern of C. flexuosa clustered with C. hirsuta in the dry condition and with C. amara in the wet condition, supporting our hypothesis. Furthermore, the induction levels of most genes in the allopolyploid were lower than in a specialist diploid species. This reflects a disadvantage of being allopolyploid arising from fixed heterozygosity. We propose that recurrent allopolyploid speciation along soil-moisture and waterlogging gradients confers niche differentiation and reproductive isolation simultaneously, and serves as a model for studying the molecular basis of ecological speciation and adaptive radiation.

Abstract

The habitats of polyploid species are generally distinct from their parental species. Stebbins described polyploids as “general purpose genotypes,” which can tolerate a wide range of environmental conditions. However, little is known about its molecular basis because of the complexity of polyploid genomes. We hypothesized that allopolyploid species might utilize the expression patterns of both parents depending on environments (polyploid plasticity hypothesis). We focused on hydrological niche segregation along fine-scale soil-moisture and waterlogging gradients. Two diploid species, Cardamine amara and C. hirsuta, grew best in submerged and unsubmerged conditions, respectively, consistent with their natural habitats. Interestingly, the allotetraploid C. flexuosa derived from them grew similarly in fluctuating as well as submerged and unsubmerged conditions, consistent with its wide environmental tolerance. A similar pattern was found in another species trio: allotetraploid C. scutata and its parents. Using the close relatedness of Cardamine and Arabidopsis, we quantified genome-wide expression patterns following dry and wet treatments using an Arabidopsis microarray. Hierarchical clustering analysis revealed that the expression pattern of C. flexuosa clustered with C. hirsuta in the dry condition and with C. amara in the wet condition, supporting our hypothesis. Furthermore, the induction levels of most genes in the allopolyploid were lower than in a specialist diploid species. This reflects a disadvantage of being allopolyploid arising from fixed heterozygosity. We propose that recurrent allopolyploid speciation along soil-moisture and waterlogging gradients confers niche differentiation and reproductive isolation simultaneously, and serves as a model for studying the molecular basis of ecological speciation and adaptive radiation.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > Functional Genomics Center Zurich
07 Faculty of Science > Department of Plant and Microbial Biology
07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
08 University Research Priority Programs > Systems Biology / Functional Genomics
08 University Research Priority Programs > Evolution in Action: From Genomes to Ecosystems
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Language:English
Date:2016
Deposited On:05 Jul 2016 12:41
Last Modified:01 Jun 2017 00:00
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:0962-1083
Publisher DOI:https://doi.org/10.1111/mec.13738

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Licence: Creative Commons: Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)

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