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Experimental and Field Data Support Range Expansion in an Allopolyploid Arabidopsis Owing to Parental Legacy of Heavy Metal Hyperaccumulation


Paape, Timothy; Akiyama, Reiko; Cereghetti, Teo; Onda, Yoshihiko; Hirao, Akira S; Kenta, Tanaka; Shimizu, Kentaro K (2020). Experimental and Field Data Support Range Expansion in an Allopolyploid Arabidopsis Owing to Parental Legacy of Heavy Metal Hyperaccumulation. Frontiers in Genetics, 11:1162.

Abstract

Empirical evidence is limited on whether allopolyploid species combine or merge parental adaptations to broaden habitats. The allopolyploid Arabidopsis kamchatica is a hybrid of the two diploid parents Arabidopsis halleri and Arabidopsis lyrata. A. halleri is a facultative heavy metal hyperaccumulator, and may be found in cadmium (Cd) and zinc (Zn) contaminated environments, as well as non-contaminated environments. A. lyrata is considered non-tolerant to these metals, but can be found in serpentine habitats. Therefore, the parents have adaptation to different environments. Here, we measured heavy metals in soils from native populations of A. kamchatica. We found that soil Zn concentration of nearly half of the sampled 40 sites was higher than the critical toxicity level. Many of the sites were near human construction, suggesting adaptation of A. kamchatica to artificially contaminated soils. Over half of the A. kamchatica populations had >1,000 μg g–1 Zn in leaf tissues. Using hydroponic treatments, most genotypes accumulated >3,000 μg g–1 Zn, with high variability among them, indicating substantial genetic variation in heavy metal accumulation. Genes involved in heavy metal hyperaccumulation showed an expression bias in the A. halleri-derived homeolog in widely distributed plant genotypes. We also found that two populations were found growing on serpentine soils. These data suggest that A. kamchatica can inhabit a range of both natural and artificial soil environments with high levels of ions that either of the parents specializes and that it can accumulate varying amount of heavy metals. Our field and experimental data provide a compelling example of combining genetic toolkits for soil adaptations to expand the habitat of an allopolyploid species.

Abstract

Empirical evidence is limited on whether allopolyploid species combine or merge parental adaptations to broaden habitats. The allopolyploid Arabidopsis kamchatica is a hybrid of the two diploid parents Arabidopsis halleri and Arabidopsis lyrata. A. halleri is a facultative heavy metal hyperaccumulator, and may be found in cadmium (Cd) and zinc (Zn) contaminated environments, as well as non-contaminated environments. A. lyrata is considered non-tolerant to these metals, but can be found in serpentine habitats. Therefore, the parents have adaptation to different environments. Here, we measured heavy metals in soils from native populations of A. kamchatica. We found that soil Zn concentration of nearly half of the sampled 40 sites was higher than the critical toxicity level. Many of the sites were near human construction, suggesting adaptation of A. kamchatica to artificially contaminated soils. Over half of the A. kamchatica populations had >1,000 μg g–1 Zn in leaf tissues. Using hydroponic treatments, most genotypes accumulated >3,000 μg g–1 Zn, with high variability among them, indicating substantial genetic variation in heavy metal accumulation. Genes involved in heavy metal hyperaccumulation showed an expression bias in the A. halleri-derived homeolog in widely distributed plant genotypes. We also found that two populations were found growing on serpentine soils. These data suggest that A. kamchatica can inhabit a range of both natural and artificial soil environments with high levels of ions that either of the parents specializes and that it can accumulate varying amount of heavy metals. Our field and experimental data provide a compelling example of combining genetic toolkits for soil adaptations to expand the habitat of an allopolyploid species.

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Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
08 Research Priority Programs > Evolution in Action: From Genomes to Ecosystems
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Scopus Subject Areas:Life Sciences > Molecular Medicine
Life Sciences > Genetics
Health Sciences > Genetics (clinical)
Uncontrolled Keywords:adaptation, expression ratio, heavy metal hyperaccumulation, homeolog, polyploid speciation, quantitative variation
Language:English
Date:30 September 2020
Deposited On:02 Feb 2021 10:25
Last Modified:10 Feb 2021 09:51
Publisher:Frontiers Research Foundation
ISSN:1664-8021
OA Status:Gold
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.3389/fgene.2020.565854
PubMed ID:33193650
Project Information:
  • : FunderUniversity of Zurich
  • : Grant IDURPP
  • : Project TitleEvolution in Action
  • : FunderJST CREST grant
  • : Grant IDJPMJCR16O3
  • : Project Title
  • : FunderSNSF
  • : Grant ID31003A_182318
  • : Project TitleEvolutionary functional genomics of selfing and polyploid speciation
  • : FunderMEXT KAKENHI
  • : Grant ID16H06469
  • : Project Title
  • : FunderMEXT KAKENHI
  • : Grant ID18H04785
  • : Project Title
  • : FunderSpecial Coordination Funds for Promoting Science and Technology
  • : Grant ID
  • : Project Title
  • : FunderInamori Foundation research grant
  • : Grant ID
  • : Project Title
  • : FunderJSPS Grant-in-Aid for Scientific Research
  • : Grant ID2277023
  • : Project Title

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