Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Metal accumulation by Arabidopsis halleri subsp. gemmifera at a limestone mining site

Aki Kosugi A , Jun Tamaru B , Kazumi Gotou B , Hazuka Y. Furihata C , Akifumi Shimizu B , Akira Kawabe C and Emiko Harada B D
+ Author Affiliations
- Author Affiliations

A Environmental Science Graduate School, The University of Shiga Prefecture, 2500, Hassaka-cho, Hikone-City, Shiga 522-8533, Japan.

B School of Environmental Science, The University of Shiga Prefecture, 2500, Hassaka-cho, Hikone-City, Shiga 522-8533, Japan.

C Faculty of Life Sciences, Kyoto Sangyo University, Motoyama, Kamigamo, Kita-Ku, Kyoto-City 603-8555, Japan.

D Corresponding author. Email: harada.e@ses.usp.ac.jp

Australian Journal of Botany 63(2) 134-140 https://doi.org/10.1071/BT14242
Submitted: 15 September 2014  Accepted: 12 January 2015   Published: 17 April 2015

Abstract

Arabidopsis halleri subsp. gemmifera, a close wild relative of A. thaliana in eastern Asia, is an important model species of Brassicaceae used to study cadmium (Cd) and zinc (Zn) tolerance and hyperaccumulation in plants. To investigate the effects of soil factors on metal accumulation in this plant, we collected plants and rhizosphere soil samples from a limestone mining site on Mount Ibuki, and compared them with those collected from non-calcareous soil in Japan. Irrespective of the sampling site, all the plants efficiently accumulated Cd in shoot tissues. The plants growing on non-calcareous soil also accumulated Zn in shoot tissues, but shoot Zn concentration in plants growing on calcareous soils was below the level required for hyperaccumulators. The pH of calcareous soil samples was between 7.68 and 8.21. Total Zn contents were similar in calcareous and non-calcareous soils, but the amounts of Zn extractable by 0.1 M HCl were lower in calcareous than in non-calcareous soil. These results indicate that the properties of calcareous soil affect metal accumulation in plants.

Additional keywords: cadmium, calcareous soil, hyperaccumulator, zinc.


References

Aizawa S (2009) Cadmium contents of Paleozoic limestones in South Kitakami Terrane, northeast Japan. Chikyukagaku (Geochemistry) 43, 59–71.

Aizawa S, Kuribara T (2006) Heavy metal contents of Triassic limestones in Okinawa-honto Island, the Ryukyus, southwest Japan. Chikyukagaku (Geochemistry) 40, 253–261.

Al-Shehbaz IA, O’Kane SL (2002) Taxonomy and phylogeny of Arabidopsis (Brassicaceae). The Arabidopsis Book 1, e0001
Taxonomy and phylogeny of Arabidopsis (Brassicaceae).Crossref | GoogleScholarGoogle Scholar | 22303187PubMed |

Alloway BJ (2009) Soil factors associated with zinc deficiency in crops and humans. Environmental Geochemistry and Health 31, 537–548.
Soil factors associated with zinc deficiency in crops and humans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVWrs77J&md5=635d74d53affe6cc883ca4b4735473e0CAS | 19291414PubMed |

Álvarez-Ayuso E (2008) Cadmium in soil-plant systems: an overview. International Journal of Environment and Pollution 33, 275–291.
Cadmium in soil-plant systems: an overview.Crossref | GoogleScholarGoogle Scholar |

Baxter I, Hermans C, Lahner B, Yakubova E, Tikhonova M, Verbruggen N, Chao DY, Salt DE (2012) Biodiversity of mineral nutrient and trace element accumulation in Arabidopsis thaliana. PLoS ONE 7, e35121
Biodiversity of mineral nutrient and trace element accumulation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntVemtro%3D&md5=931558317a10ab19c60086270cb2a020CAS | 22558123PubMed |

Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. The Plant Journal 37, 251–268.
Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVGlur8%3D&md5=48868251f9abda6ae2e858f6956774e7CAS | 14690509PubMed |

Bert V, Macnair MR, De Laguerie P, Saumitou-Laprade P, Petit D (2000) Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytologist 146, 225–233.
Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlGlsL0%3D&md5=fb4a0aaa5076843a007fc7a2443a33b9CAS |

Bert V, Bonnin I, Saumitou-Laprade P, De Laguérie P, Petit D (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytologist 155, 47–57.
Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsF2mt7w%3D&md5=d18610e99374888d4ddf1991092a39c5CAS |

Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends in Plant Science 20, 33–40.
Iron nutrition, biomass production, and plant product quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlamsb%2FO&md5=b4b50091b5906b0eb8cb151cbc66a873CAS | 25153038PubMed |

Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytologist 173, 677–702.
Zinc in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFGgsL8%3D&md5=9d22eb3500063f4b7bb8cd4941904ef3CAS | 17286818PubMed |

Chao D-Y, Silva A, Baxter I, Huang YS, Nordborg M, Danku J, Lahner B, Yakubova E, Salt DE (2012) Genome-wide association studies identify heavy metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLOS Genetics 8, e1002923
Genome-wide association studies identify heavy metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGitb7I&md5=285b1ef90783cac8a9334c34a228f614CAS | 22969436PubMed |

Clemens S (2014) Zn and Fe biofortification: The right chemical environment for human bioavailability. Plant Science 225, 52–57.
Zn and Fe biofortification: The right chemical environment for human bioavailability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFGqs7%2FM&md5=aa02236920231e615ec2dd80641ee3ecCAS | 25017159PubMed |

Deinlein U, Weber M, Schmidt H, Rensch S, Trampczynska A, Hansen TH, Husted S, Schjoerring JK, Talke IN, Krämer U, Clemens S (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. The Plant Cell 24, 708–723.
Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVCmtrnM&md5=bb51e4a9a1ca92dc73fbee8c1047853aCAS | 22374395PubMed |

Ernst WHO (1965) Ökologisch-soziologische Untersuchungen in den Schwermetall-Pflanzengesellschaften Mitteleuropas unter Einschluß der Alpen. Abhandlungen aus dem Landesmuseum für Naturkunde zu Münster in Westfalen 27, 1–54.

Fransz P, Armstrong S, Alonso-Blanco C, Fischer TC, Torres-Ruiz RA, Jones G (1998) Cytogenetics for the model system Arabidopsis thaliana. The Plant Journal 13, 867–876.
Cytogenetics for the model system Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXislejsb4%3D&md5=325a91e6e4e2764b8d44c83d31d22b98CAS | 9681023PubMed |

Harada E, Hokura A, Nakai I, Terada Y, Baba K, Yazaki K, Shiono M, Mizuno N, Mizuno T (2011) Assessment of willow (Salix sp.) as a woody heavy metal accumulator: field survey and in vivo X-ray analyses. Metallomics 3, 1340–1346.
Assessment of willow (Salix sp.) as a woody heavy metal accumulator: field survey and in vivo X-ray analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKmt7jK&md5=e90cc3859f93d0531074a4ea1c5dfb22CAS | 21969005PubMed |

Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.
Simultaneous inference in general parametric models.Crossref | GoogleScholarGoogle Scholar | 18481363PubMed |

Ikeda H, Setoguchi H, Morinaga S-I (2010) Genomic structure of lowland and highland ecotypes of Arabidopsis halleri ssp. gemmifera (Brassicaceae) on Mt. Ibuki. Acta Phytotaxonomica et Geobotanica 61, 21–26.

Imai N, Terashima S, Ohta A, Mikoshiba M, Okai T, Tachibana Y, Togashi S, Matsuhisa Y, Kanai Y, Kamioka H (2004) ‘Geochemical map in Japan. Geological survey in Japan.’ (AIST: Tukuba)

Kameyama K, Tani S, Sugawara R, Kitajima N, Ishikawa Y (2011) Remediation of Cd-contaminated andisol by Arabidopsis halleri ssp. gemmifera. Transactions of the Japanese Society of Irrigation, Drainage and Rural Engineering 79, 441–448.

Kameyama K, Tani S, Shiono T, Miyamoto T (2012) Method to predict soil Cd concentration changes by phytoextraction with Arabidopsis halleri ssp. gemmifera in a Cd-contaminated andisol field. Transactions of the Japanese Society of Irrigation, Drainage and Rural Engineering 80, 543–548.

Kawabe A, Nasuda S (2005) Structure and genomic organization of centromeric repeats in Arabidopsis species. Molecular Genetics and Genomics 272, 593–602.
Structure and genomic organization of centromeric repeats in Arabidopsis species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVGksL4%3D&md5=2ad7091f4ec9b1b2fc4689dd09640b12CAS | 15586291PubMed |

Kenderešová L, Staňová A, Pavlovkin J, Ďurišová E, Nadubinská M, Čiamporová M, Ovečka M (2012) Early Zn2+-induced effects on membrane potential account for primary heavy metal susceptibility in tolerant and sensitive Arabidopsis species. Annals of Botany 110, 445–459.
Early Zn2+-induced effects on membrane potential account for primary heavy metal susceptibility in tolerant and sensitive Arabidopsis species.Crossref | GoogleScholarGoogle Scholar | 22645116PubMed |

Kobayashi F, Furutani H (2009) Early Permian fusulines from the western part of Mt. Ryozen, Shiga Prefecture, Japan. Human and Nature 20, 29–54.

Koch MA, Wernisch M, Schmickl R (2008) Arabidopsis thaliana’s wild relatives: an updated overview on systematics, taxonomy and evolution. Taxon 57, 933–943.

Kolník M, Marhold K (2006) Distribution, chromosome numbers and nomenclature conspect of Arabidopsis halleri (Brassicaceae) in the Carpathians. Biologia 61, 41–50.
Distribution, chromosome numbers and nomenclature conspect of Arabidopsis halleri (Brassicaceae) in the Carpathians.Crossref | GoogleScholarGoogle Scholar |

Krämer U (2010) Metal hyperaccumulation in plants. Annual Review of Plant Biology 61, 517–534.
Metal hyperaccumulation in plants.Crossref | GoogleScholarGoogle Scholar | 20192749PubMed |

Kubota H, Takenaka C (2003) Arabis gemmifera is a hyperaccumulator of Cd and Zn. International Journal of Phytoremediation 5, 197–201.
Arabis gemmifera is a hyperaccumulator of Cd and Zn.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotlKmsw%3D%3D&md5=a8e5ab772bdae6e48ca72028693f468aCAS | 14750427PubMed |

Meyer C-L, Verbruggen N (2012) The use of the model species Arabidopsis halleri towards phytoextraction of cadmium polluted soils. New Biotechnology 30, 9–14.
The use of the model species Arabidopsis halleri towards phytoextraction of cadmium polluted soils.Crossref | GoogleScholarGoogle Scholar |

Ozturk L, Karanlik S, Ozkutlu F, Cakmak I, Kochian LV (2003) Shoot biomass and zinc/cadmium uptake for hyperaccumulator and non-accumulator Thlaspi species in response to growth on a zinc-deficient calcareous soil. Plant Science 164, 1095–1101.
Shoot biomass and zinc/cadmium uptake for hyperaccumulator and non-accumulator Thlaspi species in response to growth on a zinc-deficient calcareous soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjs1CksL4%3D&md5=b77db03a44cf146c79e43ffcc339a7a0CAS |

Pauwels M, Frérot H, Bonnin I, Saumitou-Laprade P (2006) A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae). Journal of Evolutionary Biology 19, 1838–1850.
A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1GrurrP&md5=ef4a420fe218b6d7f7746d10787d0df0CAS | 17040381PubMed |

Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Science 217–218, 8–17.
Facultative hyperaccumulation of heavy metals and metalloids.Crossref | GoogleScholarGoogle Scholar | 24467891PubMed |

R Core Team (2013) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna). Available at http://www.R-project.org/ [Verified 18 June 2013]

Rodríguez N, Menéndez N, Tornero J, Amils R, De La Fuente V (2005) Internal iron biomineralization in Imperata cylindrica, a perennial grass: chemical composition, speciation and plant localization. New Phytologist 165, 781–789.
Internal iron biomineralization in Imperata cylindrica, a perennial grass: chemical composition, speciation and plant localization.Crossref | GoogleScholarGoogle Scholar | 15720689PubMed |

Schmickl R, Jørgensen MH, Brysting AK, Koch MA (2010) The evolutionary history of the Arabidopsis lyrata complex: a hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier. BMC Evolutionary Biology 10, 98
The evolutionary history of the Arabidopsis lyrata complex: a hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier.Crossref | GoogleScholarGoogle Scholar | 20377907PubMed |

Schmid NB, Giehl RFH, Döll S, Mock HP, Strehmel N, Scheel D, Kong X, Hider RC, von Wirén N (2014) Feruloyl-CoA 6ʹ-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiology 164, 160–172.
Feruloyl-CoA 6ʹ-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks1CqtrY%3D&md5=9363d33980ecc041a9c180cfbea4c638CAS | 24246380PubMed |

Schmidt H, Günther C, Weber M, Spörlein C, Loscher S, Böttcher C, Schobert R, Clemens S (2014) Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition. PLoS ONE 9, e102444
Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition.Crossref | GoogleScholarGoogle Scholar | 25058345PubMed |

Shen ZG, Zhao FJ, McGrath SP (1997) Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant, Cell & Environment 20, 898–906.
Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlt1Wmt7g%3D&md5=23086f99887f3883d69c961fc80008b3CAS |

Shimizu KK, Fujii S, Marhold K, Watanabe K, Kudoh H (2005) Arabidopsis kamchatica (Fisch. ex DC.) K.Shimizu & Kudoh and A. kamchatica subsp. kawasakiana (Makino) K.Shimizu & Kudoh, new combinations. Acta Phytotaxonomica et Geobotanica 56, 163–172.

Shimizu-Inatsugi R, Lihová J, Iwanaga H, Kudoh H, Marhold K, Savolainen O, Watanabe K, Yakubov VV, Shimizu KK (2009) The allopolyploid Arabidopsis kamchatica originated from multiple individuals of Arabidopsis lyrata and Arabidopsis halleri. Molecular Ecology 18, 4024–4048.
The allopolyploid Arabidopsis kamchatica originated from multiple individuals of Arabidopsis lyrata and Arabidopsis halleri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlygtrnI&md5=6cdcb604133262bfce8a5f88c387989aCAS | 19754506PubMed |

Turner TL, Bourne EC, von Wettberg EJ, Hu TT, Nuzhdin SV (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nature Genetics 42, 260–263.
Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVWrtbw%3D&md5=d70b63473aede2961544ddf0350bbc0aCAS | 20101244PubMed |

Weber M, Harada E, Vess C, Roepenack-Lahaye Ev, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. The Plant Journal 37, 269–281.
Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVGlurw%3D&md5=2922cab466732b5ae494c45b1d6c12caCAS | 14690510PubMed |