Home LiteratureArticle Details
PMID: 18701674 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Amino acid polymorphisms in strictly conserved domains of a P-type ATPase HMA5 are involved in the mechanism of copper tolerance variation in Arabidopsis.

Plant physiology ·Vol. 148 ·No. 2 ·2008-10-00 ·Pages 969-80

Kobayashi Y, Kuroda K, Kimura K, Southron-Francis JL, Furuzawa A, Kimura K, Iuchi S, Kobayashi M, Taylor GJ, Koyama H

Abstract

Copper (Cu) is an essential element in plant nutrition, but it inhibits the growth of roots at low concentrations. Accessions of Arabidopsis (Arabidopsis thaliana) vary in their tolerance to Cu. To understand the molecular mechanism of Cu tolerance in Arabidopsis, we performed quantitative trait locus (QTL) analysis and accession studies. One major QTL on chromosome 1 (QTL1) explained 52% of the phenotypic variation in Cu tolerance in roots in a Landsberg erecta/Cape Verde Islands (Ler/Cvi) recombinant inbred population. This QTL regulates Cu translocation capacity and involves a Cu-transporting P(1B-1)-type ATPase, HMA5. The Cvi allele carries two amino acid substitutions in comparison with the Ler allele and is less functional than the Ler allele in Cu tolerance when judged by complementation assays using a T-DNA insertion mutant. Complementation assays of the ccc2 mutant of yeast using chimeric HMA5 proteins revealed that N923T of the Cvi allele, which was identified in the tightly conserved domain N(x)(6)YN(x)(4)P (where the former asparagine was substituted by threonine), is a cause of dysfunction of the Cvi HMA5 allele. Another dysfunctional HMA5 allele was identified in Chisdra-2, which showed Cu sensitivity and low capacity of Cu translocation from roots to shoots. A unique amino acid substitution of Chisdra-2 was identified in another strictly conserved domain, CPC(x)(6)P, where the latter proline was replaced with leucine. These results indicate that a portion of the variation in Cu tolerance of Arabidopsis is regulated by the functional integrity of the Cu-translocating ATPase, HMA5, and in particular the amino acid sequence in several strictly conserved motifs.

MeSH Terms
Adenosine Triphosphatases/genetics,metabolism Alleles Amino Acid Motifs Amino Acid Sequence Amino Acid Substitution Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Conserved Sequence Copper/metabolism DNA, Bacterial/genetics DNA, Plant/genetics Genes, Plant Genetic Complementation Test Genotype Molecular Sequence Data Mutagenesis, Insertional Phenotype Polymorphism, Genetic Quantitative Trait Loci Saccharomyces cerevisiae/genetics,metabolism
Chemicals
Arabidopsis Proteins DNA, Bacterial DNA, Plant T-DNA Copper Adenosine Triphosphatases
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Kobayashi Yuriko
Laboratory of Plant Cell Technology, Faculty of Applied Biological Sciences, Gifu University, Gifu, Japan.
Kuroda Keishi
Kimura Keisuke
Southron-Francis Jennafer L
Furuzawa Aya
Kimura Kazuhiko
Iuchi Satoshi
Kobayashi Masatomo
Taylor Gregory J
Koyama Hiroyuki
References (48)
48 references, click to expand
  1. A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis.
    Plant Physiol. 2005 Sep;139(1):425-36 PMID: 16126858
  2. Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase.
    Plant Physiol. 2004 Nov;136(3):3814-23 PMID: 15516513
  3. Sequence, mapping and disruption of CCC2, a gene that cross-complements the Ca(2+)-sensitive phenotype of csg1 mutants and encodes a P-type ATPase belonging to the Cu(2+)-ATPase subfamily.
    Yeast. 1995 Mar;11(3):283-92 PMID: 7785328
  4. Differences in ATP7A gene expression underlie intrafamilial variability in Menkes disease/occipital horn syndrome.
    J Med Genet. 2007 Aug;44(8):492-7 PMID: 17496194
  5. Molecular characterization of a putative Arabidopsis thaliana copper transporter and its yeast homologue.
    J Biol Chem. 1995 Nov 24;270(47):28479-86 PMID: 7499355
  6. Natural variation of Arabidopsis thaliana reveals that aluminum resistance and proton resistance are controlled by different genetic factors.
    Theor Appl Genet. 2007 Sep;115(5):709-19 PMID: 17661006
  7. Excess copper induces accumulation of hydrogen peroxide and increases lipid peroxidation and total activity of copper-zinc superoxide dismutase in roots of Elsholtzia haichowensis.
    Planta. 2008 Jan;227(2):465-75 PMID: 17909854
  8. Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population.
    Plant J. 1998 Apr;14(2):259-71 PMID: 9628021
  9. Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase.
    J Biol Chem. 1996 Jun 14;271(24):14504-9 PMID: 8662933
  10. The copper chaperone for superoxide dismutase.
    J Biol Chem. 1997 Sep 19;272(38):23469-72 PMID: 9295278
  11. The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana.
    Nat Genet. 2006 Jun;38(6):711-5 PMID: 16732287
  12. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis.
    Plant Cell. 2004 May;16(5):1327-39 PMID: 15100400
  13. Structure and function of cytochrome c oxidase.
    Annu Rev Biochem. 1990;59:569-96 PMID: 2165384
  14. Complementation of Saccharomyces cerevisiae ccc2 mutant by a putative P1B-ATPase from Brassica napus supports a copper-transporting function.
    FEBS Lett. 2004 May 21;566(1-3):218-22 PMID: 15147898
  15. Identification of a copper transporter family in Arabidopsis thaliana.
    Plant Mol Biol. 2003 Mar;51(4):577-87 PMID: 12650623
  16. RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis.
    Cell. 1999 Apr 30;97(3):383-93 PMID: 10319818
  17. P(1B)-ATPases--an ancient family of transition metal pumps with diverse functions in plants.
    Trends Plant Sci. 2005 Oct;10(10):491-502 PMID: 16154798
  18. Copper-regulated trafficking of the Menkes disease copper ATPase is associated with formation of a phosphorylated catalytic intermediate.
    J Biol Chem. 2002 Nov 29;277(48):46736-42 PMID: 12228238
  19. Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci.
    Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):10972-6 PMID: 8248199
  20. Efficacy of a copper-lysine complex as a growth promotant for weanling pigs.
    J Anim Sci. 1994 Nov;72(11):2880-6 PMID: 7730181
  21. Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases.
    J Membr Biol. 2003 Sep 15;195(2):93-108 PMID: 14692449
  22. Empirical threshold values for quantitative trait mapping.
    Genetics. 1994 Nov;138(3):963-71 PMID: 7851788
  23. Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene.
    Plant Physiol. 2001 Aug;126(4):1519-26 PMID: 11500550
  24. Molecular pathogenesis of Wilson and Menkes disease: correlation of mutations with molecular defects and disease phenotypes.
    J Med Genet. 2007 Nov;44(11):673-88 PMID: 17717039
  25. Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia.
    Plant Physiol. 1992 May;99(1):263-8 PMID: 16668860
  26. PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts.
    Plant Cell. 2003 Jun;15(6):1333-46 PMID: 12782727
  27. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2.
    Nat Genet. 2001 Dec;29(4):435-40 PMID: 11726930
  28. Copper-dependent trafficking of Wilson disease mutant ATP7B proteins.
    Hum Mol Genet. 2000 Aug 12;9(13):1927-35 PMID: 10942420
  29. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots.
    Plant J. 2006 Jan;45(2):225-36 PMID: 16367966
  30. Association of cholesteryl ester transfer protein genotypes with CETP mass and activity, lipid levels, and coronary risk.
    JAMA. 2008 Jun 18;299(23):2777-88 PMID: 18560005
  31. Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis.
    Plant Physiol. 2007 Nov;145(3):843-52 PMID: 17885092
  32. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4.
    Nature. 2008 May 15;453(7193):391-5 PMID: 18425111
  33. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts.
    Plant Cell. 2005 Apr;17(4):1233-51 PMID: 15772282
  34. Natural variation in light sensitivity of Arabidopsis.
    Nat Genet. 2001 Dec;29(4):441-6 PMID: 11726931
  35. Naturally occurring genetic variation in Arabidopsis thaliana.
    Annu Rev Plant Biol. 2004;55:141-72 PMID: 15377217
  36. Molecular mechanisms of plant metal tolerance and homeostasis.
    Planta. 2001 Mar;212(4):475-86 PMID: 11525504
  37. The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels.
    FEBS Lett. 2005 Jan 31;579(3):783-91 PMID: 15670847
  38. Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance.
    Proc Natl Acad Sci U S A. 2007 Jun 5;104(23):9900-5 PMID: 17535918
  39. Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis.
    Plant Physiol. 2005 Nov;139(3):1304-12 PMID: 16244146
  40. Identification of a functional homolog of the yeast copper homeostasis gene ATX1 from Arabidopsis.
    Plant Physiol. 1998 Aug;117(4):1227-34 PMID: 9701579
  41. Precision mapping of quantitative trait loci.
    Genetics. 1994 Apr;136(4):1457-68 PMID: 8013918
  42. A simple hydroponic culture method for the development of a highly viable root system in Arabidopsis thaliana.
    Biosci Biotechnol Biochem. 1999 Jan;63(1):210-2 PMID: 10052145
  43. A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype.
    Plant Cell. 2000 Mar;12(3):443-55 PMID: 10715329
  44. The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development.
    J Biol Chem. 2004 Apr 9;279(15):15348-55 PMID: 14726516
  45. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations.
    Genomics. 1987 Oct;1(2):174-81 PMID: 3692487
  46. Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2.
    Nat Genet. 2007 Jul;39(7):896-900 PMID: 17589509
  47. Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications.
    Plant Cell Environ. 2007 Mar;30(3):271-290 PMID: 17263774
  48. ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis.
    Plant J. 2005 Feb;41(3):353-63 PMID: 15659095
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2008-10-00
Epub
2008-00-13
Pages
969-80
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2556842
Subset
IM
Databases
GENBANK
EU877765, EU877766, EU877767, EU877768, EU877769, EU877770, EU877771, EU877772, EU877773, EU877774, EU877775, EU877776, EU877777, EU877778, EU877779, EU877780, EU877781, EU877782, EU877783, EU877784, EU877785, EU877786, EU877787, EU877788, EU877789, EU877790, EU877791, EU877792, EU877793, EU877794, EU877795, EU877796, EU877797, EU877798, EU877799, EU877800, EU877801, EU877802, EU877803
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com