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PMID: 12805592 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice.

Plant physiology ·Vol. 132 ·No. 2 ·2003-06-00 ·Pages 618-28

Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB

Abstract

Members of the P-type ATPase ion pump superfamily are found in all three branches of life. Forty-six P-type ATPase genes were identified in Arabidopsis, the largest number yet identified in any organism. The recent completion of two draft sequences of the rice (Oryza sativa) genome allows for comparison of the full complement of P-type ATPases in two different plant species. Here, we identify a similar number (43) in rice, despite the rice genome being more than three times the size of Arabidopsis. The similarly large families suggest that both dicots and monocots have evolved with a large preexisting repertoire of P-type ATPases. Both Arabidopsis and rice have representative members in all five major subfamilies of P-type ATPases: heavy-metal ATPases (P1B), Ca2+-ATPases (endoplasmic reticulum-type Ca2+-ATPase and autoinhibited Ca2+-ATPase, P2A and P2B), H+-ATPases (autoinhibited H+-ATPase, P3A), putative aminophospholipid ATPases (ALA, P4), and a branch with unknown specificity (P5). The close pairing of similar isoforms in rice and Arabidopsis suggests potential orthologous relationships for all 43 rice P-type ATPases. A phylogenetic comparison of protein sequences and intron positions indicates that the common angiosperm ancestor had at least 23 P-type ATPases. Although little is known about unique and common features of related pumps, clear differences between some members of the calcium pumps indicate that evolutionarily conserved clusters may distinguish pumps with either different subcellular locations or biochemical functions.

Keywords
Non-programmatic
MeSH Terms
Adenosine Triphosphatases/genetics Arabidopsis/classification,genetics Genome, Plant Introns Multigene Family Oryza/classification,genetics Phylogeny
Chemicals
Adenosine Triphosphatases
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Baxter Ivan
Department of Cell Biology, Plant Division, The Scripps Research Institute, La Jolla, California 92037, USA.
Tchieu Jason
Sussman Michael R
Boutry Marc
Palmgren Michael G
Gribskov Michael
Harper Jeffrey F
Axelsen Kristian B
References (49)
49 references, click to expand
  1. PLANT PLASMA MEMBRANE H+-ATPases: Powerhouses for Nutrient Uptake.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:817-845 PMID: 11337417
  2. Autoinhibition of a calmodulin-dependent calcium pump involves a structure in the stalk that connects the transmembrane domain to the ATPase catalytic domain.
    J Biol Chem. 2000 Sep 29;275(39):30301-8 PMID: 10818096
  3. Cod1p/Spf1p is a P-type ATPase involved in ER function and Ca2+ homeostasis.
    J Cell Biol. 2002 Jun 10;157(6):1017-28 PMID: 12058017
  4. Inventory of the superfamily of P-type ion pumps in Arabidopsis.
    Plant Physiol. 2001 Jun;126(2):696-706 PMID: 11402198
  5. 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
  6. Cloning of a Ca(2+)-ATPase gene and the role of cytosolic Ca2+ in the gibberellin-dependent signaling pathway in aleurone cells.
    Plant J. 1997 Mar;11(3):363-71 PMID: 9107028
  7. Computational gene finding in plants.
    Plant Mol Biol. 2002 Jan;48(1-2):39-48 PMID: 11860211
  8. Whole-genome comparison of leucine-rich repeat extensins in Arabidopsis and rice. A conserved family of cell wall proteins form a vegetative and a reproductive clade.
    Plant Physiol. 2003 Mar;131(3):1313-26 PMID: 12644681
  9. An endoplasmic reticulum-bound Ca(2+)/Mn(2+) pump, ECA1, supports plant growth and confers tolerance to Mn(2+) stress.
    Plant Physiol. 2002 Sep;130(1):128-37 PMID: 12226493
  10. Evolution of P-type ATPases.
    Biochim Biophys Acta. 1998 Jun 10;1365(1-2):37-45 PMID: 9693719
  11. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution.
    Nature. 2000 Jun 8;405(6787):647-55 PMID: 10864315
  12. Two additional type IIA Ca(2+)-ATPases are expressed in Arabidopsis thaliana: evidence that type IIA sub-groups exist.
    Gene. 1999 Aug 5;236(1):137-47 PMID: 10433975
  13. The plasma membrane H(+)-ATPase gene family in Arabidopsis: genomic sequence of AHA10 which is expressed primarily in developing seeds.
    Mol Gen Genet. 1994 Sep 28;244(6):572-87 PMID: 7969026
  14. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica).
    Science. 2002 Apr 5;296(5565):92-100 PMID: 11935018
  15. A high-throughput Arabidopsis reverse genetics system.
    Plant Cell. 2002 Dec;14(12):2985-94 PMID: 12468722
  16. Identification of a calmodulin-regulated Ca2+-ATPase in the endoplasmic reticulum.
    Plant Physiol. 1999 Apr;119(4):1165-76 PMID: 10198075
  17. Cosuppression of a plasma membrane H(+)-ATPase isoform impairs sucrose translocation, stomatal opening, plant growth, and male fertility.
    Plant Cell. 2000 Apr;12(4):535-46 PMID: 10760242
  18. Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast.
    Annu Rev Plant Physiol Plant Mol Biol. 2000;51:433-62 PMID: 11543429
  19. Structural changes in the calcium pump accompanying the dissociation of calcium.
    Nature. 2002 Aug 8;418(6898):605-11 PMID: 12167852
  20. A draft sequence of the rice genome (Oryza sativa L. ssp. indica).
    Science. 2002 Apr 5;296(5565):79-92 PMID: 11935017
  21. The complete inventory of the yeast Saccharomyces cerevisiae P-type transport ATPases.
    FEBS Lett. 1997 Jun 16;409(3):325-32 PMID: 9224683
  22. Evidence for a role in growth and salt resistance of a plasma membrane H+-ATPase in the root endodermis.
    Plant J. 2001 Aug;27(3):191-201 PMID: 11532165
  23. Identification of an Arabidopsis thaliana gene encoding a plasma membrane H(+)-ATPase whose expression is restricted to anther tissue.
    Plant J. 1994 Mar;5(3):311-7 PMID: 8180619
  24. The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast.
    Plant Physiol. 2000 Dec;124(4):1814-27 PMID: 11115896
  25. The plasma membrane proton pump ATPase: the significance of gene subfamilies.
    Planta. 2003 Jan;216(3):355-65 PMID: 12520326
  26. Compositional gradients in Gramineae genes.
    Genome Res. 2002 Jun;12(6):851-6 PMID: 12045139
  27. A computer program for aligning a cDNA sequence with a genomic DNA sequence.
    Genome Res. 1998 Sep;8(9):967-74 PMID: 9750195
  28. A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis.
    Nat Genet. 1998 Mar;18(3):219-24 PMID: 9500542
  29. A Single Gene May Encode Differentially Localized Ca2+-ATPases in Tomato.
    Plant Cell. 1996 Jul;8(7):1159-1169 PMID: 12239413
  30. Calcium pumps: structural basis for and mechanism of calcium transmembrane transport.
    Curr Opin Chem Biol. 2000 Apr;4(2):152-61 PMID: 10742184
  31. A calmodulin-stimulated Ca2+-ATPase from plant vacuolar membranes with a putative regulatory domain at its N-terminus.
    FEBS Lett. 1997 Jan 6;400(3):324-8 PMID: 9009223
  32. Modeling the three-dimensional structure of H+-ATPase of Neurospora crassa.
    Eur J Biochem. 2002 Nov;269(21):5246-58 PMID: 12392557
  33. Efficient screening of Arabidopsis T-DNA insertion lines using degenerate primers.
    Plant Physiol. 2001 Feb;125(2):513-8 PMID: 11161007
  34. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  35. At-ACA8 encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus.
    Plant Physiol. 2000 Aug;123(4):1495-506 PMID: 10938365
  36. Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases.
    Plant Cell. 2000 Dec;12(12):2441-2454 PMID: 11148289
  37. Emerging mechanisms for heavy metal transport in plants.
    Biochim Biophys Acta. 2000 May 1;1465(1-2):104-26 PMID: 10748249
  38. Evolution of substrate specificities in the P-type ATPase superfamily.
    J Mol Evol. 1998 Jan;46(1):84-101 PMID: 9419228
  39. Inventory and functional characterization of the HAK potassium transporters of rice.
    Plant Physiol. 2002 Oct;130(2):784-95 PMID: 12376644
  40. The ATP-binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis.
    Plant Physiol. 2003 Mar;131(3):1169-77 PMID: 12644668
  41. A putative proton binding site of plasma membrane H(+)-ATPase identified through homology modelling.
    FEBS Lett. 2001 Apr 6;494(1-2):6-10 PMID: 11297724
  42. Molecular aspects of higher plant P-type Ca(2+)-ATPases.
    Biochim Biophys Acta. 2000 May 1;1465(1-2):52-78 PMID: 10748247
  43. Targeting of two Arabidopsis H(+)-ATPase isoforms to the plasma membrane.
    Plant Physiol. 1996 Oct;112(2):833-44 PMID: 8883393
  44. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  45. Structure, mechanism, and regulation of the Neurospora plasma membrane H+-ATPase.
    Science. 2002 Sep 6;297(5587):1692-6 PMID: 12169656
  46. A novel calmodulin-regulated Ca2+-ATPase (ACA2) from Arabidopsis with an N-terminal autoinhibitory domain.
    J Biol Chem. 1998 Jan 9;273(2):1099-106 PMID: 9422775
  47. Homology modeling of the cation binding sites of Na+K+-ATPase.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):15977-82 PMID: 12461183
  48. Drs2p-dependent formation of exocytic clathrin-coated vesicles in vivo.
    Curr Biol. 2002 Sep 17;12(18):1623-7 PMID: 12372257
  49. Two distinctly localized p-type ATPases collaborate to maintain organelle homeostasis required for glycoprotein processing and quality control.
    Mol Biol Cell. 2002 Nov;13(11):3955-66 PMID: 12429838
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2003-06-00
Pages
618-28
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC167002
Subset
IM
Corrections
ErratumIn
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