Home LiteratureArticle Details
PMID: 16344959 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

NADPH oxidases in Eukaryotes: red algae provide new hints!

Current genetics ·Vol. 49 ·No. 3 ·2006-03-00 ·Pages 190-204

Hervé C, Tonon T, Collén J, Corre E, Boyen C

Abstract

The red macro-alga Chondrus crispus is known to produce superoxide radicals in response to cell-free extracts of its green algal pathogenic endophyte Acrochaete operculata. So far, no enzymes involved in this metabolism have been isolated from red algae. We report here the isolation of a gene encoding a homologue of the respiratory burst oxidase gp91(phox) in C. crispus, named Ccrboh. This single copy gene encodes a polypeptide of 825 amino acids. Search performed in available genome and EST algal databases identified sequences showing common features of NADPH oxidases in other algae such as the red unicellular Cyanidioschyzon merolae, the economically valuable red macro-alga Porphyra yezoensis and the two diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. Domain organization and phylogenetic relationships with plant, animal, fungal and algal NADPH oxidase homologues were analyzed. Transcription analysis of the C. crispus gene revealed that it was over-transcribed during infection of C. crispus gametophyte by the endophyte A. operculata, and after incubation in presence of atrazine, methyl jasmonate and hydroxyperoxides derived from C20 polyunsaturated fatty acids (PUFAs). These results also illustrate the interest of exploring the red algal lineage for gaining insight into the deep evolution of NADPH oxidases in Eukaryotes.

MeSH Terms
Algal Proteins/genetics,metabolism Amino Acid Sequence Chondrus/enzymology Cloning, Molecular Diatoms/chemistry Eukaryotic Cells/enzymology Evolution, Molecular Molecular Sequence Data NADPH Oxidases/genetics,metabolism Phylogeny Sequence Homology, Amino Acid
Chemicals
Algal Proteins NADPH Oxidases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Hervé Cécile
UMR7139 (CNRS-UPMC-LIA DIAMS), Station Biologique, F-29682, Roscoff Cedex, France.
Tonon Thierry
Collén Jonas
Corre Erwan
Boyen Catherine
References (61)
61 references, click to expand
  1. Cell transformation by the superoxide-generating oxidase Mox1.
    Nature. 1999 Sep 2;401(6748):79-82 PMID: 10485709
  2. Hydrogen peroxide and nitric oxide as signalling molecules in plants.
    J Exp Bot. 2002 May;53(372):1237-47 PMID: 11997372
  3. rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene.
    Plant J. 1996 Sep;10(3):515-22 PMID: 8811865
  4. Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme.
    FEBS Lett. 1996 Mar 11;382(1-2):213-7 PMID: 8612756
  5. Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato.
    Mol Plant Microbe Interact. 2001 Jun;14(6):725-36 PMID: 11386368
  6. NADPH oxidase and the respiratory burst.
    Semin Cell Biol. 1995 Dec;6(6):357-65 PMID: 8748143
  7. Biotic interactions of marine algae.
    Curr Opin Plant Biol. 2002 Aug;5(4):308-17 PMID: 12179964
  8. Microbial ferric iron reductases.
    FEMS Microbiol Rev. 2003 Jun;27(2-3):427-47 PMID: 12829278
  9. The innate immunity of a marine red alga involves oxylipins from both the eicosanoid and octadecanoid pathways.
    Plant Physiol. 2004 Jul;135(3):1838-48 PMID: 15247395
  10. The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells.
    Plant J. 2002 Jul;31(2):137-47 PMID: 12121444
  11. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans.
    Mol Microbiol. 2003 Nov;50(4):1241-55 PMID: 14622412
  12. Identification of renox, an NAD(P)H oxidase in kidney.
    Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):8010-4 PMID: 10869423
  13. NADPH oxidases: not just for leukocytes anymore!
    Trends Biochem Sci. 2003 Sep;28(9):502-8 PMID: 13678962
  14. Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox.
    J Cell Biol. 2001 Aug 20;154(4):879-91 PMID: 11514595
  15. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):517-22 PMID: 11756663
  16. Apoplastic oxidation of L-asparagine is involved in the control of the green algal endophyte Acrochaete operculata Correa & Nielsen by the red seaweed Chondrus crispus Stackhouse.
    J Exp Bot. 2005 May;56(415):1317-26 PMID: 15784529
  17. Prostaglandins and leukotrienes: advances in eicosanoid biology.
    Science. 2001 Nov 30;294(5548):1871-5 PMID: 11729303
  18. How neutrophils kill microbes.
    Annu Rev Immunol. 2005;23:197-223 PMID: 15771570
  19. Signal transduction during oxidative stress.
    J Exp Bot. 2002 May;53(372):1227-36 PMID: 11997371
  20. Active oxygen in plant pathogenesis.
    Annu Rev Phytopathol. 1995;33:299-321 PMID: 18999963
  21. Metalloregulation of FRE1 and FRE2 homologs in Saccharomyces cerevisiae.
    J Biol Chem. 1998 Sep 11;273(37):23716-21 PMID: 9726978
  22. Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of laminariales.
    J Chem Ecol. 2002 Oct;28(10):2057-81 PMID: 12474900
  23. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system.
    J Exp Bot. 2002 May;53(372):1367-76 PMID: 11997382
  24. Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans.
    Plant Cell. 2003 Mar;15(3):706-18 PMID: 12615943
  25. Role of reactive oxygen species in cell signalling pathways.
    Biochem Soc Trans. 2001 May;29(Pt 2):345-50 PMID: 11356180
  26. Intramembrane bis-heme motif for transmembrane electron transport conserved in a yeast iron reductase and the human NADPH oxidase.
    J Biol Chem. 1996 Dec 6;271(49):31021-4 PMID: 8940093
  27. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism.
    Science. 2004 Oct 1;306(5693):79-86 PMID: 15459382
  28. Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cdnas.
    J Biol Chem. 1999 Dec 24;274(52):37265-9 PMID: 10601291
  29. Interactions between the components of the human NADPH oxidase: a review about the intrigues in the phox family.
    Front Biosci. 1996 Jul 01;1:d72-90 PMID: 9159214
  30. Generation of 10,154 expressed sequence tags from a leafy gametophyte of a marine red alga, Porphyra yezoensis.
    DNA Res. 2000 Jun 30;7(3):223-7 PMID: 10907854
  31. The deep roots of eukaryotes.
    Science. 2003 Jun 13;300(5626):1703-6 PMID: 12805537
  32. Detection of specific sequences among DNA fragments separated by gel electrophoresis.
    J Mol Biol. 1975 Nov 5;98(3):503-17 PMID: 1195397
  33. A Ca(2+)-activated NADPH oxidase in testis, spleen, and lymph nodes.
    J Biol Chem. 2001 Oct 5;276(40):37594-601 PMID: 11483596
  34. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata.
    Plant Physiol. 2001 Jan;125(1):278-91 PMID: 11154336
  35. Characterisation of complementary DNAs from the expressed sequence tag analysis of life cycle stages of Laminaria digitata (Phaeophyceae).
    Plant Mol Biol. 2000 Jul;43(4):503-13 PMID: 11052202
  36. Spatiotemporal patterning of reactive oxygen production and Ca(2+) wave propagation in fucus rhizoid cells.
    Plant Cell. 2002 Oct;14(10):2369-81 PMID: 12368492
  37. The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence--a review.
    Gene. 1996 Nov 7;179(1):45-51 PMID: 8955628
  38. A ferric-chelate reductase for iron uptake from soils.
    Nature. 1999 Feb 25;397(6721):694-7 PMID: 10067892
  39. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.
    Cell. 1994 Nov 18;79(4):583-93 PMID: 7954825
  40. Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition.
    Plant Physiol. 2002 May;129(1):85-94 PMID: 12011340
  41. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:251-275 PMID: 15012264
  42. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs.
    Plant Cell. 1998 Feb;10(2):255-66 PMID: 9490748
  43. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D.
    Nature. 2004 Apr 8;428(6983):653-7 PMID: 15071595
  44. Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase.
    Biochem J. 1993 Feb 15;290 ( Pt 1):41-9 PMID: 8439298
  45. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5.
    Gene. 2001 May 16;269(1-2):131-40 PMID: 11376945
  46. Reactive oxygen species and development in microbial eukaryotes.
    Trends Microbiol. 2005 Mar;13(3):111-8 PMID: 15737729
  47. Methyl jasmonate as a vital substance in plants.
    Trends Genet. 2003 Jul;19(7):409-13 PMID: 12850447
  48. Limiting nutrients: an old problem with new solutions?
    Curr Opin Plant Biol. 2002 Apr;5(2):158-63 PMID: 11856613
  49. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.
    Nature. 2003 Mar 27;422(6930):442-6 PMID: 12660786
  50. Fatty acid-derived signals in plants.
    Trends Plant Sci. 2002 May;7(5):217-24 PMID: 11992827
  51. Sulfated Oligosaccharides Mediate the Interaction between a Marine Red Alga and Its Green Algal Pathogenic Endophyte.
    Plant Cell. 1999 Sep;11(9):1635-1650 PMID: 10488232
  52. Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection.
    Plant Physiol. 2001 Jul;126(3):1281-90 PMID: 11457979
  53. NADPH oxidase: an enzyme for multicellularity?
    Trends Microbiol. 2003 Jan;11(1):9-12 PMID: 12526848
  54. Oxidative burst: an early plant response to pathogen infection.
    Biochem J. 1997 Mar 15;322 ( Pt 3):681-92 PMID: 9148737
  55. The Diatom EST Database.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D344-7 PMID: 15608213
  56. Chemical cues for surface colonization.
    J Chem Ecol. 2002 Oct;28(10):1935-51 PMID: 12474892
  57. A novel superoxide-producing NAD(P)H oxidase in kidney.
    J Biol Chem. 2001 Jan 12;276(2):1417-23 PMID: 11032835
  58. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.
    EMBO J. 2003 Jun 2;22(11):2623-33 PMID: 12773379
  59. The evolution of modern eukaryotic phytoplankton.
    Science. 2004 Jul 16;305(5682):354-60 PMID: 15256663
  60. The superoxide-generating NADPH oxidase: structural aspects and activation mechanism.
    Cell Mol Life Sci. 2002 Sep;59(9):1428-59 PMID: 12440767
  61. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox).
    Plant J. 1998 May;14(3):365-70 PMID: 9628030
Article Info
Journal
Current genetics
Abbr.
Curr Genet
ISSN
0172-8083
DOI
10.1007/s00294-005-0044-z
Published
2006-03-00
Epub
2005-00-13
Pages
190-204
Language
English
Region
United States
NLM ID
8004904
Subset
IM
External Links
PubMed source DOI: 10.1007/s00294-005-0044-z View journal details
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: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2