Home LiteratureArticle Details
PMID: 7599316 Published · ppublish English Comparative Study Journal Article

The marine red alga Chondrus crispus has a highly divergent beta-tubulin gene with a characteristic 5' intron: functional and evolutionary implications.

Plant molecular biology ·Vol. 28 ·No. 2 ·1995-05-00 ·Pages 313-25

Liaud MF, Brandt U, Cerff R

Abstract

We characterized a nuclear gene and its corresponding cDNA encoding beta-tubulin (gene TubB1) of the marine red alga Chondrus crispus. The deduced TubB1 protein is the most divergent beta-tubulin so far reported with only 64 to 69% amino acid identity relative to other beta-tubulins from higher and lower eukaryotes. Our analysis reveals that TubB1 has an accelerated evolutionary rate probably due to a release of functional constraints in connexion with a specialization of microtubular structures in rhodophytes. It further indicates that isoform diversity and functional differentiation of tubulins in eukaryotic cells may be controlled by independent selective constraints. TubB1 has a short spliceosomal intron at its 5' end which seems to be a characteristic feature of nuclear protein-coding genes from rhodophytes. The splice junctions of the four known rhodophyte introns comply well with the corresponding consensus sequences of higher plants in agreement with previous suggestions from phylogenetic inference that red algae and green plants may be sister groups. The paucity and asymmetrical location of introns in rhodophyte genes can be explained by differential intron loss due to conversion of genes by homologous recombination with cDNAs corresponding to reverse transcribed mRNAs or partially spliced pre-mRNAs, respectively. The identification of an intron containing TubB1 cDNA in C. crispus confirms that pre-mRNAs can escape both splicing and degradation in the nucleus prior to transport into the cytoplasm. Differential Southern hybridizations under non-stringent conditions with homologous and heterologous probes suggest that C. crispus contains a second degenerate beta-tubulin gene (or pseudogene?) which, however, is only distantly related to TubB1 as it is to the more conserved homologues of other organisms.

Related Genes
MeSH Terms
Amino Acid Sequence Base Sequence Blotting, Southern DNA, Complementary/genetics Genomic Library Introns/genetics Marine Biology Molecular Sequence Data Phylogeny Polymerase Chain Reaction RNA Splicing Rhodophyta/genetics Sequence Analysis, DNA Sequence Homology, Amino Acid Sequence Homology, Nucleic Acid Tubulin/genetics
Chemicals
DNA, Complementary Tubulin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Liaud M F
Institut für Genetik, Technische Universität Braunschweig, Germany.
Brandt U
Cerff R
References (51)
51 references, click to expand
  1. Origin of the algae.
    Nature. 1989 May 11;339(6220):142-4 PMID: 2716835
  2. Expression of beta 1 tubulin (beta Tub56D) in Drosophila testis stem cells is regulated by a short upstream sequence while intron elements guide expression in somatic cells.
    Mol Gen Genet. 1993 Nov;241(3-4):263-70 PMID: 8246879
  3. Free intermingling of mammalian beta-tubulin isotypes among functionally distinct microtubules.
    Cell. 1987 May 22;49(4):539-48 PMID: 3552250
  4. Characterization of two divergent beta-tubulin genes from Colletotrichum graminicola.
    Gene. 1990 Feb 14;86(2):163-70 PMID: 2323570
  5. Pseudogenes in yeast?
    Cell. 1987 Apr 10;49(1):5-6 PMID: 3549000
  6. Intron existence predated the divergence of eukaryotes and prokaryotes.
    Science. 1988 Nov 25;242(4882):1164-6 PMID: 3055302
  7. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  8. cDNA cloning and characterization of the nuclear gene encoding chloroplast glyceraldehyde-3-phosphate dehydrogenase from the marine red alga Gracilaria verrucosa.
    Curr Genet. 1993 May-Jun;23(5-6):483-9 PMID: 7916671
  9. Preferential expression of one beta-tubulin gene during flagellate development in Physarum.
    J Gen Microbiol. 1992 Jan;138(1):229-38 PMID: 1556551
  10. The evolutionary origin of red algae as deduced from the nuclear genes encoding cytosolic and chloroplast glyceraldehyde-3-phosphate dehydrogenases from Chondrus crispus.
    J Mol Evol. 1994 Apr;38(4):319-27 PMID: 8007000
  11. Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8692-6 PMID: 8378350
  12. Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins.
    Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11558-62 PMID: 8265589
  13. Structure, evolution and anaerobic regulation of a nuclear gene encoding cytosolic glyceraldehyde-3-phosphate dehydrogenase from maize.
    J Mol Biol. 1989 Aug 20;208(4):551-65 PMID: 2810356
  14. Generation of antisera that discriminate among mammalian alpha-tubulins: introduction of specialized isotypes into cultured cells results in their coassembly without disruption of normal microtubule function.
    J Cell Biol. 1988 Jun;106(6):2011-22 PMID: 3290224
  15. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum.
    Anal Biochem. 1984 Feb;137(1):266-7 PMID: 6329026
  16. The two beta-tubulin genes of Chlamydomonas reinhardtii code for identical proteins.
    Mol Cell Biol. 1984 Dec;4(12):2686-96 PMID: 6098820
  17. Differential intron loss and endosymbiotic transfer of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes to the nucleus.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8918-22 PMID: 2247465
  18. Intron conservation across the prokaryote-eukaryote boundary: structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2672-6 PMID: 3357887
  19. Five identical intron positions in ancient duplicated genes of eubacterial origin.
    Nature. 1994 Jan 27;367(6461):387-9 PMID: 8114942
  20. Beta-tubulins are encoded by at least four genes in the brown alga Ectocarpus variabilis.
    Plant Mol Biol. 1991 Sep;17(3):487-92 PMID: 1883999
  21. Microtubule Components of the Plant Cell Cytoskeleton.
    Plant Physiol. 1994 Jan;104(1):1-6 PMID: 12232055
  22. The exon theory of genes.
    Cold Spring Harb Symp Quant Biol. 1987;52:901-5 PMID: 2456887
  23. Molecular phylogenetic analysis of actin genic regions from Achlya bisexualis (Oomycota) and Costaria costata (Chromophyta).
    J Mol Evol. 1991 Dec;33(6):525-36 PMID: 1779434
  24. Perspectives on tubulin isotype function and evolution based on the observation that Tetrahymena thermophila microtubules contain a single alpha- and beta-tubulin.
    Cell Motil Cytoskeleton. 1993;25(3):243-53 PMID: 8221902
  25. Intron splicing and intron-mediated enhanced expression in monocots.
    Prog Nucleic Acid Res Mol Biol. 1992;42:229-57 PMID: 1574588
  26. Genomic structure, expression and evolution of the alfalfa aspartate aminotransferase genes.
    Plant Mol Biol. 1994 Jun;25(3):387-99 PMID: 8049365
  27. Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1- mutant.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7034-8 PMID: 8346213
  28. Sequences that confer beta-tubulin autoregulation through modulated mRNA stability reside within exon 1 of a beta-tubulin mRNA.
    Cell. 1987 Aug 28;50(5):671-9 PMID: 3621343
  29. The GAPDH gene system of the red alga Chondrus crispus: promoter structures, intron/exon organization, genomic complexity and differential expression of genes.
    Plant Mol Biol. 1993 Dec;23(5):981-94 PMID: 8260635
  30. Strong functional GC pressure in a light-regulated maize gene encoding subunit GAPA of chloroplast glyceraldehyde-3-phosphate dehydrogenase: implications for the evolution of GAPA pseudogenes.
    J Mol Evol. 1989 Nov;29(5):412-21 PMID: 2515291
  31. Limited expression of a diverged beta-tubulin gene during soybean (Glycine max [L.] Merr.) development.
    Plant Mol Biol. 1991 Feb;16(2):225-34 PMID: 1716497
  32. Structural features and phylogeny of the actin gene of Chondrus crispus (Gigartinales, Rhodophyta).
    Curr Genet. 1995 Jul;28(2):164-72 PMID: 8590468
  33. Structural analysis of mutations in the Drosophila beta 2-tubulin isoform reveals regions in the beta-tubulin molecular required for general and for tissue-specific microtubule functions.
    Genetics. 1995 Jan;139(1):267-86 PMID: 7705629
  34. Nucleotide sequence and expression of two beta-tubulin genes in Stylonychia lemnae.
    J Mol Biol. 1987 Dec 20;198(4):643-53 PMID: 3123702
  35. The beta-tubulin gene family of pea: primary structures, genomic organization and intron-dependent evolution of genes.
    Plant Mol Biol. 1992 Feb;18(4):639-51 PMID: 1558942
  36. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia.
    Science. 1989 Jan 6;243(4887):75-7 PMID: 2911720
  37. Are tubulin isotypes functionally significant.
    Mol Biol Cell. 1993 May;4(5):445-57 PMID: 8334301
  38. Functions of microtubules in the Saccharomyces cerevisiae cell cycle.
    J Cell Biol. 1988 Oct;107(4):1409-26 PMID: 3049620
  39. Tubulin synthesis, structure, and function: what are the relationships?
    Biochem Cell Biol. 1989 Nov-Dec;67(11-12):770-90 PMID: 2695144
  40. CLUSTAL V: improved software for multiple sequence alignment.
    Comput Appl Biosci. 1992 Apr;8(2):189-91 PMID: 1591615
  41. Molecular biology and genetics of tubulin.
    Annu Rev Biochem. 1985;54:331-65 PMID: 3896122
  42. Plant transcription factors: present knowledge and future challenges.
    Trends Genet. 1992 Jan;8(1):22-7 PMID: 1369731
  43. A chicken-yeast chimeric beta-tubulin protein is incorporated into mouse microtubules in vivo.
    Cell. 1986 Feb 14;44(3):461-8 PMID: 3753663
  44. The triosephosphate isomerase gene from maize: introns antedate the plant-animal divergence.
    Cell. 1986 Jul 4;46(1):133-41 PMID: 3755078
  45. Physical evidence for cotranslational regulation of beta-tubulin mRNA degradation.
    Mol Cell Biol. 1992 Feb;12(2):791-9 PMID: 1732744
  46. Alpha-tubulin II is a male-specific protein in Plasmodium falciparum.
    Mol Biochem Parasitol. 1992 Dec;56(2):239-50 PMID: 1484548
  47. Intron-dependent transient expression of the maize GapA1 gene.
    Plant Mol Biol. 1995 Jul;28(4):667-76 PMID: 7647299
  48. Cloning and characterization of the nuclear gene encoding plastid glyceraldehyde-3-phosphate dehydrogenase from the marine red alga Gracilaria verrucosa.
    Curr Genet. 1994 Jul;26(1):79-86 PMID: 7954900
  49. The mammalian beta-tubulin repertoire: hematopoietic expression of a novel, heterologous beta-tubulin isotype.
    J Cell Biol. 1986 Nov;103(5):1903-10 PMID: 3782288
  50. The alpha- and beta-tubulins of Toxoplasma gondii are encoded by single copy genes containing multiple introns.
    Mol Biochem Parasitol. 1988 Jun;29(2-3):261-73 PMID: 3412377
  51. Tracing origins with molecular sequences: metazoan and eukaryotic beginnings.
    Trends Biochem Sci. 1991 Feb;16(2):46-50 PMID: 1858129
Article Info
Journal
Plant molecular biology
Abbr.
Plant Mol Biol
ISSN
0167-4412
Published
1995-05-00
Pages
313-25
Language
English
Region
Netherlands
NLM ID
9106343
Subset
IM
Databases
GENBANK
X71784, X71785
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