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. 1996 Jan;8(1):15–30. doi: 10.1105/tpc.8.1.15

Conserved expression of the Arabidopsis ACT1 and ACT 3 actin subclass in organ primordia and mature pollen.

Y Q An 1, S Huang 1, J M McDowell 1, E C McKinney 1, R B Meagher 1
PMCID: PMC161078  PMID: 8597657

Abstract

We have proposed that ancient and divergent classes of plant actin genes have been preserved throughout vascular plant evolution, because they have distinct patterns of gene regulation. The hypothesis was explored for ACT1 and ACT3, which represent one of the six ancient subclasses in the Arabidopsis actin gene family. Comparison of ACT1 and ACT3 cDNA and genomic sequences revealed highly divergent flaking and intron sequences, whereas they encoded nearly identical proteins. Quantification of their level of divergence suggests that they have not shared a common ancestor for 30 to 60 million years. Gene-specific RNA gel blot hybridization and reverse transcriptase-polymerase chain reaction analyses demonstrated that the distribution of ACT1 and ACT3 mRNAs was very similar: both preferentially accumulated at high levels in mature pollen and at very low levels in the other major organs. The 5' flanking regions of both genes, including the promoter, leader exon and intron, and the first 19 condons, were fused to the beta-glucuronidase (GUS) reporter gene. The expression of these reporter fusions was examined in a large number of transgenic Arabidopsis plants. Histochemical assays demonstrated that both ACT1-GUS and ACT3-GUS constructs were expressed preferentially in pollen, pollen tubes, and in all organ primordia, including those in roots shoots, and the inflorescence. Comparison of the 5' flanking regions of ACT1 and ACT3 revealed a number of short conserved sequences, which may direct their common transcriptional and post-transcriptional regulation. The expression patterns observed were distinct from those of any other other Arabidopsis actin subclass. The conservation of their expression pattern and amino acid sequences suggests that this actin subclass plays a distinct and required role in the plant cytoskeleton.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baird W. V., Meagher R. B. A complex gene superfamily encodes actin in petunia. EMBO J. 1987 Nov;6(11):3223–3231. doi: 10.1002/j.1460-2075.1987.tb02639.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Carpenter J. L., Ploense S. E., Snustad D. P., Silflow C. D. Preferential expression of an alpha-tubulin gene of Arabidopsis in pollen. Plant Cell. 1992 May;4(5):557–571. doi: 10.1105/tpc.4.5.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cavener D. R. Combinatorial control of structural genes in Drosophila: solutions that work for the animal. Bioessays. 1987 Sep;7(3):103–107. doi: 10.1002/bies.950070303. [DOI] [PubMed] [Google Scholar]
  4. Cooney M., Czernuszewicz G., Postel E. H., Flint S. J., Hogan M. E. Site-specific oligonucleotide binding represses transcription of the human c-myc gene in vitro. Science. 1988 Jul 22;241(4864):456–459. doi: 10.1126/science.3293213. [DOI] [PubMed] [Google Scholar]
  5. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dickinson W. J. On the architecture of regulatory systems: evolutionary insights and implications. Bioessays. 1988 Jun;8(6):204–208. doi: 10.1002/bies.950080608. [DOI] [PubMed] [Google Scholar]
  7. Drouin G., Dover G. A. Independent gene evolution in the potato actin gene family demonstrated by phylogenetic procedures for resolving gene conversions and the phylogeny of angiosperm actin genes. J Mol Evol. 1990 Aug;31(2):132–150. doi: 10.1007/BF02109482. [DOI] [PubMed] [Google Scholar]
  8. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  9. Foley K. P., Engel J. D. Individual stage selector element mutations lead to reciprocal changes in beta- vs. epsilon-globin gene transcription: genetic confirmation of promoter competition during globin gene switching. Genes Dev. 1992 May;6(5):730–744. doi: 10.1101/gad.6.5.730. [DOI] [PubMed] [Google Scholar]
  10. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hemerly A. S., Ferreira P., de Almeida Engler J., Van Montagu M., Engler G., Inzé D. cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell. 1993 Dec;5(12):1711–1723. doi: 10.1105/tpc.5.12.1711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hightower R. C., Meagher R. B. Divergence and differential expression of soybean actin genes. EMBO J. 1985 Jan;4(1):1–8. doi: 10.1002/j.1460-2075.1985.tb02309.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jefferson R. A., Kavanagh T. A., Bevan M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kozak M. The scanning model for translation: an update. J Cell Biol. 1989 Feb;108(2):229–241. doi: 10.1083/jcb.108.2.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Logemann J., Schell J., Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987 May 15;163(1):16–20. doi: 10.1016/0003-2697(87)90086-8. [DOI] [PubMed] [Google Scholar]
  16. Lu G., Ferl R. J. Site-specific oligodeoxynucleotide binding to maize Adh1 gene promoter represses Adh1-GUS gene expression in vivo. Plant Mol Biol. 1992 Aug;19(5):715–723. doi: 10.1007/BF00027068. [DOI] [PubMed] [Google Scholar]
  17. Mascarenhas J. P. Molecular Mechanisms of Pollen Tube Growth and Differentiation. Plant Cell. 1993 Oct;5(10):1303–1314. doi: 10.1105/tpc.5.10.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McElroy D., Rothenberg M., Reece K. S., Wu R. Characterization of the rice (Oryza sativa) actin gene family. Plant Mol Biol. 1990 Aug;15(2):257–268. doi: 10.1007/BF00036912. [DOI] [PubMed] [Google Scholar]
  19. McElroy D., Zhang W., Cao J., Wu R. Isolation of an efficient actin promoter for use in rice transformation. Plant Cell. 1990 Feb;2(2):163–171. doi: 10.1105/tpc.2.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McHugh K. M., Crawford K., Lessard J. L. A comprehensive analysis of the developmental and tissue-specific expression of the isoactin multigene family in the rat. Dev Biol. 1991 Dec;148(2):442–458. doi: 10.1016/0012-1606(91)90263-3. [DOI] [PubMed] [Google Scholar]
  21. McKinney E. C., Ali N., Traut A., Feldmann K. A., Belostotsky D. A., McDowell J. M., Meagher R. B. Sequence-based identification of T-DNA insertion mutations in Arabidopsis: actin mutants act2-1 and act4-1. Plant J. 1995 Oct;8(4):613–622. doi: 10.1046/j.1365-313x.1995.8040613.x. [DOI] [PubMed] [Google Scholar]
  22. McLean B. G., Eubanks S., Meagher R. B. Tissue-specific expression of divergent actins in soybean root. Plant Cell. 1990 Apr;2(4):335–344. doi: 10.1105/tpc.2.4.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Meagher R. B., Berry-Lowe S., Rice K. Molecular evolution of the small subunit of ribulose bisphosphate carboxylase: nucleotide substitution and gene conversion. Genetics. 1989 Dec;123(4):845–863. doi: 10.1093/genetics/123.4.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Medford J. I., Elmer J. S., Klee H. J. Molecular cloning and characterization of genes expressed in shoot apical meristems. Plant Cell. 1991 Apr;3(4):359–370. doi: 10.1105/tpc.3.4.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Meyerowitz E. M. Arabidopsis, a useful weed. Cell. 1989 Jan 27;56(2):263–269. doi: 10.1016/0092-8674(89)90900-8. [DOI] [PubMed] [Google Scholar]
  26. Mueller P. R., Wold B. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science. 1989 Nov 10;246(4931):780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]
  27. Nairn C. J., Winesett L., Ferl R. J. Nucleotide sequence of an actin gene from Arabidopsis thaliana. Gene. 1988 May 30;65(2):247–257. doi: 10.1016/0378-1119(88)90461-1. [DOI] [PubMed] [Google Scholar]
  28. Palevitz B. A. Actin in the preprophase band of Allium cepa. J Cell Biol. 1987 Jun;104(6):1515–1519. doi: 10.1083/jcb.104.6.1515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Senecoff J. F., Meagher R. B. Isolating the Arabidopsis thaliana genes for de novo purine synthesis by suppression of Escherichia coli mutants. I. 5'-Phosphoribosyl-5-aminoimidazole synthetase. Plant Physiol. 1993 Jun;102(2):387–399. doi: 10.1104/pp.102.2.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shimada T., Fujii H., Lin H. A 165-base pair sequence between the dihydrofolate reductase gene and the divergently transcribed upstream gene is sufficient for bidirectional transcriptional activity. J Biol Chem. 1989 Dec 5;264(34):20171–20174. [PubMed] [Google Scholar]
  31. Tanzer M. M., Meagher R. B. Faithful degradation of soybean rbcS mRNA in vitro. Mol Cell Biol. 1994 Apr;14(4):2640–2650. doi: 10.1128/mcb.14.4.2640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thompson D. M., Tanzer M. M., Meagher R. B. Degradation products of the mRNA encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean and transgenic petunia. Plant Cell. 1992 Jan;4(1):47–58. doi: 10.1105/tpc.4.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Twell D., Yamaguchi J., McCormick S. Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development. 1990 Jul;109(3):705–713. doi: 10.1242/dev.109.3.705. [DOI] [PubMed] [Google Scholar]
  34. Zhang W., McElroy D., Wu R. Analysis of rice Act1 5' region activity in transgenic rice plants. Plant Cell. 1991 Nov;3(11):1155–1165. doi: 10.1105/tpc.3.11.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]

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