Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1998 Jun;149(2):717–725. doi: 10.1093/genetics/149.2.717

Detection of deleterious genotypes in multigenerational studies. I. Disruptions in individual Arabidopsis actin genes.

L U Gilliland 1, E C McKinney 1, M A Asmussen 1, R B Meagher 1
PMCID: PMC1460190  PMID: 9611186

Abstract

Plant actins are involved in numerous cytoskeletal processes effecting plant development, including cell division plane determination, cell elongation, and cell wall deposition. Arabidopsis thaliana has five ancient subclasses of actin with distinct patterns of spatial and temporal expression. To test their functional roles, we identified insertion mutants in three Arabidopsis actin genes, ACT2, ACT4, and ACT7, representing three subclasses. Adult plants homozygous for the act2-1, act4-1, and act7-1 mutant alleles appear to be robust, morphologically normal, and fully fertile. However, when grown as populations descended from a single heterozygous parent, all three mutant alleles were found at extremely low frequencies relative to the wild-type in the F2 generation. Thus, all three mutant alleles appear to be deleterious. The act2-1 mutant allele was found at normal frequencies in the F1, but at significantly lower frequencies than expected in the F2 and F3 generations. These data suggest that the homozygous act2-1/act2-1 mutant adult plants have a reduced fitness in the 2N sporophytic portion of the life cycle, consistent with the vegetative expression of ACT2. These data are interpreted in light of the extreme conservation of plant actin subclasses and genetic redundancy.

Full Text

The Full Text of this article is available as a PDF (178.6 KB).

Selected References

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

  1. An Y. Q., Huang S., McDowell J. M., McKinney E. C., Meagher R. B. Conserved expression of the Arabidopsis ACT1 and ACT 3 actin subclass in organ primordia and mature pollen. Plant Cell. 1996 Jan;8(1):15–30. doi: 10.1105/tpc.8.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. An Y. Q., McDowell J. M., Huang S., McKinney E. C., Chambliss S., Meagher R. B. Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J. 1996 Jul;10(1):107–121. doi: 10.1046/j.1365-313x.1996.10010107.x. [DOI] [PubMed] [Google Scholar]
  3. Colucci-Guyon E., Portier M. M., Dunia I., Paulin D., Pournin S., Babinet C. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell. 1994 Nov 18;79(4):679–694. doi: 10.1016/0092-8674(94)90553-3. [DOI] [PubMed] [Google Scholar]
  4. De Lozanne A., Spudich J. A. Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science. 1987 May 29;236(4805):1086–1091. doi: 10.1126/science.3576222. [DOI] [PubMed] [Google Scholar]
  5. Hanks M., Wurst W., Anson-Cartwright L., Auerbach A. B., Joyner A. L. Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science. 1995 Aug 4;269(5224):679–682. doi: 10.1126/science.7624797. [DOI] [PubMed] [Google Scholar]
  6. Huang S., An Y. Q., McDowell J. M., McKinney E. C., Meagher R. B. The Arabidopsis ACT11 actin gene is strongly expressed in tissues of the emerging inflorescence, pollen, and developing ovules. Plant Mol Biol. 1997 Jan;33(1):125–139. doi: 10.1023/a:1005741514764. [DOI] [PubMed] [Google Scholar]
  7. Huang S., An Y. Q., McDowell J. M., McKinney E. C., Meagher R. B. The Arabidopsis thaliana ACT4/ACT12 actin gene subclass is strongly expressed throughout pollen development. Plant J. 1996 Aug;10(2):189–202. doi: 10.1046/j.1365-313x.1996.10020189.x. [DOI] [PubMed] [Google Scholar]
  8. Kimura M. Recent development of the neutral theory viewed from the Wrightian tradition of theoretical population genetics. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):5969–5973. doi: 10.1073/pnas.88.14.5969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Klimyuk V. I., Carroll B. J., Thomas C. M., Jones J. D. Alkali treatment for rapid preparation of plant material for reliable PCR analysis. Plant J. 1993 Mar;3(3):493–494. doi: 10.1111/j.1365-313x.1993.tb00169.x. [DOI] [PubMed] [Google Scholar]
  10. Li X., Noll M. Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions. Nature. 1994 Jan 6;367(6458):83–87. doi: 10.1038/367083a0. [DOI] [PubMed] [Google Scholar]
  11. McDowell J. M., An Y. Q., Huang S., McKinney E. C., Meagher R. B. The arabidopsis ACT7 actin gene is expressed in rapidly developing tissues and responds to several external stimuli. Plant Physiol. 1996 Jul;111(3):699–711. doi: 10.1104/pp.111.3.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. McDowell J. M., Huang S., McKinney E. C., An Y. Q., Meagher R. B. Structure and evolution of the actin gene family in Arabidopsis thaliana. Genetics. 1996 Feb;142(2):587–602. doi: 10.1093/genetics/142.2.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Meagher R. B. Divergence and differential expression of actin gene families in higher plants. Int Rev Cytol. 1991;125:139–163. doi: 10.1016/s0074-7696(08)61218-8. [DOI] [PubMed] [Google Scholar]
  15. Nowak M. A., Boerlijst M. C., Cooke J., Smith J. M. Evolution of genetic redundancy. Nature. 1997 Jul 10;388(6638):167–171. doi: 10.1038/40618. [DOI] [PubMed] [Google Scholar]
  16. Oliver S. G., van der Aart Q. J., Agostoni-Carbone M. L., Aigle M., Alberghina L., Alexandraki D., Antoine G., Anwar R., Ballesta J. P., Benit P. The complete DNA sequence of yeast chromosome III. Nature. 1992 May 7;357(6373):38–46. doi: 10.1038/357038a0. [DOI] [PubMed] [Google Scholar]
  17. Purrington C. B., Bergelson J. Fitness consequences of genetically engineered herbicide and antibiotic resistance in Arabidopsis thaliana. Genetics. 1997 Mar;145(3):807–814. doi: 10.1093/genetics/145.3.807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rudnicki M. A., Braun T., Hinuma S., Jaenisch R. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell. 1992 Oct 30;71(3):383–390. doi: 10.1016/0092-8674(92)90508-a. [DOI] [PubMed] [Google Scholar]
  19. Thomas J. H. Thinking about genetic redundancy. Trends Genet. 1993 Nov;9(11):395–399. doi: 10.1016/0168-9525(93)90140-d. [DOI] [PubMed] [Google Scholar]
  20. Witke W., Schleicher M., Noegel A. A. Redundancy in the microfilament system: abnormal development of Dictyostelium cells lacking two F-actin cross-linking proteins. Cell. 1992 Jan 10;68(1):53–62. doi: 10.1016/0092-8674(92)90205-q. [DOI] [PubMed] [Google Scholar]
  21. Zwaal R. R., Broeks A., van Meurs J., Groenen J. T., Plasterk R. H. Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7431–7435. doi: 10.1073/pnas.90.16.7431. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES