Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1996 Oct;112(2):705–715. doi: 10.1104/pp.112.2.705

Novel molecular markers for late phases of the growth cycle of Arabidopsis thaliana cell-suspension cultures are expressed during organ senescence.

D Callard 1, M Axelos 1, L Mazzolini 1
PMCID: PMC157995  PMID: 8883383

Abstract

In an Arabidopsis thaliana T87-C3 cell-suspension culture, entry into the growth-arrest phase is rapidly followed by a loss of cell viability. Three cDNA clones, SRG1, SRG2, and SRG3, corresponding to genes with transcripts that accumulate during these late phases, were isolated by the mRNA differential display method. Amino acid sequence analysis shows that the putative SRG1 protein is a new member of the Fe(II)/ascorbate oxidase superfamily, and that SRG2 codes for a protein with significant homology to beta-glucosidases. Significantly, all three SRG genes are expressed in senescing organs of Arbidopsis plants. Two previously characterized genes, SAG2 and SAG4, induced during natural senescence in Arabidopsis, were also found to be expressed in cell-suspension cultures and have expression kinetics similar to those observed for the SRG1 gene. Taken together these finding suggest that certain molecular events are common to both plant senescence and growth arrest in arabidopsis cell suspensions. Both internucleosomal cleavage of nDNA and an apparent compaction of chromatin, two characteristic features of programmed cell death in animal cells, have been observed in Arabidopsis cell cultures at a stage corresponding to loss of cell viability.

Full Text

The Full Text of this article is available as a PDF (3.2 MB).

Selected References

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

  1. Apte S. S., Mattei M. G., Seldin M. F., Olsen B. R. The highly conserved defender against the death 1 (DAD1) gene maps to human chromosome 14q11-q12 and mouse chromosome 14 and has plant and nematode homologs. FEBS Lett. 1995 Apr 24;363(3):304–306. doi: 10.1016/0014-5793(95)00321-y. [DOI] [PubMed] [Google Scholar]
  2. Axelos M., Bardet C., Liboz T., Le Van Thai A., Curie C., Lescure B. The gene family encoding the Arabidopsis thaliana translation elongation factor EF-1 alpha: molecular cloning, characterization and expression. Mol Gen Genet. 1989 Oct;219(1-2):106–112. doi: 10.1007/BF00261164. [DOI] [PubMed] [Google Scholar]
  3. Bariola P. A., Howard C. J., Taylor C. B., Verburg M. T., Jaglan V. D., Green P. J. The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J. 1994 Nov;6(5):673–685. doi: 10.1046/j.1365-313x.1994.6050673.x. [DOI] [PubMed] [Google Scholar]
  4. Britsch L., Dedio J., Saedler H., Forkmann G. Molecular characterization of flavanone 3 beta-hydroxylases. Consensus sequence, comparison with related enzymes and the role of conserved histidine residues. Eur J Biochem. 1993 Oct 15;217(2):745–754. doi: 10.1111/j.1432-1033.1993.tb18301.x. [DOI] [PubMed] [Google Scholar]
  5. Chen M. H., Liu L. F., Chen Y. R., Wu H. K., Yu S. M. Expression of alpha-amylases, carbohydrate metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J. 1994 Nov;6(5):625–636. doi: 10.1046/j.1365-313x.1994.6050625.x. [DOI] [PubMed] [Google Scholar]
  6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  7. Crowell D. N., Amasino R. M. Induction of Specific mRNAs in Cultured Soybean Cells during Cytokinin or Auxin Starvation. Plant Physiol. 1991 Mar;95(3):711–715. doi: 10.1104/pp.95.3.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Dominov J. A., Stenzler L., Lee S., Schwarz J. J., Leisner S., Howell S. H. Cytokinins and auxins control the expression of a gene in Nicotiana plumbaginifolia cells by feedback regulation. Plant Cell. 1992 Apr;4(4):451–461. doi: 10.1105/tpc.4.4.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gräbnitz F., Seiss M., Rücknagel K. P., Staudenbauer W. L. Structure of the beta-glucosidase gene bglA of Clostridium thermocellum. Sequence analysis reveals a superfamily of cellulases and beta-glycosidases including human lactase/phlorizin hydrolase. Eur J Biochem. 1991 Sep 1;200(2):301–309. doi: 10.1111/j.1432-1033.1991.tb16186.x. [DOI] [PubMed] [Google Scholar]
  11. Henrissat B. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1991 Dec 1;280(Pt 2):309–316. doi: 10.1042/bj2800309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hensel L. L., Grbić V., Baumgarten D. A., Bleecker A. B. Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in arabidopsis. Plant Cell. 1993 May;5(5):553–564. doi: 10.1105/tpc.5.5.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hsieh H. M., Liu W. K., Huang P. C. A novel stress-inducible metallothionein-like gene from rice. Plant Mol Biol. 1995 Jun;28(3):381–389. doi: 10.1007/BF00020388. [DOI] [PubMed] [Google Scholar]
  14. Leah R., Kigel J., Svendsen I., Mundy J. Biochemical and molecular characterization of a barley seed beta-glucosidase. J Biol Chem. 1995 Jun 30;270(26):15789–15797. doi: 10.1074/jbc.270.26.15789. [DOI] [PubMed] [Google Scholar]
  15. Lee S. P., Chen T. H. Molecular cloning of abscisic acid-responsive mRNAs expressed during the induction of freezing tolerance in bromegrass (Bromus inermis Leyss) suspension culture. Plant Physiol. 1993 Mar;101(3):1089–1096. doi: 10.1104/pp.101.3.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lelievre J. M., Balague C., Pech J. C., Meyer Y. Protein synthesis associated with quiescence and senescence in auxin-starved pear cells. Plant Physiol. 1987 Oct;85(2):400–406. doi: 10.1104/pp.85.2.400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lhernould S., Karamanos Y., Priem B., Morvan H. Carbon starvation increases endoglycosidase activities and production of "unconjugated N-glycans" in Silene alba cell-suspension cultures. Plant Physiol. 1994 Oct;106(2):779–784. doi: 10.1104/pp.106.2.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McGarvey D. J., Sirevåg R., Christoffersen R. E. Ripening-related gene from avocado fruit : ethylene-inducible expression of the mRNA and polypeptide. Plant Physiol. 1992 Feb;98(2):554–559. doi: 10.1104/pp.98.2.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mittler R., Lam E. In Situ Detection of nDNA Fragmentation during the Differentiation of Tracheary Elements in Higher Plants. Plant Physiol. 1995 Jun;108(2):489–493. doi: 10.1104/pp.108.2.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Poulton J. E. Cyanogenesis in plants. Plant Physiol. 1990 Oct;94(2):401–405. doi: 10.1104/pp.94.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Raff M. C. Social controls on cell survival and cell death. Nature. 1992 Apr 2;356(6368):397–400. doi: 10.1038/356397a0. [DOI] [PubMed] [Google Scholar]
  22. Regad F., Bardet C., Tremousaygue D., Moisan A., Lescure B., Axelos M. cDNA cloning and expression of an Arabidopsis GTP-binding protein of the ARF family. FEBS Lett. 1993 Jan 25;316(2):133–136. doi: 10.1016/0014-5793(93)81201-a. [DOI] [PubMed] [Google Scholar]
  23. Roitsch T., Bittner M., Godt D. E. Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol. 1995 May;108(1):285–294. doi: 10.1104/pp.108.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Smyth D. R., Bowman J. L., Meyerowitz E. M. Early flower development in Arabidopsis. Plant Cell. 1990 Aug;2(8):755–767. doi: 10.1105/tpc.2.8.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tang X., Wang H., Brandt A. S., Woodson W. R. Organization and structure of the 1-aminocyclopropane-1-carboxylate oxidase gene family from Petunia hybrida. Plant Mol Biol. 1993 Dec;23(6):1151–1164. doi: 10.1007/BF00042349. [DOI] [PubMed] [Google Scholar]
  27. Taylor C. B., Bariola P. A., delCardayré S. B., Raines R. T., Green P. J. RNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5118–5122. doi: 10.1073/pnas.90.11.5118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tseng T. C., Tsai T. H., Lue M. Y., Lee H. T. Identification of sucrose-regulated genes in cultured rice cells using mRNA differential display. Gene. 1995 Aug 19;161(2):179–182. doi: 10.1016/0378-1119(95)00243-y. [DOI] [PubMed] [Google Scholar]
  29. Xu Y. L., Li L., Wu K., Peeters A. J., Gage D. A., Zeevaart J. A. The GA5 locus of Arabidopsis thaliana encodes a multifunctional gibberellin 20-oxidase: molecular cloning and functional expression. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6640–6644. doi: 10.1073/pnas.92.14.6640. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES