Skip to main content
Genetics logoLink to Genetics
. 1999 May;152(1):461–476. doi: 10.1093/genetics/152.1.461

Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes.

D Perazza 1, M Herzog 1, M Hülskamp 1, S Brown 1, A M Dorne 1, J M Bonneville 1
PMCID: PMC1460599  PMID: 10224275

Abstract

Leaf trichomes in Arabidopsis are unicellular epidermal hairs with a branched morphology. They undergo successive endoreduplication rounds early during cell morphogenesis. Mutations affecting trichome nuclear DNA content, such as triptychon or glabra3, alter trichome branching. We isolated new mutants with supernumerary trichome branches, which fall into three unlinked complementation groups: KAKTUS and the novel loci, POLYCHOME and RASTAFARI. They map to chromosomes IV, II, and V, respectively. The trichomes of these mutants presented an increased DNA content, although to a variable extent. The spindly-5 mutant, which displays a constitutive gibberellin response, also produces overbranched trichomes containing more nuclear DNA. We analyzed genetic interactions using double mutants and propose that two independent pathways, defined by SPINDLY and TRIPTYCHON, act to limit trichome growth. KAKTUS and POLYCHOME might have redundant actions mediating gibberellin control via SPINDLY. The overall leaf polysomaty was not notably affected by these mutations, suggesting that they affect the control of DNA synthesis in a tissue- or cell type-specific manner. Wild-type tetraploids also produce overbranched trichomes; they displayed a shifted polysomaty in trichomes and in the whole leaf, suggesting a developmental program controlling DNA increases via the counting of endoreduplication rounds.

Full Text

The Full Text of this article is available as a PDF (965.6 KB).

Selected References

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

  1. Bell C. J., Ecker J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994 Jan 1;19(1):137–144. doi: 10.1006/geno.1994.1023. [DOI] [PubMed] [Google Scholar]
  2. Chien J. C., Sussex I. M. Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 1996 Aug;111(4):1321–1328. doi: 10.1104/pp.111.4.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Doerner P., Jørgensen J. E., You R., Steppuhn J., Lamb C. Control of root growth and development by cyclin expression. Nature. 1996 Apr 11;380(6574):520–523. doi: 10.1038/380520a0. [DOI] [PubMed] [Google Scholar]
  4. Eisner T., Eisner M., Hoebeke E. R. When defense backfires: detrimental effect of a plant's protective trichomes on an insect beneficial to the plant. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4410–4414. doi: 10.1073/pnas.95.8.4410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Esch J. J., Oppenheimer D. G., Marks M. D. Characterization of a weak allele of the GL1 gene of Arabidopsis thaliana. Plant Mol Biol. 1994 Jan;24(1):203–207. doi: 10.1007/BF00040586. [DOI] [PubMed] [Google Scholar]
  6. Folkers U., Berger J., Hülskamp M. Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. Development. 1997 Oct;124(19):3779–3786. doi: 10.1242/dev.124.19.3779. [DOI] [PubMed] [Google Scholar]
  7. Galbraith D. W., Harkins K. R., Knapp S. Systemic Endopolyploidy in Arabidopsis thaliana. Plant Physiol. 1991 Jul;96(3):985–989. doi: 10.1104/pp.96.3.985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Galway M. E., Masucci J. D., Lloyd A. M., Walbot V., Davis R. W., Schiefelbein J. W. The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol. 1994 Dec;166(2):740–754. doi: 10.1006/dbio.1994.1352. [DOI] [PubMed] [Google Scholar]
  9. Gendreau E., Höfte H., Grandjean O., Brown S., Traas J. Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J. 1998 Jan;13(2):221–230. doi: 10.1046/j.1365-313x.1998.00030.x. [DOI] [PubMed] [Google Scholar]
  10. Gendreau E., Traas J., Desnos T., Grandjean O., Caboche M., Höfte H. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 1997 May;114(1):295–305. doi: 10.1104/pp.114.1.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Guarente L. Synthetic enhancement in gene interaction: a genetic tool come of age. Trends Genet. 1993 Oct;9(10):362–366. doi: 10.1016/0168-9525(93)90042-g. [DOI] [PubMed] [Google Scholar]
  12. Hemerly A., Engler J. de A., Bergounioux C., Van Montagu M., Engler G., Inzé D., Ferreira P. Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 1995 Aug 15;14(16):3925–3936. doi: 10.1002/j.1460-2075.1995.tb00064.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hülskamp M., Schnittger A. Spatial regulation of trichome formation in Arabidopsis thaliana. Semin Cell Dev Biol. 1998 Apr;9(2):213–220. doi: 10.1006/scdb.1997.0209. [DOI] [PubMed] [Google Scholar]
  14. Jacobsen S. E., Binkowski K. A., Olszewski N. E. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9292–9296. doi: 10.1073/pnas.93.17.9292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jacobsen S. E., Olszewski N. E. Characterization of the Arrest in Anther Development Associated with Gibberellin Deficiency of the gib-1 Mutant of Tomato. Plant Physiol. 1991 Sep;97(1):409–414. doi: 10.1104/pp.97.1.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jacobsen S. E., Olszewski N. E. Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell. 1993 Aug;5(8):887–896. doi: 10.1105/tpc.5.8.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kominami K., Toda T. Fission yeast WD-repeat protein pop1 regulates genome ploidy through ubiquitin-proteasome-mediated degradation of the CDK inhibitor Rum1 and the S-phase initiator Cdc18. Genes Dev. 1997 Jun 15;11(12):1548–1560. doi: 10.1101/gad.11.12.1548. [DOI] [PubMed] [Google Scholar]
  18. Koornneef M., Alonso-Blanco C., Blankestijn-de Vries H., Hanhart C. J., Peeters A. J. Genetic interactions among late-flowering mutants of Arabidopsis. Genetics. 1998 Feb;148(2):885–892. doi: 10.1093/genetics/148.2.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Koornneef M., Dellaert L. W., van der Veen J. H. EMS- and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh. Mutat Res. 1982 Mar;93(1):109–123. doi: 10.1016/0027-5107(82)90129-4. [DOI] [PubMed] [Google Scholar]
  20. Larkin J. C., Oppenheimer D. G., Lloyd A. M., Paparozzi E. T., Marks M. D. Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA Genes in Arabidopsis Trichome Development. Plant Cell. 1994 Aug;6(8):1065–1076. doi: 10.1105/tpc.6.8.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Larkin J. C., Oppenheimer D. G., Pollock S., Marks M. D. Arabidopsis GLABROUS1 Gene Requires Downstream Sequences for Function. Plant Cell. 1993 Dec;5(12):1739–1748. doi: 10.1105/tpc.5.12.1739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lilly M. A., Spradling A. C. The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev. 1996 Oct 1;10(19):2514–2526. doi: 10.1101/gad.10.19.2514. [DOI] [PubMed] [Google Scholar]
  23. Manly K. F. A Macintosh program for storage and analysis of experimental genetic mapping data. Mamm Genome. 1993;4(6):303–313. doi: 10.1007/BF00357089. [DOI] [PubMed] [Google Scholar]
  24. Marks M. D., Feldmann K. A. Trichome Development in Arabidopsis thaliana. I. T-DNA Tagging of the GLABROUS1 Gene. Plant Cell. 1989 Nov;1(11):1043–1050. doi: 10.1105/tpc.1.11.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Melaragno J. E., Mehrotra B., Coleman A. W. Relationship between Endopolyploidy and Cell Size in Epidermal Tissue of Arabidopsis. Plant Cell. 1993 Nov;5(11):1661–1668. doi: 10.1105/tpc.5.11.1661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moreno S., Nurse P. Regulation of progression through the G1 phase of the cell cycle by the rum1+ gene. Nature. 1994 Jan 20;367(6460):236–242. doi: 10.1038/367236a0. [DOI] [PubMed] [Google Scholar]
  27. Nishitani H., Nurse P. p65cdc18 plays a major role controlling the initiation of DNA replication in fission yeast. Cell. 1995 Nov 3;83(3):397–405. doi: 10.1016/0092-8674(95)90117-5. [DOI] [PubMed] [Google Scholar]
  28. Oppenheimer D. G., Herman P. L., Sivakumaran S., Esch J., Marks M. D. A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell. 1991 Nov 1;67(3):483–493. doi: 10.1016/0092-8674(91)90523-2. [DOI] [PubMed] [Google Scholar]
  29. Oppenheimer D. G., Pollock M. A., Vacik J., Szymanski D. B., Ericson B., Feldmann K., Marks M. D. Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6261–6266. doi: 10.1073/pnas.94.12.6261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Perazza D, Vachon G, Herzog M. Gibberellins promote trichome formation by Up-regulating GLABROUS1 in arabidopsis . Plant Physiol. 1998 Jun;117(2):375–383. doi: 10.1104/pp.117.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pickett F. B., Meeks-Wagner D. R. Seeing double: appreciating genetic redundancy. Plant Cell. 1995 Sep;7(9):1347–1356. doi: 10.1105/tpc.7.9.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rerie W. G., Feldmann K. A., Marks M. D. The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev. 1994 Jun 15;8(12):1388–1399. doi: 10.1101/gad.8.12.1388. [DOI] [PubMed] [Google Scholar]
  33. Robertson M., Swain S. M., Chandler P. M., Olszewski N. E. Identification of a negative regulator of gibberellin action, HvSPY, in barley. Plant Cell. 1998 Jun;10(6):995–1007. doi: 10.1105/tpc.10.6.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sauter M., Mekhedov S. L., Kende H. Gibberellin promotes histone H1 kinase activity and the expression of cdc2 and cyclin genes during the induction of rapid growth in deepwater rice internodes. Plant J. 1995 Apr;7(4):623–632. doi: 10.1046/j.1365-313x.1995.7040623.x. [DOI] [PubMed] [Google Scholar]
  35. Schnittger A., Jürgens G., Hülskamp M. Tissue layer and organ specificity of trichome formation are regulated by GLABRA1 and TRIPTYCHON in Arabidopsis. Development. 1998 Jun;125(12):2283–2289. doi: 10.1242/dev.125.12.2283. [DOI] [PubMed] [Google Scholar]
  36. Sun Tp., Goodman H. M., Ausubel F. M. Cloning the Arabidopsis GA1 Locus by Genomic Subtraction. Plant Cell. 1992 Feb;4(2):119–128. doi: 10.1105/tpc.4.2.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Szymanski D. B., Klis D. A., Larkin J. C., Marks M. D. cot1: a regulator of Arabidopsis trichome initiation. Genetics. 1998 Jun;149(2):565–577. doi: 10.1093/genetics/149.2.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Szymanski D. B., Marks M. D. GLABROUS1 overexpression and TRIPTYCHON alter the cell cycle and trichome cell fate in Arabidopsis. Plant Cell. 1998 Dec;10(12):2047–2062. doi: 10.1105/tpc.10.12.2047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Telfer A., Bollman K. M., Poethig R. S. Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development. 1997 Feb;124(3):645–654. doi: 10.1242/dev.124.3.645. [DOI] [PubMed] [Google Scholar]
  40. Wagner G. J. Secreting glandular trichomes: more than just hairs. Plant Physiol. 1991 Jul;96(3):675–679. doi: 10.1104/pp.96.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wilson R. N., Somerville C. R. Phenotypic Suppression of the Gibberellin-Insensitive Mutant (gai) of Arabidopsis. Plant Physiol. 1995 Jun;108(2):495–502. doi: 10.1104/pp.108.2.495. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES