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PMID: 15908600 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Loss-of-function mutations of ROOT HAIR DEFECTIVE3 suppress root waving, skewing, and epidermal cell file rotation in Arabidopsis.

Plant physiology ·Vol. 138 ·No. 2 ·2005-06-00 ·Pages 701-14

Yuen CY, Sedbrook JC, Perrin RM, Carroll KL, Masson PH

Abstract

Wild-type Arabidopsis (Arabidopsis thaliana L. Heynh.) roots growing on a tilted surface of impenetrable hard-agar media adopt a wave-like pattern and tend to skew to the right of the gravity vector (when viewed from the back of the plate through the medium). Reversible root-tip rotation often accompanies the clockwise and counterclockwise curves that form each wave. These rotations are manifested by epidermal cell file rotation (CFR) along the root. Loss-of-function alleles of ROOT HAIR DEFECTIVE3 (RHD3), a gene previously implicated in the control of vesicle trafficking between the endoplasmic reticulum and the Golgi compartments, resulted in an almost complete suppression of epidermal CFR, root skewing, and waving on hard-agar surfaces. Several other root hair defective mutants (rhd2-1, rhd4-1, and rhd6-1) did not exhibit dramatic alterations in these root growth behaviors, suggesting that a generalized defect in root hair formation is not responsible for the surface-dependent phenotypes of rhd3. However, similar alterations in root growth behavior were observed in a variety of mutants characterized by defects in cell expansion (cob-1, cob-2, eto1-1, eto2-1, erh2-1, and erh3-1). The erh2-1 and rhd3-1 mutants differed from other anisotropic cell expansion mutants, though, by an inability to respond to low doses of the microtubule-binding drug propyzamide, which normally causes enhanced left-handed CFR and right skewing. We hypothesize that RHD3 may control epidermal CFR, root skewing, and waving on hard-agar surfaces by regulating the traffic of wall- or plasma membrane-associated determinants of anisotropic cell expansion.

Keywords
NASA Discipline Plant Biology Non-NASA Center
MeSH Terms
Arabidopsis/genetics,growth & development,metabolism Arabidopsis Proteins/genetics,physiology Base Sequence GTP-Binding Proteins/genetics,physiology Gene Expression Regulation, Plant Gravitropism Microtubules/physiology Molecular Sequence Data Mutation Phenotype Plant Epidermis/genetics,physiology Plant Roots/genetics,growth & development
Chemicals
Arabidopsis Proteins GTP-Binding Proteins RHD3 protein, Arabidopsis
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Yuen Christen Y L
Laboratory of Genetics, University of Wisconsin, Madison, Wisconsin 53706, USA.
Sedbrook John C
Perrin Robyn M
Carroll Kathleen L
Masson Patrick H
Investigators
1 investigators, click to expand
Masson P H
U WI, Madison
References (49)
49 references, click to expand
  1. T-DNA-associated duplication/translocations in Arabidopsis. Implications for mutant analysis and functional genomics.
    Plant Physiol. 2001 Aug;126(4):1527-38 PMID: 11500551
  2. Plant gravitropism. Unraveling the ups and downs of a complex process.
    Plant Physiol. 2003 Dec;133(4):1677-90 PMID: 14681531
  3. Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein.
    Plant Cell. 2002 Sep;14(9):2145-60 PMID: 12215512
  4. ARG1 (altered response to gravity) encodes a DnaJ-like protein that potentially interacts with the cytoskeleton.
    Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):1140-5 PMID: 9927707
  5. Conditional root expansion mutants of Arabidopsis.
    Development. 1995 Apr;121(4):1237-52 PMID: 7743935
  6. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein.
    Curr Biol. 2004 Aug 24;14(16):1515-21 PMID: 15324671
  7. Tornado1 and tornado2 are required for the specification of radial and circumferential pattern in the Arabidopsis root.
    Development. 2000 Aug;127(15):3385-94 PMID: 10887093
  8. The SPIRAL genes are required for directional control of cell elongation in Aarabidopsis thaliana.
    Development. 2000 Oct;127(20):4443-53 PMID: 11003843
  9. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants.
    Plant Cell. 1990 Jun;2(6):513-23 PMID: 2152173
  10. Extending the Microtubule/Microfibril paradigm. Cellulose synthesis is required for normal cortical microtubule alignment in elongating cells
    Plant Physiol. 1998 Mar;116(3):1043-51 PMID: 9501137
  11. Reversible root tip rotation in Arabidopsis seedlings induced by obstacle-touching stimulus.
    Science. 1990 Oct 12;250(4978):274-6 PMID: 17797309
  12. New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis.
    Plant Physiol. 2000 Dec;124(4):1493-506 PMID: 11115865
  13. The ROOT HAIR DEFECTIVE3 gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required for regulated cell enlargement in Arabidopsis.
    Genes Dev. 1997 Mar 15;11(6):799-811 PMID: 9087433
  14. Mutant alleles of Arabidopsis RADIALLY SWOLLEN 4 and 7 reduce growth anisotropy without altering the transverse orientation of cortical microtubules or cellulose microfibrils.
    Development. 2002 Oct;129(20):4821-30 PMID: 12361973
  15. Alkali treatment for rapid preparation of plant material for reliable PCR analysis.
    Plant J. 1993 Mar;3(3):493-4 PMID: 8220456
  16. Microtubule basis for left-handed helical growth in Arabidopsis.
    Nature. 2002 May 9;417(6885):193-6 PMID: 12000963
  17. A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus.
    Plant J. 2004 Feb;37(3):398-414 PMID: 14731265
  18. Progress in understanding the role of microtubules in plant cells.
    Curr Opin Plant Biol. 2004 Dec;7(6):651-60 PMID: 15491913
  19. The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process.
    Plant Physiol. 1994 Dec;106(4):1335-1346 PMID: 12232412
  20. The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein.
    Plant Cell. 2003 Feb;15(2):545-59 PMID: 12566591
  21. Molecular genetic analysis of left-right handedness in plants.
    Philos Trans R Soc Lond B Biol Sci. 2002 Jun 29;357(1422):799-808 PMID: 12079675
  22. Spiralizations and tropisms in Arabidopsis roots.
    Trends Plant Sci. 2001 Dec;6(12):561-5 PMID: 11738380
  23. Cell specification in the Arabidopsis root epidermis requires the activity of ECTOPIC ROOT HAIR 3--a katanin-p60 protein.
    Development. 2002 Jan;129(1):123-31 PMID: 11782406
  24. The Arabidopsis SKU5 gene encodes an extracellular glycosyl phosphatidylinositol-anchored glycoprotein involved in directional root growth.
    Plant Cell. 2002 Jul;14(7):1635-48 PMID: 12119380
  25. The Arabidopsis RHD3 gene is required for cell wall biosynthesis and actin organization.
    Planta. 2003 Oct;217(6):912-21 PMID: 12844267
  26. Building a root: the control of patterning and morphogenesis during root development.
    Plant Cell. 1997 Jul;9(7):1089-98 PMID: 9254932
  27. Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells.
    Plant Cell. 2003 Jun;15(6):1414-29 PMID: 12782733
  28. Morphology and microtubule organization in Arabidopsis roots exposed to oryzalin or taxol.
    Plant Cell Physiol. 1994 Sep;35(6):935-42 PMID: 7981964
  29. Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein.
    Nature. 2004 Apr 29;428(6986):945-50 PMID: 15118728
  30. Ethylene modulates root-wave responses in Arabidopsis.
    Plant Physiol. 2003 Jun;132(2):1085-96 PMID: 12805636
  31. Root-growth behavior of the Arabidopsis mutant rgr1. Roles of gravitropism and circumnutation in the waving/coiling phenomenon.
    Plant Physiol. 1998 Dec;118(4):1139-45 PMID: 9847088
  32. Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis.
    Plant Physiol. 2004 Dec;136(4):3933-44 PMID: 15557095
  33. Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells.
    Plant Cell Physiol. 2004 Sep;45(9):1330-4 PMID: 15509858
  34. WVD2 and WDL1 modulate helical organ growth and anisotropic cell expansion in Arabidopsis.
    Plant Physiol. 2003 Feb;131(2):493-506 PMID: 12586874
  35. Genetic Control of Root Hair Development in Arabidopsis thaliana.
    Plant Cell. 1990 Mar;2(3):235-243 PMID: 12354956
  36. A katanin-like protein regulates normal cell wall biosynthesis and cell elongation.
    Plant Cell. 2001 Apr;13(4):807-27 PMID: 11283338
  37. An improved PCR method for walking in uncloned genomic DNA.
    Nucleic Acids Res. 1995 Mar 25;23(6):1087-8 PMID: 7731798
  38. SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells.
    Plant Cell. 2004 May;16(5):1178-90 PMID: 15084720
  39. The reb1-1 mutation of Arabidopsis alters the morphology of trichoblasts, the expression of arabinogalactan-proteins and the organization of cortical microtubules.
    Planta. 2002 Oct;215(6):949-58 PMID: 12355155
  40. Arabidopsis thaliana sku mutant seedlings show exaggerated surface-dependent alteration in root growth vector.
    Plant Physiol. 1996 Aug;111(4):987-98 PMID: 8756492
  41. The Arabidopsis sku6/spiral1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion.
    Plant Cell. 2004 Jun;16(6):1506-20 PMID: 15155883
  42. Structural and genetic analysis of epidermal cell differentiation in Arabidopsis primary roots.
    Development. 1997 May;124(9):1789-98 PMID: 9165126
  43. Root-gel interactions and the root waving behavior of Arabidopsis.
    Plant Physiol. 2004 Jul;135(3):1822-37 PMID: 15247406
  44. COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis.
    Genes Dev. 2001 May 1;15(9):1115-27 PMID: 11331607
  45. The Arabidopsis WAVY GROWTH 2 protein modulates root bending in response to environmental stimuli.
    Plant Cell. 2005 Feb;17(2):537-47 PMID: 15659627
  46. Galactose biosynthesis in Arabidopsis: genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers.
    Curr Biol. 2002 Oct 29;12(21):1840-5 PMID: 12419184
  47. A novel root gravitropism mutant of Arabidopsis thaliana exhibiting altered auxin physiology.
    Physiol Plant. 1995;93:790-8 PMID: 11540162
  48. Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4766-71 PMID: 9539813
  49. The ARG1-LIKE2 gene of Arabidopsis functions in a gravity signal transduction pathway that is genetically distinct from the PGM pathway.
    Plant Physiol. 2003 Sep;133(1):100-12 PMID: 12970478
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2005-06-00
Epub
2005-00-20
Pages
701-14
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC1150390
Subset
IM
Grants
NIGMS NIH HHS · T32 GM007133 · United States
NIGMS NIH HHS · 1 R15 GM06849 · United States
NIGMS NIH HHS · 5 F32 GM069184-02 · United States
NIGMS NIH HHS · 5T32GM07133 · United States
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