PLANT PHYSIOLOGY , Vol 106, Issue 4 1335-1346, Copyright © 1994 by American Society of Plant Biologists

DEVELOPMENT AND GROWTH REGULATION

The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process

J. D. Masucci and J. W. Schiefelbein
Department of Biology, University of Michigan, Ann Arbor, Michigan 48109

Root-hair initiation in Arabidopsis thaliana provides a model for studying cell polarity and its role in plant morphogenesis. Root hairs normally emerge at the apical end of root epidermal cells, implying that these cells are polarized. We have identified a mutant, rhd6, that displays three defects: (a) a reduction in the number of root hairs, (b) an overall basal shift in the site of root-hair emergence, and (c) a relatively high frequency of epidermal cells with multiple root hairs. These defects implicate the RHD6 gene in root-hair initiation and indicate that RHD6 is normally associated with the establishment of, or response to, root epidermal cell polarity. Similar alterations in the site of root-hair emergence, although less extreme, were also discovered in roots of the auxin-, ethylene-, abscisic acid-resistant mutant axr2 and the ethylene-resistant mutant etr1. All three rhd6 mutant phenotypes were rescued when either auxin (indoleacetic acid) or an ethylene precursor (1-aminocyclopropane-1-carboxylic acid) was included in the growth medium. The rhd6 root phenotypes could be phenocopied by treating wild-type seedlings with an inhibitor of the ethylene pathway (aminoethoxyvinylglycine). These results indicate that RHD6 is normally involved in directing the selection or assembly of the root-hair initiation site through a process involving auxin and ethylene.

This article has been cited by other articles:

				S.-K. Won, Y.-J. Lee, H.-Y. Lee, Y.-K. Heo, M. Cho, and H.-T. Cho cis-Element- and Transcriptome-Based Screening of Root Hair-Specific Genes and Their Functional Characterization in Arabidopsis Plant Physiology, July 1, 2009; 150(3): 1459 - 1473. [Abstract] [Full Text] [PDF]

				J. Schiefelbein, S.-H. Kwak, Y. Wieckowski, C. Barron, and A. Bruex The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis J. Exp. Bot., April 1, 2009; 60(5): 1515 - 1521. [Abstract] [Full Text] [PDF]

				H. A. Contreras-Cornejo, L. Macias-Rodriguez, C. Cortes-Penagos, and J. Lopez-Bucio Trichoderma virens, a Plant Beneficial Fungus, Enhances Biomass Production and Promotes Lateral Root Growth through an Auxin-Dependent Mechanism in Arabidopsis Plant Physiology, March 1, 2009; 149(3): 1579 - 1592. [Abstract] [Full Text] [PDF]

				L. Brechenmacher, J. Lee, S. Sachdev, Z. Song, T. H. N. Nguyen, T. Joshi, N. Oehrle, M. Libault, B. Mooney, D. Xu, et al. Establishment of a Protein Reference Map for Soybean Root Hair Cells Plant Physiology, February 1, 2009; 149(2): 670 - 682. [Abstract] [Full Text] [PDF]

				A. Leblanc, H. Renault, J. Lecourt, P. Etienne, C. Deleu, and E. Le Deunff Elongation Changes of Exploratory and Root Hair Systems Induced by Aminocyclopropane Carboxylic Acid and Aminoethoxyvinylglycine Affect Nitrate Uptake and BnNrt2.1 and BnNrt1.1 Transporter Gene Expression in Oilseed Rape Plant Physiology, April 1, 2008; 146(4): 1928 - 1940. [Abstract] [Full Text] [PDF]

				R.-C. Lin, H.-J. Park, and H.-Y. Wang Role of Arabidopsis RAP2.4 in Regulating Light- and Ethylene-Mediated Developmental Processes and Drought Stress Tolerance Mol Plant, January 1, 2008; 1(1): 42 - 57. [Abstract] [Full Text] [PDF]

				J. P. Hammond and P. J. White Sucrose transport in the phloem: integrating root responses to phosphorus starvation J. Exp. Bot., January 1, 2008; 59(1): 93 - 109. [Abstract] [Full Text] [PDF]

				S. Guimil and C. Dunand Cell growth and differentiation in Arabidopsis epidermal cells J. Exp. Bot., November 1, 2007; 58(14): 3829 - 3840. [Abstract] [Full Text] [PDF]

				B. Menand, K. Yi, S. Jouannic, L. Hoffmann, E. Ryan, P. Linstead, D. G. Schaefer, and L. Dolan An Ancient Mechanism Controls the Development of Cells with a Rooting Function in Land Plants Science, June 8, 2007; 316(5830): 1477 - 1480. [Abstract] [Full Text] [PDF]

				B. N. Devaiah, A. S. Karthikeyan, and K. G. Raghothama WRKY75 Transcription Factor Is a Modulator of Phosphate Acquisition and Root Development in Arabidopsis Plant Physiology, April 1, 2007; 143(4): 1789 - 1801. [Abstract] [Full Text] [PDF]

				X. Li, X. Mo, H. Shou, and P. Wu Cytokinin-Mediated Cell Cycling Arrest of Pericycle Founder Cells in Lateral Root Initiation of Arabidopsis Plant Cell Physiol., August 1, 2006; 47(8): 1112 - 1123. [Abstract] [Full Text] [PDF]

				S. H. Lee and H.-T. Cho PINOID Positively Regulates Auxin Efflux in Arabidopsis Root Hair Cells and Tobacco Cells PLANT CELL, July 1, 2006; 18(7): 1604 - 1616. [Abstract] [Full Text] [PDF]

				M. Kwasniewski and I. Szarejko Molecular Cloning and Characterization of beta-Expansin Gene Related to Root Hair Formation in Barley Plant Physiology, July 1, 2006; 141(3): 1149 - 1158. [Abstract] [Full Text] [PDF]

				C. Zhu, L. Gan, Z. Shen, and K. Xia Interactions between jasmonates and ethylene in the regulation of root hair development in Arabidopsis J. Exp. Bot., March 1, 2006; 57(6): 1299 - 1308. [Abstract] [Full Text] [PDF]

				C.-W. Chen, Y.-W. Yang, H.-S. Lur, Y.-G. Tsai, and M.-C. Chang A Novel Function of Abscisic Acid in the Regulation of Rice (Oryza sativa L.) Root Growth and Development Plant Cell Physiol., January 1, 2006; 47(1): 1 - 13. [Abstract] [Full Text] [PDF]

				R. Shin, R. H. Berg, and D. P. Schachtman Reactive Oxygen Species and Root Hairs in Arabidopsis Root Response to Nitrogen, Phosphorus and Potassium Deficiency Plant Cell Physiol., August 1, 2005; 46(8): 1350 - 1357. [Abstract] [Full Text] [PDF]

				C. Ringli, N. Baumberger, and B. Keller The Arabidopsis Root Hair Mutants der2-der9 are Affected at Different Stages of Root Hair Development Plant Cell Physiol., July 1, 2005; 46(7): 1046 - 1053. [Abstract] [Full Text] [PDF]

				C. Y.L. Yuen, J. C. Sedbrook, R. M. Perrin, K. L. Carroll, and P. H. Masson Loss-of-Function Mutations of ROOT HAIR DEFECTIVE3 Suppress Root Waving, Skewing, and Epidermal Cell File Rotation in Arabidopsis Plant Physiology, June 1, 2005; 138(2): 701 - 714. [Abstract] [Full Text] [PDF]

				R. S. Tegg, L. Melian, C. R. Wilson, and S. Shabala Plant Cell Growth and Ion Flux Responses to the Streptomycete Phytotoxin Thaxtomin A: Calcium and Hydrogen Flux Patterns Revealed by the Non-invasive MIFE Technique Plant Cell Physiol., April 1, 2005; 46(4): 638 - 648. [Abstract] [Full Text] [PDF]

				J. Xu and B. Scheres Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 Function in Epidermal Cell Polarity PLANT CELL, February 1, 2005; 17(2): 525 - 536. [Abstract] [Full Text] [PDF]

				C. Bernhardt, M. Zhao, A. Gonzalez, A. Lloyd, and J. Schiefelbein The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis Development, January 15, 2005; 132(2): 291 - 298. [Abstract] [Full Text] [PDF]

				T. Nagata, S. Todoriki, and S. Kikuchi Radial Expansion of Root Cells and Elongation of Root Hairs of Arabidopsis thaliana Induced by Massive Doses of Gamma Irradiation Plant Cell Physiol., November 15, 2004; 45(11): 1557 - 1565. [Abstract] [Full Text] [PDF]

				T. E. Sondergaard, A. Schulz, and M. G. Palmgren Energization of Transport Processes in Plants. Roles of the Plasma Membrane H+-ATPase Plant Physiology, September 1, 2004; 136(1): 2475 - 2482. [Full Text] [PDF]

				A. Diet, S. Brunner, and C. Ringli The enl Mutants Enhance the lrx1 Root Hair Mutant Phenotype of Arabidopsis thaliana Plant Cell Physiol., June 15, 2004; 45(6): 734 - 741. [Abstract] [Full Text] [PDF]

				S. J. Ahn, R. Shin, and D. P. Schachtman Expression of KT/KUP Genes in Arabidopsis and the Role of Root Hairs in K+ Uptake Plant Physiology, March 1, 2004; 134(3): 1135 - 1145. [Abstract] [Full Text] [PDF]

				M. Muller and W. Schmidt Environmentally Induced Plasticity of Root Hair Development in Arabidopsis Plant Physiology, January 1, 2004; 134(1): 409 - 419. [Abstract] [Full Text] [PDF]

				Y.-J. Zhang, J. P. Lynch, and K. M. Brown Ethylene and phosphorus availability have interacting yet distinct effects on root hair development J. Exp. Bot., October 1, 2003; 54(391): 2351 - 2361. [Abstract] [Full Text] [PDF]

				H. Takahashi, A. Kawahara, and Y. Inoue Ethylene Promotes the Induction by Auxin of the Cortical Microtubule Randomization Required for Low-pH-Induced Root Hair Initiation in Lettuce (Lactuca sativa L.) Seedlings Plant Cell Physiol., September 15, 2003; 44(9): 932 - 940. [Abstract] [Full Text] [PDF]

				C. S. Buer, G. O. Wasteneys, and J. Masle Ethylene Modulates Root-Wave Responses in Arabidopsis Plant Physiology, June 1, 2003; 132(2): 1085 - 1096. [Abstract] [Full Text] [PDF]

				H. Takahashi, K. Hirota, A. Kawahara, E. Hayakawa, and Y. Inoue Randomization of Cortical Microtubules in Root Epidermal Cells Induces Root Hair Initiation in Lettuce (Lactuca sativa L.) Seedlings Plant Cell Physiol., March 15, 2003; 44(3): 350 - 359. [Abstract] [Full Text] [PDF]

				V. Willemsen, J. Friml, M. Grebe, A. van den Toorn, K. Palme, and B. Scheres Cell Polarity and PIN Protein Positioning in Arabidopsis Require STEROL METHYLTRANSFERASE1 Function PLANT CELL, March 1, 2003; 15(3): 612 - 625. [Abstract] [Full Text] [PDF]

				Z. Ma, T. I. Baskin, K. M. Brown, and J. P. Lynch Regulation of Root Elongation under Phosphorus Stress Involves Changes in Ethylene Responsiveness Plant Physiology, March 1, 2003; 131(3): 1381 - 1390. [Abstract] [Full Text] [PDF]

				H. Takahashi, T. Iwasa, T. Shinkawa, A. Kawahara, T. Kurusu, and Y. Inoue Isolation and Characterization of the ACC Synthase Genes from Lettuce (Lactuca sativa L.), and the Involvement in Low pH-Induced Root Hair Initiation Plant Cell Physiol., January 15, 2003; 44(1): 62 - 69. [Abstract] [Full Text] [PDF]

				H.-T. Cho and D. J. Cosgrove Regulation of Root Hair Initiation and Expansin Gene Expression in Arabidopsis PLANT CELL, December 1, 2002; 14(12): 3237 - 3253. [Abstract] [Full Text] [PDF]

				A. Rahman, S. Hosokawa, Y. Oono, T. Amakawa, N. Goto, and S. Tsurumi Auxin and Ethylene Response Interactions during Arabidopsis Root Hair Development Dissected by Auxin Influx Modulators Plant Physiology, December 1, 2002; 130(4): 1908 - 1917. [Abstract] [Full Text] [PDF]

				C. Ringli, N. Baumberger, A. Diet, B. Frey, and B. Keller ACTIN2 Is Essential for Bulge Site Selection and Tip Growth during Root Hair Development of Arabidopsis Plant Physiology, August 1, 2002; 129(4): 1464 - 1472. [Abstract] [Full Text] [PDF]

				H. Shi and J.-K. Zhu SOS4, A Pyridoxal Kinase Gene, Is Required for Root Hair Development in Arabidopsis Plant Physiology, June 1, 2002; 129(2): 585 - 593. [Abstract] [Full Text] [PDF]

				H. Wang, M. M. Lee, and J. W. Schiefelbein Regulation of the Cell Expansion Gene RHD3 during Arabidopsis Development Plant Physiology, June 1, 2002; 129(2): 638 - 649. [Abstract] [Full Text] [PDF]

				M. Bucher, S. Brunner, P. Zimmermann, G. I. Zardi, N. Amrhein, L. Willmitzer, and J. W. Riesmeier The Expression of an Extensin-Like Protein Correlates with Cellular Tip Growth in Tomato Plant Physiology, March 1, 2002; 128(3): 911 - 923. [Full Text] [PDF]

				T. Wada, T. Kurata, R. Tominaga, Y. Koshino-Kimura, T. Tachibana, K. Goto, M. D. Marks, Y. Shimura, and K. Okada Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation Development, January 12, 2002; 129(23): 5409 - 5419. [Abstract] [Full Text] [PDF]

				M. Webb, S. Jouannic, J. Foreman, P. Linstead, and L. Dolan Cell specification in the Arabidopsis root epidermis requires the activity of ECTOPIC ROOT HAIR 3 - a katanin-p60 protein Development, January 1, 2002; 129(1): 123 - 131. [Abstract] [Full Text] [PDF]

				K. Vissenberg, S. C. Fry, and J.-P. Verbelen Root Hair Initiation Is Coupled to a Highly Localized Increase of Xyloglucan Endotransglycosylase Action in Arabidopsis Roots Plant Physiology, November 1, 2001; 127(3): 1125 - 1135. [Abstract] [Full Text] [PDF]

				M. Wissuwa and N. Ae Genotypic differences in the presence of hairs on roots and gynophores of peanuts ( Arachis hypogaea L.) and their significance for phosphorus uptake J. Exp. Bot., August 1, 2001; 52(361): 1703 - 1710. [Abstract] [Full Text] [PDF]

				N. Baumberger, C. Ringli, and B. Keller The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana Genes & Dev., May 1, 2001; 15(9): 1128 - 1139. [Abstract] [Full Text]

				B. Favery, E. Ryan, J. Foreman, P. Linstead, K. Boudonck, M. Steer, P. Shaw, and L. Dolan KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis Genes & Dev., January 1, 2001; 15(1): 79 - 89. [Abstract] [Full Text]

				S. Rigas, G. Debrosses, K. Haralampidis, F. Vicente-Agullo, K. A. Feldmann, A. Grabov, L. Dolan, and P. Hatzopoulos TRH1 Encodes a Potassium Transporter Required for Tip Growth in Arabidopsis Root Hairs PLANT CELL, January 1, 2001; 13(1): 139 - 151. [Abstract] [Full Text]

				J. W. Schiefelbein Constructing a Plant Cell. The Genetic Control of Root Hair Development Plant Physiology, December 1, 2000; 124(4): 1525 - 1531. [Full Text]

				J. S. Parker, A. C. Cavell, L. Dolan, K. Roberts, and C. S. Grierson Genetic Interactions during Root Hair Morphogenesis in Arabidopsis PLANT CELL, October 1, 2000; 12(10): 1961 - 1974. [Abstract] [Full Text]

				T. R. Bates and J. P. Lynch Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae) Am. J. Botany, July 1, 2000; 87(7): 958 - 963. [Abstract] [Full Text]

				T. R. Bates and J. P. Lynch The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition Am. J. Botany, July 1, 2000; 87(7): 964 - 970. [Abstract] [Full Text]

				W. Schmidt, J. Tittel, and A. Schikora Role of Hormones in the Induction of Iron Deficiency Responses in Arabidopsis Roots Plant Physiology, April 1, 2000; 122(4): 1109 - 1118. [Abstract] [Full Text]

				C. Bernhardt and M. L. Tierney Expression of AtPRP3, a Proline-Rich Structural Cell Wall Protein from Arabidopsis, Is Regulated by Cell-Type-Specific Developmental Pathways Involved in Root Hair Formation Plant Physiology, March 1, 2000; 122(3): 705 - 714. [Abstract] [Full Text] [PDF]

				G Cnops, X Wang, P Linstead, M Van Montagu, M Van Lijsebettens, and L Dolan Tornado1 and tornado2 are required for the specification of radial and circumferential pattern in the Arabidopsis root Development, January 8, 2000; 127(15): 3385 - 3394. [Abstract] [PDF]

				J. S. Schmidt, J. E. Harper, T. K. Hoffman, and A. F. Bent Regulation of Soybean Nodulation Independent of Ethylene Signaling Plant Physiology, March 1, 1999; 119(3): 951 - 960. [Abstract] [Full Text]

				C.-Y. Hung, Y. Lin, M. Zhang, S. Pollock, M. David Marks, and J. Schiefelbein A Common Position-Dependent Mechanism Controls Cell-Type Patterning and GLABRA2 Regulation in the Root and Hypocotyl Epidermis of Arabidopsis Plant Physiology, May 1, 1998; 117(1): 73 - 84. [Abstract] [Full Text]

				R. Sanchez-Fernandez, M. Fricker, L. B. Corben, N. S. White, N. Sheard, C. J. Leaver, M. Van Montagu, D. Inze, and M. J. May Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control PNAS, March 18, 1997; 94(6): 2745 - 2750. [Abstract] [Full Text] [PDF]

				H Wang, S K Lockwood, M F Hoeltzel, and J W Schiefelbein 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., March 15, 1997; 11(6): 799 - 811. [Abstract] [PDF]

				K Schneider, B Wells, L Dolan, and K Roberts Structural and genetic analysis of epidermal cell differentiation in Arabidopsis primary roots Development, January 5, 1997; 124(9): 1789 - 1798. [Abstract] [PDF]

				A Cernac, C Lincoln, D Lammer, and M Estelle The SAR1 gene of Arabidopsis acts downstream of the AXR1 gene in auxin response Development, January 4, 1997; 124(8): 1583 - 1591. [Abstract] [PDF]

				J. Masucci, W. Rerie, D. Foreman, M Zhang, M. Galway, M. Marks, and J. Schiefelbein The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana Development, January 4, 1996; 122(4): 1253 - 1260. [Abstract] [PDF]

				Ecker JR The ethylene signal transduction pathway in plants Science, May 5, 1995; 268(5211): 667 - 675. [Abstract] [PDF]

				M. A. Jones, J.-J. Shen, Y. Fu, H. Li, Z. Yang, and C. S. Grierson The Arabidopsis Rop2 GTPase Is a Positive Regulator of Both Root Hair Initiation and Tip Growth PLANT CELL, April 1, 2002; 14(4): 763 - 776. [Abstract] [Full Text] [PDF]