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The Arabidopsis RHD3 gene is required for cell wall biosynthesis and actin organization

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Abstract

The Arabidopsis thaliana (L.) Heynh. ROOT HAIR DEFECTIVE3 (RHD3) gene has previously been shown to be essential for normal cell expansion [H. Wang et al. (1997) Genes Dev 11:799–811]. In this report, we demonstrated that mutation of the RHD3 gene in the Arabidopsis fragile fiber 4 (fra4) mutant caused a dramatic reduction in the wall thickness of fibers, vessels, and pith cells in the inflorescence stems and, concomitantly, a decrease in the mechanical strength of stems. The reduced wall thickness in the fra4 mutant was accompanied by an alteration in cell wall composition. Consistent with the defective fiber and vessel wall phenotypes, the RHD3 gene exhibited a strong expression in developing fiber and xylem cells. We showed that the Arabidopsis genome contains two additional RHD3-like genes, one of which was expressed specifically in flowers. In addition, we found that mutation of the RHD3 gene caused an alteration in the organization of the actin cytoskeleton but no effects on cortical microtubules. Our findings suggest an essential role of RHD3 in cell wall biosynthesis and actin organization, both of which are known to be important for cell expansion.

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Fig. 1a–f.
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Fig. 3a–f.
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Abbreviations

GUS:

β-glucuronidase

MS:

Murashige and Skoog (medium)

RT–PCR:

reverse transcription–polymerase chain reaction

References

  • Baluska F, Busti E, Dolfini S, Gavazzi G, Volkmann D (2001a) Lilliputian mutant of maize lacks cell elongation and shows defects in organization of actin cytoskeleton. Dev Biol 236:478–491

    Article  CAS  PubMed  Google Scholar 

  • Baluska F, Jasik J, Edelmann HG, Salajova T, Volkmann D (2001b) Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin-dependent. Dev Biol 231:113–124

    Article  CAS  PubMed  Google Scholar 

  • Baumberger N, Ringli C, Keller B (2001) The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev 15:1128–1139

    Article  CAS  PubMed  Google Scholar 

  • Bechtold N, Bouchez D (1994) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. In: Potrykus I, Spangenberg G (eds) Gene transfer to plants. Springer, Berlin Heidelberg New York, pp 19–23

  • Blancaflor EB (2002) The cytoskeleton and gravitropism in higher plants. J Plant Growth Regul 21:120–136

    Article  CAS  PubMed  Google Scholar 

  • Burk DH, Ye Z-H (2002) Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule severing protein. Plant Cell 14:2145–2160

    Article  CAS  PubMed  Google Scholar 

  • Burk DH, Liu B, Zhong R, Morrison WH, Ye Z-H (2001) A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13:807–827

    Google Scholar 

  • Dever TE, Glynias MJ, Merrick WC (1987) GTP-binding domain: Three consensus sequence elements with distinct spacing. Proc Natl Acad Sci USA 84:1814–1818

    CAS  PubMed  Google Scholar 

  • Dong C-H, Xia GX, Hong Y, Ramachandran S, Kost B, Chua N-H (2001) ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13:1333–1346

    Google Scholar 

  • Favery B, Ryan E, Foreman J, Linstead P, Boudonck K, Steer M, Shaw P, Dolan L (2001) KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev 15:79–89

    PubMed  Google Scholar 

  • Galway ME, Heckman JW, Schiefelbein JW (1997) Growth and ultrastructure of Arabidopsis root hairs: the rhd3 mutation alters vacuole enlargement and tip growth. Planta 201:209–218

    CAS  PubMed  Google Scholar 

  • Hoebler C, Barry JL, David A, Delort-Laval J (1989) Rapid acid-hydrolysis of plant cell wall polysaccharides and simplified quantitative determination of their neutral monosaccharides by gas-liquid chromatography. J Agric Food Chem 37:360–367

    CAS  Google Scholar 

  • Martin C, Bhatt K, Baumann K (2001) Shaping in plant cells. Curr Opin Plant Biol 4:540–549

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Ringli C, Baumberger N, Diet A, Frey B, Keller B (2002) ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol 129:1464–1472

    Article  CAS  PubMed  Google Scholar 

  • Schiefelbein JW, Somerville C (1990) Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2:235–243

    CAS  Google Scholar 

  • Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51:257–288

    Google Scholar 

  • Sugimoto K, Williamson RE, Wasteneys GO (2000) New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol 124:1493–1506

    Article  CAS  PubMed  Google Scholar 

  • Taylor NG, Scheible W-R, Cutler S, Somerville CR, Turner SR (1999) The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11:769–779

    CAS  PubMed  Google Scholar 

  • Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2539

    CAS  PubMed  Google Scholar 

  • Turner SR, Hall M (2000) The gapped xylem mutant identifies a common regulatory step in secondary cell wall deposition. Plant J 24:477–488

    Article  CAS  PubMed  Google Scholar 

  • Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701

    CAS  PubMed  Google Scholar 

  • Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424

    CAS  PubMed  Google Scholar 

  • Vitha S, Baluska,F, Braun M, Samaj J, Volkmann D, Barlow PW (2000) Comparison of cryofixation and aldehyde fixation for plant actin immunocytochemistry: aldehydes do not destroy F-actin. Histochem J 32:457–466

    Article  CAS  PubMed  Google Scholar 

  • Waller F, Nick P (1997) Response of actin microfilaments during phytochrome-controlled growth of maize seedlings. Protoplasma 200:154–162

    CAS  Google Scholar 

  • Waller F, Riemann M, Nick P (2002) A role for actin-driven secretion in auxin-induced growth. Protoplasma 219:72–81

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Lockwood SK, Hoeltzel MF, Schiefelbein JW (1997) 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 11:799–811

    CAS  PubMed  Google Scholar 

  • Wang H, Lee MM, Schiefelbein JW (2002) Regulation of the cell expansion gene RHD3 during Arabidopsis development. Plant Physiol 129:638–649

    Article  CAS  PubMed  Google Scholar 

  • Wang QY, Nick P (1998) The auxin response of actin is altered in the rice mutant Yin-Yang. Protoplasma 204:22–33

    CAS  PubMed  Google Scholar 

  • Wang X, Cnops G, Vanderhaeghen R, Block SD, Van Montagu M, Van Lijsebettens M (2001) AtCELD3, a cellulose synthase-like gene important for root hair growth in Arabidopsis. Plant Physiol 126:575–586

    CAS  PubMed  Google Scholar 

  • Wasteneys GO (2000) The cytoskeleton and growth polarity. Curr Opin Plant Biol 3:503–511

    Article  CAS  PubMed  Google Scholar 

  • Wasteneys GO, Galway ME (2003) Remodeling the cytoskeleton for growth and form: an overview with some new views. Annu Rev Plant Biol 54:691–722

    Article  Google Scholar 

  • Ye Z-H, Freshour G, Hahn MG, Burk DH, Zhong R (2002) Vascular development in Arabidopsis. Int Rev Cytol 220:225–256

    CAS  PubMed  Google Scholar 

  • Zhong R, Ye Z-H (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11:2139–2152

    CAS  PubMed  Google Scholar 

  • Zhong R, Taylor JJ, Ye Z-H (1997) Disruption of interfascicular fiber differentiation in an Arabidopsis mutant. Plant Cell 9:2159–2170

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Burk DH, Ye Z-H (2001) Fibers. A model for studying cell differentiation, cell elongation, and cell wall biosynthesis. Plant Physiol 126:477–479

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Burk DH, Morrison WHIII, Ye Z-H (2002) A Kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14:3101–3117

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Morrison WHIII, Freshour G, Hahn M, Ye Z-H (2003) Expression of a mutant form of cellulose synthase AtCesA7 causes dominant negative effect on cellulose biosynthesis. Plant Physiol 132:786–795

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Beth Richardson for her help with transmission electron microscopy, and the editor and reviewers for their constructive comments and suggestions. This work was supported by a grant from the US Department of Agriculture.

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Authors and Affiliations

  1. Department of Plant Biology, University of Georgia, Athens, GA 30602, USA

    Yun Hu, Ruiqin Zhong & Zheng-Hua Ye

  2. Richard B. Russell Agriculture Research Center, Agriculture Research Service, U.S. Department of Agriculture, Athens, GA 30604, USA

    W. Herbert Morrison III

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  1. Yun Hu
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  2. Ruiqin Zhong
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  3. W. Herbert Morrison III
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  4. Zheng-Hua Ye
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Correspondence to Zheng-Hua Ye.

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Hu, Y., Zhong, R., Morrison III, W.H. et al. The Arabidopsis RHD3 gene is required for cell wall biosynthesis and actin organization. Planta 217, 912–921 (2003). https://doi.org/10.1007/s00425-003-1067-7

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  • DOI: https://doi.org/10.1007/s00425-003-1067-7

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