Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development

Plant Journal

Volumn 35, Issue 1, 2003, Pages 71-81

  Baumberger, N ^a,c   Steiner, M ^a   Ryser, U ^b   Keller, B ^a   Ringli, C ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

^c SAINSBURY LABORATORY   (United Kingdom)

Author keywords

Cell morphogenesis; Cell wall; LRR extensins

Indexed keywords

GENES; PROTEINS; TRANSMISSION ELECTRON MICROSCOPY;

MUTANTS;

PLANTS (BOTANY);

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL WALL; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PLANT ROOTS; SEQUENCE HOMOLOGY;

ARABIDOPSIS; EMBRYOPHYTA; EUKARYOTA;

EID: 0037629264     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01784.x     Document Type: Article

References (46)

1. Arioli, T., Peng, L.C., Betzner, A.S. et al. (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science, 279, 717-720.
2. Baumberger, N., Ringli, C. and 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.
3. Baumberger, N., Doesseger, B., Guyot, R. et al. (2003) Whole-genome comparison of LRR-extensins (LRXs) in Arabidopsis thatiana and Oryza sativa: a conserved family of cell wall proteins form a vegetative and a reproductive clade. Plant Physiol. 131, 1313-1326.
4. Becker, D., Kemper, E., Schell, J. and Masterson, R. (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol. Biol. 20, 1195-1197.
5. Carpita, N.C. and Gibeaut, D.M. (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3, 1-30.
6. Carpita, N., Tierney, M. and Campbell, M. (2001) Molecular biology of the plant cell wall: searching for the genes that define structure, architecture and dynamics. Plant Mol. Biol. 47, 1-5.
7. Cassab, G.I. (1998) Plant cell wall proteins. Annu. Rev. Plant Physiol. 49, 281-309.
8. De Lorenzo, G. and Cervone, F. (1997) Polygalacturonase-inhibiting proteins (PGIPs): their role in specificity and defense against pathogenic fungi. In Plant-Microbe Interactions (Stacey, G. and Keen, N.T., eds). New York: Chapman & Hall, pp. 76-93.
9. Ding, L. and Zhu, J.K. (1997) A role for arabinogalactan-proteins in root epidermal cell expansion. Planta, 203, 289-294.
10. Dolan, L., Duckett, C., Grierson, C., Linstead, P., Schneider, K., Lawson, E., Dean, C., Poethig, S. and Roberts, K. (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development, 120, 2465-2474.
11. Edwards, M.E., Dickson, C.A., Chengappa, S., Sidebottom, C., Gidley, M.J. and Reid, J.S.G. (1999) Molecular characterisation of a membrane-bound galactosyltransferase of plant cell wall matrix polysaccharide biosynthesis. Plant J. 19, 691-697.
12. Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S. and Hofte, H. (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell, 12, 2409-2423.
13. Favery, B., Ryan, E., Foreman, J., Linstead, P., Boudonck, K., Steer, M., Shaw, P. and Dolan, L. (2001) KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev. 15, 79-89.
14. Galway, M.E., Lane, D.C. and Schiefelbein, J.W. (1999) Defective control of growth rate and cell diameter in tip-growing root hairs of the rhd4 mutant of Arabidopsis thaliana. Can. J. Bot. 77, 494-507.
15. Gilliland, LU., Kandasamy, M.K., Pawloski, L.C. and Meagher, R.B. (2002) Both vegetative and reproductive actin isovariants complement the stunted root hair phenotype of the Arabidopsis act2-1 mutant. Plant Physiol. 130, 2199-2209.
16. Gilroy, S. and Jones, D.L (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci., 5, 56-60.
17. Gleave, A.P. (1992) A vesatile binary vector system with a T-DNA organizational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203-1207.
18. Grierson, C.S., Roberts, K., Feldmann, K.A. and Dolan, L. (1997) The COW1 locus of Arabidopsis acts after RHD2, and in parallel with RHD3 and TIP1, to determine the shape, rate of elongation, and number of root hairs produced from each site of hair formation. Plant Physiol. 115, 981-990.
19. Hall, Q. and Cannon, M.C. (2002) The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell, 14, 1161-1172.
20. Jones, D.A. and Jones, J.D.G. (1997) The role of leucine-rich repeat proteins in plant defences. In Adv. Bot. Res. Inc. Adv. in Plant Pathol., Vol. 24, pp. 89-167.
21. Kobe, B. and Deisenhofer, J. (1995) A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature, 374, 183-186.
22. Leckie, F., Mattei, B., Capodicasa, C., Hemmings, A., Nuss, L., Aracri, B., De Lorenzo, G. and Cervone, F. (1999) The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent exposed b-strand/b-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J. 18, 2352-2363.
23. Lynch, M. and Conery, J.S. (2000) The evolutionary fate and consequences of duplicate genes. Science, 290, 1151-1155.
24. Masucci, J.D. and Schiefelbein, J.W. (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin-associated and ethylene-associated process. Plant Physiol. 106, 1335-1346.
25. Meagher, R.B., McKinney, E.C. and Kandasamy, M.K. (1999) Isovariant dynamics expand and buffer the responses of complex systems: the diverse plant actin gene family. Plant Cell, 11, 995-1005.
26. Ohno, S. (1973) Evolution by Gene Duplication. New York: Springer Verlag.
27. Papageorgiou, A.C., Shapiro, R. and Acharya, K.R. (1997) Molecular recognition of human angiogenin by placental ribonuclease inhibitor: an X-ray crystallographic study at 2.0-angstrom resolution. EMBO J. 16, 5162-5177.
28. Perrin, R.M., DeRocher, A.E., Bar-Peled, M., Zeng, W.Q., Norambuena, L., Orellana, A., Raikhel, N.V. and Keegstra, K. (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science, 284, 1976-1979.
29. Pritchard, J. (1994) The control of cell expansion in roots. New Phytol. 127, 3-26.
30. Rigas, S., Debrosses, G., Haralampidis, K., Vicente-Agullo, F., Feldmann, K.A., Grabov, A., Dolan, L. and Hatzopoulos, P. (2001) TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell, 13, 139-151.
31. Ringli, C., Baumberger, N., Diet, A., Frey, B. and Keller, B. (2002) ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol. 129, 1464-1472.
32. Rubinstein, A.L., Marquez, J., Suarez Cervera, M. and Bedinger, P.A. (1995b) Extensin-like glycoproteins in the maize pollen tube wall. Plant Cell, 7, 2211-2225.
33. Ryan, E., Grierson, C.S., Cavell, A., Steer, M. and Dolan, L. (1998) TIP1 is required for both tip growth and non-tip growth in Arabidopsis. New Phytol. 138, 49-58.
34. Sassen, M.M.A., Traas, J.A. and Wolter-Arts, A.M.C. (1985) De position of cellulose microfibrils in cell walls of root hairs. Eur. J. Cell Biol. 37, 21-26.
35. Schiefelbein, J.W. (2000) Constructing a plant cell. The genetic control of root hair development. Plant Physiol. 124, 1525-1531.
36. Schiefelbein, J.W. and Somerville, C. (1990) Genetic control of root hair development in Arabidopsis thaliana. Plant Cell, 2, 235-243.
37. Schiefelbein, J., Galway, M., Masucci, J. and Ford, S. (1993) Pollen tube and root hair tip growth is disrupted in a mutant of Arabidopsis thaliana. Plant Physiol. 103, 979-985.
38. Schindelman, G., Morikami, A., Jung, J., Baskin, T.I., Carpita, N.C., Derbyshire, P., McCann, M.C. and Benfey, P.N. (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev. 15, 1115-1127.
39. Showalter, A.M. (1993) Structure and function of plant cell wall proteins. Plant Cell, 5, 9-23.
40. Vision, T.J., Brown, D.G. and Tanksley, S.D. (2000) The origins of genomic duplications in Arabidopsis. Science, 90, 2114-2117.
41. Wang, H.Y., Lockwood, S.K., Hoeltzel, M.F. and Schiefelbein, J.W. (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.
42. Wang, X., Cnops, G., Vanderhaeghen, R., De Block, S., Van Montagu, M. and Van Lijsebettens, M. (2001) AtCSLD3, a cellulose synthase-like gene important for root hair growth in Arabidopsis. Plant Physiol. 126, 575-586.
43. Wild, P., Schraner, E.M., Adler, H. and Humbel, B.M. (2001) Enhanced resolution of membranes in cultured cells by cryoimmobilization and freeze-substitution. Microsc. Res. Tech. 53, 313-321.
44. Wisman, E., Cardon, G.H., Fransz, P. and Saedler, H. (1998) The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Mol. Biol. 37, 989-999.
45. Wymer, C.L., Bibikova, T.N. and Gilroy, S. (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J. 12, 427-439.
46. Yang, Z.B. (1998) Signaling tip growth in plants. Curr. Opin. Plant Biol. 1, 525.