Skip to main content
SpringerLink
Log in

The elongation defective1 mutant of Arabidopsis is impaired in the gene encoding a serine-rich secreted protein

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Coordinated cell growth and differentiation is crucial for the development of higher plants. Using the elongation defective 1-1 (eld1-1) mutant, we cloned the ELD1 gene, which encodes a serine-rich protein. Genes homologous to ELD1 can be found in plants, includingArabidopsis, rice, and tobacco, but not in other organisms. Using reverse genetics, we identified a new allele, eld1-2, which is phenotypically indistinguishable from eld1-1, but does not produce a detectable ELD1 transcript. The ELD1 gene sequence is the same as that of the KOBITO1 sequence. However, the kob1 mutants display weak phenotype relative to the two eld1 mutants, which are likely null alleles. KOB1 was reported to be a membrane protein involved in cellulose synthesis. However, based on ELD1-GFP localization in plasmolyzed cells, we found that ELD1 is localized to the cell wall/extracellular matrix, rather than the membrane. Thus, ELD1/KOB1 is a secreted protein involved in promoting cell growth. To investigate the relationship between ELD1 and Arabidopsis genes with high sequence similarity, we analyzed the possible subcellular location of their proteins as well as their amino acid sequence. The ELD1-related proteins in Arabidopsis were predicted to be localized to subcellular compartments different from that of ELD1. Thus, ELD1 is likely to be functionally distinct from related Arabidopsis genes. These results suggest that ELD1 is a single-copy gene which belongs to a small family of plant-specific genes with diverse function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Aubert, D., Chen, L., Moon, Y.-H., Martin, D., Castle, L.A., Yang, C.-H. and Sung, Z.R. 2001. EMF1, a novel protein involved in the control of shoot architecture and flowering in Arabidopsis. Plant Cell 13: 1865–1875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azpiroz, R., Wu, Y., LoCascio, J.C. and Feldmann, K.A. 1998. An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10: 219–230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell, C.J. and Ecker, J.R. 1994. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19: 137–144.

    Article  CAS  PubMed  Google Scholar 

  • Cassab, G.I. 1998. Plant cell wall proteins. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 49: 281–309.

    Article  CAS  PubMed  Google Scholar 

  • Chang, S., Puryear, J. and Cairney, J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11: 113–116.

    Article  CAS  Google Scholar 

  • Chen, H., Nelson, R.S. and Sherwood, J.L. 1994. Enhanced recovery of transformants of Agrobacterium tumefaciens after freeze-thaw transformation and drug selection. Biotechniques 16: 664–668, 670.

    CAS  PubMed  Google Scholar 

  • Cheng, J.C., Lertpiriyapong, K., Wang, S. and Sung, Z.R. 2000. The role of the Arabidopsis ELD1 gene in cell development and photomorphogenesis. Plant Physiol. 123: 509–520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough, S.J. and Bent, A.F. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743.

    Article  CAS  PubMed  Google Scholar 

  • Clouse, S.D., Langford, M. and McMorris, T.C. 1996. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 111: 671–678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corpet, F., Servant, F., Gouzy, J. and Kahn, D. 2000. ProDom and ProDom-CG: tools for protein domain analysis and whole genome comparisons. Nucl. Acids Res. 28: 267–269.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove, D.J. 1997. Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell 9: 1031–1041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove, D.J. 2000. Expansive growth of plant cell walls. Plant Physiol. Biochem. 38: 109–124.

    Article  CAS  PubMed  Google Scholar 

  • Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S. and Höfte, H. 2000. PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12: 2409–2424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujioka, S., Li, J., Choi, Y.-H., Seto, H., Takatsuto, S., Noguchi, T., Watanabe, T., Kuriyama, H., Yokota, T., Chory, J. and Sakurai, A. 1997. The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9: 1951–1962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hajdukiewicz, P., Svab, Z. and Maliga, P. 1994. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989–994.

    Article  CAS  PubMed  Google Scholar 

  • Klahre, U. 1998. The Arabidopsis DIMINUTO/DWARF1 gene encodes a protein involved in steroid synthesis. Plant Cell 10: 1677–1690.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohchi, T., Mukougawa, K., Frankenberg, N., Masuda, M., Yokota, A. and Lagarias, J.C. 2001. The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell 13: 425–436.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohorn, B.D. 2000. Plasma membrane-cell wall contacts. Plant Physiol. 124: 31–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohorn, B.D. 2001.WAKS, cell wall associated kinases: Commentary. Curr. Opin. Cell Biol. 13: 529–533.

    Article  CAS  PubMed  Google Scholar 

  • Konieczny, A. and Ausubel, F.M. 1993. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCRbased markers. Plant J. 4: 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Koonin, E.V., Altschul, S.F. and Bork, P. 1996. Functional motifs. Nature Genet. 13: 266–268.

    Article  CAS  PubMed  Google Scholar 

  • Mandel, M.A., Feldmann, K.A., Herrera-Estrella, L., Rocha-Sosa, M. and Leon, P. 1996. CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J. 5: 649–658.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 18: 100–127.

    Google Scholar 

  • Nakai, K. and Horton, P. 1999. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24: 34–36.

    Article  CAS  PubMed  Google Scholar 

  • Neuwald, A.F. and Landsman, D. 1997. GCN5-related histone N acetyltransferases belong to a diverse superfamily that includes the yeast SPT10 protein. Trends Biochem. Sci. 22: 154–155.

    Article  CAS  PubMed  Google Scholar 

  • Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H. and Höfte H. 1998. A plasma membrane-bound putative endo-1,4-β-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17: 5563–5576.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Prot. Eng. 10: 1–6.

    Article  CAS  Google Scholar 

  • Nielson, H. and Krogh, A. 1998. Prediction of signal peptides and signal anchors by a hidden Markov model. In: Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology (ISMB6), AAAI Press, Menlo Park, CA, pp. 122–130.

    Google Scholar 

  • Odell, J.T., Nagy, F. and Chua, N.H. 1985. Identification of DNA sequences required for activity of the cauliflower mosaic virus-35S promoter. Nature 313: 810–812.

    Article  CAS  PubMed  Google Scholar 

  • Pagant, S., Bichet, A., Sugimoto, K., Lerouxel, O., Desprez, T., McCann, M., Lerouge, P., Vernhettes, S. and Höfte, H. 2002. KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14: 2001–2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rojo, E., Sharma, V.K., Kovaleva, V., Raikhel, N.V. and Fletcher, J.C. 2002. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14: 969–977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schumacher, K., Vafeados, D., McCarthy, M., Sze, H., Wilkins, T. and Chory, J. 1999. The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development. Genes Dev. 13: 3259–3270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sundberg, E., Slagter, J.G., Fridborg, I., Cleary, S.P., Robinson, C. and Coupland, G. 1997. ALBIN03, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9: 717–730.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sze, H., Li, X. and Palmgren, M.G. 1999. Energization of plant cell membranes by H+-pumping ATPases: regulation and biosynthesis. Plant Cell 11: 677–689.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Szekeres, M., Németh, K., Koncz-Kálmán, Z., Mathur, J., Kauschmann, A., Altmann, T., Rédei, G.P., Nagy, F., Schell, J. and Koncz C. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85: 171–182.

    Article  CAS  PubMed  Google Scholar 

  • Zhong, R., Kays, S.J., Schroeder, B.P. and Ye Z.-H. 2002. Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14: 165–179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant and Microbial Biology, University of California, Berkeley, CA, 94720, USA

    Kvin Lertpiriyapong & Zinmay Renee Sung

Authors
  1. Kvin Lertpiriyapong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zinmay Renee Sung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zinmay Renee Sung.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lertpiriyapong, K., Sung, Z.R. The elongation defective1 mutant of Arabidopsis is impaired in the gene encoding a serine-rich secreted protein. Plant Mol Biol 53, 581–595 (2003). https://doi.org/10.1023/B:PLAN.0000019067.05185.d6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PLAN.0000019067.05185.d6

Search

Navigation