Skip to main content
SpringerLink
Log in

Cold responsive EARLI1 type HyPRPs improve freezing survival of yeast cells and form higher order complexes in plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Plants have large families of proteins sharing a conserved eight-cysteine-motif (8CM) domain. The biological functions of these proteins are largely unknown. EARLI1 is a cold responsive Arabidopsis gene that encodes a hybrid proline-rich protein (HyPRP) with a three-domain architecture: a putative signal peptide at the N-terminus, a proline-rich domain (PRD) in the middle, and an 8CM domain at the C-terminus. We report here that yeast cells expressing different EARLI1 genes had significantly higher rates of freezing survival than empty-vector transformed controls. Arabidopsis plants with knocked down EARLI1 genes had an increased tendency for freezing-induced cellular damage. EARLI1-GFP fluorescence in transgenic plants and immunoblot analyses using protoplasts suggested cell wall localization for EARLI1 proteins. Immunoblot analyses showed that EARLI1 proteins form higher order complexes in plants, and that the PRD is a soluble and the 8CM an insoluble protein domain. We propose that EARLI1 proteins have a bimodular architecture in which the PRD may interact with the cell wall and the 8CM domain with the plasma membrane to protect the cells during freezing stress.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

8CM:

Eight-cysteine-motif

CaMV:

Cauliflower mosaic virus

Col:

Columbia ecotype of Arabidopsis

EL:

Electrolyte leakage

EXT:

Extensin

HyPRP:

Hybrid proline-rich protein

LTP:

Lipid transfer protein

β-ME:

β-Mercaptoethanol

PRD:

Proline-rich domain

PRP:

Proline-rich protein

RNAi:

RNA interference

References

  • Blom N, Gammeltoft S, Brunak S (1999) Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–1362

    Article  PubMed  CAS  Google Scholar 

  • Bubier J, Schläppi M (2004) Cold induction of EARLI1, a putative Arabidopsis lipid transfer protein, is light and calcium dependent. Plant Cell Environ 27:929–936

    Article  CAS  Google Scholar 

  • Chen THH, Gusta LV, Fowler DB (1983) Freezing injury and root development in winter cereals. Plant Physiol 73:773–777

    Article  PubMed  Google Scholar 

  • Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638

    Article  PubMed  CAS  Google Scholar 

  • Deutch CE, Winicov I (1995) Post-transcriptional regulation of a salt-inducible alfalfa gene encoding a putative chimeric proline-rich cell wall protein. Plant Mol Biol 27:411–418

    Article  PubMed  CAS  Google Scholar 

  • Endo S, Demura T, Fukuda H (2001) Inhibition of proteasome activity by the TED4 protein in extracellular space: a novel mechanism for protection of living cells from injury caused by dying cells. Plant Cell Physiol 42:9–19

    Article  PubMed  CAS  Google Scholar 

  • Gleave AP (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20:1203–1207

    Article  PubMed  CAS  Google Scholar 

  • Goodwin W, Pallas JA, Jenkins GI (1996) Transcripts of a gene encoding a putative cell wall-plasma membrane linker protein are specifically cold-induced in Brassica napus. Plant Mol Biol 31:771–781

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Imai R, Chang L, Otha A, Bray EA, Takagi M (1996) A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisiae. Gene 170:243–248

    Article  PubMed  CAS  Google Scholar 

  • Josè-Estanyol M, Gomis-Ruth FX, Puigdomenech P (2004) The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiol Biochem 42:355–365

    Article  PubMed  CAS  Google Scholar 

  • Kader J-C (1996) Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 47:627–654

    Article  PubMed  CAS  Google Scholar 

  • Karev GP, Wolf YI, Rzhetsky AY, Berezovskaya FS, Koonin EV (2002) Birth and death of protein domains: a simple model of evolution explains power law behavior. BMC Evol Biol 2:18

    Article  PubMed  Google Scholar 

  • Lee I, Amasino RM (1995) Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol 108:157–162

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Reeves PH, Coupland G (2000) Response of plant development to environment: control of flowering by daylength and temperature. Curr Opin Plant Biol 3:37–42

    Article  PubMed  CAS  Google Scholar 

  • Richards KD, Gardner RC (1995) pEARLI1: an Arabidopsis member of a conserved gene family. Plant Physiol 109:1497

    Article  Google Scholar 

  • Sambrook J, Maniatis T, Fritsch EF (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Press, Cold Spring Harbor, NY

    Google Scholar 

  • Showalter MA (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    Article  PubMed  CAS  Google Scholar 

  • Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89

    Article  CAS  Google Scholar 

  • Veal EA, Ross SJ, Malakasi P, Peacock E, Morgan BA (2003) Ybp1 is required for the hydrogen peroxide-induced oxidation of the Yap1 transcription factor. J Biol Chem 278:30896–30904

    Article  PubMed  CAS  Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211

    Article  PubMed  CAS  Google Scholar 

  • von Arnim AG, Deng XW, Stacey MG (1998) Cloning vectors for the expression of green fluorescent protein fusion proteins in transgenic plants. Gene 221:35–43

    Article  Google Scholar 

  • Warren G, McKown R, Marin AL, Teutonico R (1996) Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Plant Physiol 111:1011–1019

    Article  PubMed  CAS  Google Scholar 

  • Wei H, Dhanaraj AL, Arora R, Rowland LJ, Fu Y, Sun L (2006) Identification of cold acclimation-responsive rhododendron genes for lipid metabolism, membrane transport and lignin biosynthesis: importance of moderately abundant ESTs in genomic studies. Plant Cell Environ 29:558–570

    Article  PubMed  CAS  Google Scholar 

  • Weiser RL, Wallner SJ, Waddell JW (1990) Cell wall and extensin mRNA changes during cold acclimation of pea seedlings. Plant Physiol 93:1021–1026

    PubMed  CAS  Google Scholar 

  • Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdigk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27:581–590

    Article  PubMed  CAS  Google Scholar 

  • Weyman PD, Pan Z, Feng Q, Gilchrist DG, Bostock RM (2006a) A circadian rhythm-regulated tomato gene is induced by arachidonic acid and Phythophthora infestans infection. Plant Physiol 140:235–248

    Article  PubMed  CAS  Google Scholar 

  • Weyman PD, Pan Z, Feng Q, Gilchrist DG, Bostock RM (2006b) DEA1, a circadian- and cold-regulated tomato gene, protects yeast cells from freezing death. Plant Mol Biol 62:547–559

    Article  PubMed  CAS  Google Scholar 

  • Whitham SA, Wang Y (2004) Roles for host factors in plant viral pathogenicity. Curr Opin Plant Biol 7:365–371

    Article  PubMed  CAS  Google Scholar 

  • Wilkosz R, Schläppi M (2000) A gene expression screen identifies EARLI1 as a novel vernalization-responsive gene in Arabidopsis thaliana. Plant Mol Biol 44:777–787

    Article  PubMed  CAS  Google Scholar 

  • Yamada T, Kuroda K, Jitsuyama Y, Takezawa D, Arakawa K, Fujikawa S (2002) Roles of the plasma membrane and the cell wall in the responses of plant cells to freezing. Planta 215:770–778

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Ohta A, Takagi M, Imai R (2000) Expression of plant group 2 and group 3 lea genes in Saccharomyces cerevisiae revealed functional divergence among LEA proteins. J Biochem 127:611–616

    PubMed  CAS  Google Scholar 

  • Zhang JH, Jia WS, Yang JC, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res 97:111–119

    Article  Google Scholar 

Download references

Acknowledgment

We are grateful to J. Anderson (Marquette University, Milwaukee, WI, USA) and members of his lab for help with yeast experiments; to J. Bubier and G. T. Hayman (Marquette University) for generating EARLI1 knockdown lines; to M. Nagao (Iwate University, Morioka, Japan) for help with the electrolyte leakage assays; and to Y. Pan (Marquette University) for protoplast preparation. The phosphorimager was provided by NSF Instrumentation grant No. D.B.I. 0100667. This research was supported by NRI Competitive Grant No. 2001-35100-10688 from the US Department of Agriculture.

Author information

Author notes

  1. Yi Zhang

    Present address: Biotechnology and Bioengineering Center, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI, 53226, USA

Authors and Affiliations

  1. Department of Biological Sciences, Marquette University, 530 North 15th Street, Milwaukee, WI, 53233, USA

    Yi Zhang & Michael Schläppi

Authors
  1. Yi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Schläppi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Schläppi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Y., Schläppi, M. Cold responsive EARLI1 type HyPRPs improve freezing survival of yeast cells and form higher order complexes in plants. Planta 227, 233–243 (2007). https://doi.org/10.1007/s00425-007-0611-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-007-0611-2

Keywords

Search

Navigation