The evolutionary history of calreticulin and calnexin genes in green plants

Abstract

Calreticulin and calnexin are Ca2+-binding chaperones localized in the endoplasmic reticulum of eukaryotes acting in glycoprotein folding quality control and Ca2+ homeostasis. The evolutionary histories of calreticulin and calnexin gene families were inferred by comprehensive phylogenetic analyses using 18 completed genomes and ESTs covering the major green plants groups, from green algae to angiosperms. Calreticulin and calnexin possibly share a common origin, and both proteins are present along all green plants lineages. The calreticulin founder gene within green plants duplicated in early tracheophytes leading to two possible groups of orthologs with specialized functions, followed by lineage-specific gene duplications in spermatophytes. Calnexin founder gene in land plants was inherited from basal green algae during evolution in a very conservative copy number. A comprehensive classification in possible groups of orthologs and a catalog of calreticulin and calnexin genes from green plants are provided.

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

Fig. 1

References

  1. Baluska F, Samaj J, Napier R, Volkmann D (1999) Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 19:481–488

    CAS  Article  PubMed  Google Scholar 

  2. Chen MH, Tian GW, Gafni Y, Citovsky V (2005) Effects of calreticulin on viral cell-to-cell movement. Plant Physiol 138:1866–1876

    CAS  Article  PubMed  Google Scholar 

  3. Christensen A, Svensson K, Persson S, Jung J, Michalak M, Widell S, Sommarin M (2008) Functional characterization of Arabidopsis calreticulin1a: a key alleviator of endoplasmic reticulum stress. Plant Cell Physiol 49:912–924

    CAS  Article  PubMed  Google Scholar 

  4. Christensen A, Svensson K, Thelin L, Zhang W, Tintor N, Prins D, Funke N, Michalak M, Schulze-Lefert P, Saijo Y, Sommarin M, Widell S, Persson S (2010) Higher plant calreticulins have acquired specialized functions in Arabidopsis. PLoS One 5(6):e11342

    Article  PubMed  Google Scholar 

  5. Crofts AJ, Denecke J (1998) Calreticulin and calnexin in plants. Trends Plants Sci 3:396–399

    Article  Google Scholar 

  6. Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. Natl Biomed Res Found, Washington, pp 345–352

  7. Del Bem LEV, Vincentz MGA (2010) Evolution of xyloglucan-related genes in green plants. BMC Evol Biol 10:341

    Article  PubMed  Google Scholar 

  8. Eck RV, Dayhoff MO (1966) Atlas of protein sequence and structure. National biomedical research foundation, Silver Springs

    Google Scholar 

  9. Felsenstein J (1989) PHYLIP–Phylogeny inference package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  10. Hammond C, Braakman I, Helenius A (1994) Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc Natl Acad Sci USA 91(3):913–917

    CAS  Article  PubMed  Google Scholar 

  11. Huang L, Franklin AE, Hoffman NE (1993) Primary structure and characterization of an Arabidopsis thaliana calnexin-like protein. J Biol Chem 268:6560–6566

    CAS  PubMed  Google Scholar 

  12. Jia XY, Xu CY, Jing RL, Li RZ, Mao XG, Wang JP, Chang XP (2008) Molecular cloning and characterization of wheat calreticulin (CRT) gene involved in drought-stressed responses. J Exp Bot 59:739–751

    CAS  Article  PubMed  Google Scholar 

  13. Jin H, Hong Z, Su W, Li J (2009) A plant-specific calreticulin is a key retention factor for a defective brassinosteroid receptor in the endoplasmic reticulum. PNAS 106(32):13612–13617

    CAS  Article  PubMed  Google Scholar 

  14. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298

    CAS  Article  PubMed  Google Scholar 

  15. Laporte C, Vetter G, Loudes AM, Robinson DG, Hillmer S, Stussi-Garaud C, Ritzenthaler C (2003) Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell 15:2058–2075

    CAS  Article  PubMed  Google Scholar 

  16. Li J, Zhao-Huia C, Batoux M, Nekrasov V, Roux M, Chinchilla D, Zipfel C, Jones JDG (2009) Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. PNAS 106(37):15973–15978

    CAS  Article  PubMed  Google Scholar 

  17. Michalak M, Groenendyk J, Szabo E, Gold LI, Opas M (2009) Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J 417:651–666

    CAS  Article  PubMed  Google Scholar 

  18. Papini-Terzi FS, Rocha FR, Vêncio RZ, Felix JM, Branco DS, Waclawovsky AJ, Del Bem LEV, Lembke CG, Costa MD, Nishiyama MY Jr, Vicentini R, Vincentz MG, Ulian EC, Menossi M, Souza GM (2009) Sugarcane genes associated with sucrose content. BMC Genomics 10:120

    Article  PubMed  Google Scholar 

  19. Persson S, Wyatt SE, Love J, Thompson WF, Robertson D, Boss WF (2001) The Ca(2+) status of the endoplasmic reticulum is altered by induction of calreticulin expression in transgenic plants. Plant Physiol 126:1092–1104

    CAS  Article  PubMed  Google Scholar 

  20. Persson S, Rosenquist M, Svensson K, Galvão R, Boss WF, Sommarin M (2003) Phylogenetic analyses and expression studies reveal two distinct groups of calreticulin isoforms in higher plants. Plant Physiol 133:1385–1396

    CAS  Article  PubMed  Google Scholar 

  21. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  Article  PubMed  Google Scholar 

  22. Saijo Y, Tintor N, Lu X, Rauf P, Pajerowska-Mukhtar K, Haweker H, Dong X, Robatzek S, Schulze-Lefert P (2009) Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J 28:3439–3449

    CAS  Article  PubMed  Google Scholar 

  23. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  24. Schrag JD, Bergeron JJM, Li Y, Borisova S, Hahn M, Thomas DY, Cygler M (2001) The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol Cell 8(3):633–644

    CAS  Article  PubMed  Google Scholar 

  25. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    CAS  Article  PubMed  Google Scholar 

  26. Ware FE, Vassilakos A, Peterson PA, Jackson MR, Lehrman MA, Williams DB (1995) The molecular chaperone calnexin binds Glc1Man9GlcNAc2 oligosaccharide as an initial step in recognizing unfolded glycoproteins. J Biol Chem 270:4697–4704

    CAS  Article  PubMed  Google Scholar 

  27. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18(5):691–699

    CAS  PubMed  Google Scholar 

Download references

Acknowledgment

I would like to thank the JGI (www.jgi.doe.gov/) for providing most of the data used in this work.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Luiz Eduardo V. Del Bem.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

CRT and CNX Possible Groups of Orthologous (PoGOs) in green plants (XLS 44 kb)

Supplemental Figure 1

Detailed phylogenetic analysis of CNXs in green plants. Tree topology is a consensus from NJ, MP and Bayesian analyses. Bootstrap values and posterior probabilities from the original trees higher than 50% are shown (NJ/MP/Bayesian).

Supplemental Figure 2

Detailed phylogenetic analysis of CRTs in green plants. Tree topology is a consensus from NJ, MP and Bayesian analyses. Bootstrap values and posterior probabilities from the original trees higher than 50% are shown (NJ/MP/Bayesian).

Supplemental Figure 3

Shared intron positions betweenArabidopsis thaliana,Sorghum bicolor, Physcomitrella patens patensandVolvox carteri CNX genes. Single amino acid positions, highlighted in blue, represents intron location within the corresponding codon and double amino acid positions, highlighted in red, represent intron location between two codons. Supplementary material 4 (TIFF 349 kb)

Supplemental Figure 3

Shared intron positions betweenArabidopsis thaliana,Sorghum bicolor, Physcomitrella patens patensandVolvox carteri CRT genes. Single amino acid positions, highlighted in blue, represents intron location within the corresponding codon and double amino acid positions, highlighted in red, represent intron location between two codons. Supplementary material 5 (TIFF 341 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Del Bem, L.E.V. The evolutionary history of calreticulin and calnexin genes in green plants. Genetica 139, 255–259 (2011). https://doi.org/10.1007/s10709-010-9544-y

Download citation

Keywords

  • Calreticulin
  • Calnexin
  • Chaperones
  • Evolution
  • Green plants