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Evolution and functional diversification of the small heat shock protein/α-crystallin family in higher plants

Planta volume 235, pages 1299–1313 (2012)Cite this article

Abstract

Small heat shock proteins (sHSPs) are chaperones that play an important role in stress tolerance. They consist of an alpha-crystallin domain (ACD) flanked by N- and C-terminal regions. However, not all proteins that contain an ACD, hereafter referred to as ACD proteins, are sHSPs because certain ACD proteins are known to have different functions. Furthermore, since not all ACD proteins have been identified yet, current classifications are incomplete. A total of 17 complete plant proteomes were screened for the presence of ACD proteins by HMMER profiling and the identified ACD protein sequences were classified by maximum likelihood phylogeny. Differences among and within groups were analysed, and levels of functional constraint were determined. There are 29 different classes of ACD proteins, eight of which contain classical sHSPs and five likely chaperones. The other classes contain proteins with uncharacterised or poorly characterised functions. N- and C-terminal sequences are conserved within the phylogenetic classes. Phylogenetics suggests a single duplication of the CI sHSP ancestor that occurred prior to the speciation of mono- and dicotyledons. This was followed by a number of more recent duplications that resulted in the presence of many paralogues. The results suggest that N- and C-terminal sequences of sHSPs play a role in class-specific functionality and that non-sHSP ACD proteins have conserved but unexplored functions, which are mainly determined by subsequences other than that of the ACD.

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Abbreviations

ACD:

Alpha-crystallin domain

CAM:

C-terminal anchoring module

MC:

Monophyletic clades

MSA:

Multiple sequence alignment

NaLi:

Sodium–lithium tolerance

sHSPs:

Small heat shock proteins

UAP:

Uncharacterised ACD protein

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Acknowledgments

Financial resources: Universidad Nacional de Mar del Plata, project EXA468/09; HGB is a postdoctoral fellow at CONICET; EMV and AtH are members of CONICET research career.

A. lyrata, B. distachyon, C. papaya, C. sativus, M. esculenta, M. guttatus, M. truncatula, P. persica, R. communis, V. vinifera and Z. mays sequence data were produced by the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/) in collaboration with the user community (Phytozome v5).

Conflict of interest

The authors declare that they have no conflict of interest.

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Affiliations

  1. Facultad de Ciencias Exactas y Naturales, Instituto de Investigaciones Biológicas (IIB-CONICET-UNMdP), Universidad Nacional de Mar del Plata, CC 1245, 7600, Mar del Plata, Argentina

    Hernán Gabriel Bondino & Arjen ten Have

  2. Facultad de Ciencias Bioquímicas y Farmacéuticas, Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Universidad Nacional de Rosario, Suipacha 531, S2002LRK, Rosario, Argentina

    Estela Marta Valle

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  1. Hernán Gabriel Bondino
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  2. Estela Marta Valle
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Correspondence to Arjen ten Have.

Electronic supplementary material

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Supplemental Data file S1 Complete Sequences of 824 ACD proteins (FASTA format). The first two letters of the accession codes correspond to the plant species: AL, A. lyrata; AT, A. thaliana; BD, B. distachyon; CP, C. papaya; CS, C. sativus; GM, G. max; ME, M. esculenta; MG, M. guttatus; MT, M. truncatula; OS, O. sativa; PP, P. persica; PT, P. trichocarpa; RC, R. communis; SB, S. bicolor; SL, S. lycopersicum; VV, V. vinifera; ZM, Z. mays

Supplemental Data file S2 Truncated MSA (Clustal format). The first two letters of the accession codes correspond to the plant species: AL, A. lyrata; AT, A. thaliana; BD, B. distachyon; CP, C. papaya; CS, C. sativus; GM, G. max; ME, M. esculenta; MG, M. guttatus; MT, M. truncatula; OS, O. sativa; PP, P. persica; PT, P. trichocarpa; RC, R. communis; SB, S. bicolor; SL, S. lycopersicum; VV, V. vinifera; ZM, Z. mays

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Bondino, H.G., Valle, E.M. & ten Have, A. Evolution and functional diversification of the small heat shock protein/α-crystallin family in higher plants. Planta 235, 1299–1313 (2012). https://doi.org/10.1007/s00425-011-1575-9

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Keywords

  • Alpha-crystallin domain
  • Chaperone
  • Comparative genomics
  • Molecular evolution
  • Small heat shock proteins
  • Stress