A genomics approach to the chaperone network of Arabidopsis thaliana

In 1962, the pioneering work of Ritossa led to one of the most important discoveries in modern cell biology. After a serendipitous increase in the temperature of the incubator with Drosophila cultures, he observed remarkable changes of the puffing, ie, gene activity patterns, of the polytene chromosomes in larval salivary glands (Ritossa 1962). Surprisingly, the same reprogramming of transcription was also observed with chemical stressors, such as salicylate, 2,4-dinitrophenol, and azide. About 10 years later, Tissieres et al (1974) identified the newly formed heat shock proteins (Hsps). Soon, the rapidly developing field included investigations of other eukaryotic organisms and bacteria. Ritossa had, in fact, discovered the central parts of a general stress response system conserved throughout the living world (for references to early literature, see Ashburner and Bonner 1979; Nover et al 1989; Nover 1991; Vierling 1991).

Today, the term heat stress protein is used in a broad sense to define related proteins belonging to 11 multiprotein families, whose members are structurally and functionally conserved among bacteria, plants, and animals. Only a few of them are strictly heat stress–inducible proteins. Many others are constitutively present, and their expression can be increased under stress conditions. Finally, some of these proteins are also expressed in a cell-specific manner at specific developmental stages. During the last decade, more and more details of the biochemical function of Hsps have emerged. As molecular chaperones, they help other proteins maintain or regain their native conformation by stabilizing partially unfolded states. They do not contain specific information for correct folding, but rather prevent unproductive interactions (aggregation) between nonnative proteins. Frequently, proteins from different Hsp families are combined in multisubunit complexes, so-called chaperone machines (Bukau and Horwich 1998), and these chaperone complexes may interact to generate a network for protein maturation, assembly, and targeting (Forreiter and Nover 1998; Agashe and Hartl 2000; Ellis 2000; Feldman and Frydman 2000; MacRae 2000; Pearl and Prodromou 2000; Saibil 2000; Schleiff and Soll 2000).

Such chaperones are indispensable for the maturation of newly formed proteins. Thus, different sets of chaperones exist in all compartments of eukaryotic cells with ongoing protein synthesis and/or processing, ie, in the cytoplasm, endoplasmic reticulum, mitochondria, and chloroplasts. The essential role of these proteins not only for protein homeostasis but also for the rapid assembly and disassembly of multiprotein complexes is supported by numerous reports documenting chaperone effects on signal transduction pathways, cell cycle control, cytoskeletal rearrangements, apoptosis, tumorigenesis and neurodegenerative diseases, complex developmental pathways, and evolution (Rutherford and Lindquist 1998; Samali and Orrenius 1998; Caplan 1999; Cohen 1999; Feder and Hofmann 1999; Zahn 1999; Arrigo 2000; Cheung and Smith 2000; Ferrigno and Silver 2000; Jolly and Morimoto 2000; Kühl and Rensing 2000; Lewis et al 2000; Pearl and Prodromou 2000; Bharti and Nover 2001).

Because of their sessile and poikilothermic existence, plants are generally more affected by unfavorable environmental changes than animals. Typically, plant growth and development can be characterized as a daily multistress challenge. As a result, a multiplicity of partially overlapping stress response systems has evolved. The integrated and highly flexible stress network is characterized by a number of multivalent or even general stress metabolites and proteins.

Unicellular microbes independently gave rise to the distinctly different kingdoms, plants, and animals. Although analyses of the genomes of the simpler eukaryotes, Saccharomyces cerevisiae (Goffeau et al 1996), Caenorhabditis elegans (The C. elegans Sequencing Consortium 1998), and Drosophila melanogaster (Adams et al 2000), have provided substantial insight into physiology, biochemistry, and genetics, they represent only a limited survey. The recently completed sequencing and annotation of the nuclear genome of the model flowering plant Arabidopsis thaliana (The Arabidopsis Genome Initiative 2000) will allow us to define the genetic bases underlying the manifold differences between plants and other eukaryotes. As has been succinctly noted by Bassham and Raikhel (2000), “Plant cells are not just green yeast.” Prominent contributors to the complexity of plant cells include both the plastid family of organelles and a Byzantine extracellular matrix. Among the various subdisciplines of cell biology, the availability of the complete A thaliana nuclear genome sequence provides a unique opportunity for study of the stress response and protein folding.

In this special issue of the journal, experts from different groups have each compiled overviews of a particular chaperone family based on genome sequence information and, if available, previously published experimental results. In some instances, data from nonplant organisms have been included for the sake of comparison. It is hoped that this series of reviews not only will help provide a unified and genetically based nomenclature for molecular chaperones and heat stress transcription factors, but will also serve as a bridge leading from the theoretical, ie, DNA-sequence based, to functional proteomics of this important group of proteins. We encourage our colleagues, whatever the experimental organism, to join with us as we move enthusiastically into the genomics era of cell stress and chaperones!