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Plant cells coordinately regulate the expression of nuclear and plastid genes that encode components of the photosynthetic apparatus. Nuclear genes that regulate chloroplast development and chloroplast gene expression provide part of this coordinate control. However, there is compelling evidence that information also flows in the opposite direction, from chloroplasts to the nucleus. This hypothesised, second pathway functions to coordinate the expression of nuclear genes encoding components of the photosynthetic apparatus with the functional state of the chloroplast. Here we review the evidence for the signal transduction pathway from the chloroplasts to the nucleus and suggest possible signal molecules.

Alalysis of the cloned gene confirms that hsp26 of Saccharomyces cerevisiae is a member of the small heat shock protein superfamily. Previous mutational analysis failed to demonstrate any function for the protein.Further experiments presented here demonstrate that hsp26 has no obvious regulatory role and no major effect on thermotolerance. It is possible that the small heat shock protein genes originated as primitive viral or selfish DNA elements.All organisms respond to heat and other stresses by synthesizing a set of proteins named the heat shock proteins (HSPs). Of the major HSPs, the small HSPs are the most diverse group and the most elusive with respect to function. These proteins range in size from 15 (8) to 40 (28) kilodaltons (kDa). Moreover, the number of small-HSP genes per haploid genome varies from 1 in Saccharomyces cerevisiae (34) to more than 30 in plants (27). Despite this diversity, the small HSPs share a number of properties by which they may be grouped together as a distinct protein family. First, the small HSPs from different organisms are highly induced, not only in response to stress, but also during the course of normal development, when certain other HSPs are not induced (25). Second, the small HSPs of distantly related organisms contain short regions of amino acid identity (8,16,18,21,28,29,38). Finally, the small HSPs of diverse species form morphologically distinctive 15 to 20S complexes in stressed cells (1,31,40).Functions of small HSPs. The function(s) of the small HSPs is obscure. One approach to determining the functions has been to examine the patterns of intracellular distribution. Immunolocalization studies show that the small HSPs of plants, Drosophila melanogaster, and mammalian cells form large cytoplasmic particles called heat shock granules (HSGs) (1, 2, 31, 40). In cell fractionation studies with tomato cells, control mRNAs, but not heat shock mRNAs, copurify with the HSGs and are sequestered away from the pool of actively translated heat shock messages during the stress (31). Thus, it has been proposed that the small HSPs and the HSGs of tomato play a role in translational regulation of the heat shock response. Although hsp26 of S. cerevisiae forms large aggregates (37) (ii) no other protein is noticeably overexpressed in compensation for the loss of hsp26 in hsp26 mutants; (iii) no other protein is recognized by a polyclonal antiserum raised against hsp26; and (iv) no other gene can be detected by low-stringency hybridization with an HSP26 probe (34). It might seem unlikely, then, that another small HSP is providing protection against thermal stress in the absence of hsp26. However, considering the extreme sequence divergence among the small HSPs of other species, it is possible that a minor heat-inducible protein or a major constitutively synthesized protein escaped identification by these criteria yet compensated for the loss of hsp26. If, indeed, the function of hsp26 is masked by another protein in hsp26 mutants, it might be possible to uncover the function of hsp2...

Chloroplast development requires the coordinated expression of nuclear and chloroplastic genes. A hypothesized signal from the chloroplast couples the transcription of certain nuclear genes encoding photosynthetic proteins with chloroplast function. We have previously described an Arabidopsis fhaliana mutant, gunl, which has a defect in the signal transduction pathway coupling such nuclear and plastidic gene expression. Here we show that gunt seedlings are also defective in establishing photoautotrophic growth. gunl seedlings develop normally in the dark, but, based on morphologicai criteria and the kinetics of chlorophyll accumulation, photosynthetic mRNA accumulation, and the differentiation of etioplasts to chloroplasts, are retarded in their ability to de-etiolate. Therefore, we propose that the GUNl gene plays an important role in the transition from heterotrophic to photoautotrophic growth, suggesting an important physiological role for the plastid-nucleus signaling pathway during chloroplast biogenesis.

hsp26, the small heat shock protein of Saccharomyces cerevisiae, accumulates in response to heat and other types of stress. It also accumulates during the normal course of development, as cells enter stationary phase growth or begin to sporulate (S. Kurtz, J. Rossi, L. Petko, and S. Lindquist, Science 231:1154-1157, 1986). Analysis of deletion and insertion mutations demonstrated that transcriptional control plays a critical role in regulating HSP26 expression. The HSP26 promoter was found to be complex and appears to contain repressing elements as well as activating elements. Several upstream deletion mutations resulted in strong constitutive expression of HSP26. Furthermore, upstream sequences from the HSP26 gene repressed the constitutive expression of a heterologous heat shock gene. We propose that basal repression and heat-induced depression of transcription play major roles in regulating the expression of HSP26. None of the recombinant constructs that we analyzed separated cis-regulatory sequences responsible for heat shock regulation from those responsible for developmental regulation of HSP26. Depression of HSP26 transcription may be the general mechanism of HSP26 induction in yeast cells. This regulatory scheme is very different from that described for the regulation of most other heat shock genes.