Light-Regulated Transcription of Genes Encoding Peridinin Chlorophyll a Proteins and the Major Intrinsic Light-Harvesting Complex Proteins in the DinoflagellateAmphidinium carterae Hulburt (Dinophycae)1

Abstract

In the dinoflagellate Amphidinium carterae, photoadaptation involves changes in the transcription of genes encoding both of the major classes of light-harvesting proteins, the peridinin chlorophyll a proteins (PCPs) and the major a/c-containing intrinsic lightharvesting proteins (LHCs). PCP and LHC transcript levels were increased up to 86-and 6-fold higher, respectively, under low-light conditions relative to cells grown at high illumination. These increases in transcript abundance were accompanied by decreases in the extent of methylation of CpG and CpNpG motifs within or near PCP-and LHC-coding regions. Cytosine methylation levels in A. carterae are therefore nonstatic and may vary with environmental conditions in a manner suggestive of involvement in the regulation of gene expression. However, chemically induced undermethylation was insufficient in activating transcription, because treatment with two methylation inhibitors had no effect on PCP mRNA or protein levels. Regulation of gene activity through changes in DNA methylation has traditionally been assumed to be restricted to higher eukaryotes (deuterostomes and green plants); however, the atypically large genomes of dinoflagellates may have generated the requirement for systems of this type in a relatively "primitive" organism. Dinoflagellates may therefore provide a unique perspective on the evolution of eukaryotic DNA-methylation systems.In many respects dinoflagellates are an unusual group of chromophytic algae, their closest relatives being the apicomplexans (van der Peer et al., 1993). For example, uniquely among eukaryotes, their chromatin appears to be entirely devoid of histones (Rizzo, 1981(Rizzo, , 1991 and is not organized in the normal nucleosomal structure (Herzog and Soyer, 1981). Light harvesting is mediated in dinoflagellates by two classes of proteins, the PCPs and the LHCs. PCP, a water-soluble protein containing the carotenoid peridinin, is unique to dinoflagellates and appears to be unrelated to any other light-harvesting protein (Norris and Miller, 1994), whereas the LHCs are related to the cab proteins of higher plants (Hiller et al., 1993) and their algal homologs (for review, see Grossman et al., 1990). Both PCPs and LHCs are present in multiple forms in dinoflagellates. The functional significance of this and the nature of the interaction between these two classes of lightharvesting proteins are completely unknown. Chromophyte chloroplasts appear to lack many of the mechanisms known to be central to photoadaptation in chlorophytes, such as lateral mobility of photosynthetic complexes and stacking/unstacking of thylakoids. One hypothesis is that the multiple forms of light-harvesting proteins fulfill related roles in dinoflagellates, i.e. that the synthesis of different PCP and LHC complements facilitates photoadaptation.In Amphibinium carterae, both PCPs and LHCs are encoded by nuclear genes (Hiller et al., 1995;Sharples et al., 1996) and synthesized with N-terminal transit peptides directing chloroplast translocation (Norris and...

Eukaryotic DNA methylation as an evolutionary device

“…(9,12) In the dinoflagellate protist Amphidinium carterae, genes encoding light-harvesting proteins exhibit hypermethylation in response to a regimen of increased light. (25) Given examples such as these, the absence of any detectable methylation in some organisms does not necessarily imply a true lack of methylation. It may instead reflect the existence in these organisms of dynamic methylation and demethylation processes, or else fractional methylation of genomes particularly poor in repeats.…”

“…(21) Moreover, although methylation of cellular genes has long been held as a distinctive feature of vertebrates and has been related to their uniquely large gene set, (22) methylated genes are found in invertebrates close to the vertebrate boundary (21) as well as in plants, (23) and anecdotal reports of methylated genes exist for an insect (24) and a protist. (25) Differences in methylation patterns between eukaryotes may often be primarily a reflection of differences in the distribution of repeats within the genome. For instance, the genome-wide methylation characteristic of mammals could be explained simply by an almost systematic colonization of the nontranslated regions of the transcribed part of their genes by mobile elements, (18) and by the spread of methylation into adjacent single copy sequences.…”

Different Regulatory Mechanisms Modulate the Expression of a Dinoflagellate Iron-Superoxide Dismutase

“…Whether this is caused by increased transcription or slower degradation of mRNA, or both, cannot be specified. Transcriptional control of the expression of other genes in dinoflagellates has been reported recently (38,39), and in other eukaryotes transcription of SOD genes is activated by redox-sensitive transcription factors such as AP-1 and NF-B (40,41). Indeed, the promoter regions of many eukaryotic SOD genes contain multiple regulatory elements responsible for transcriptional control in response to a variety of stimuli (42)(43)(44).…”

Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium

“…The influence of temperature on the steady-state pool of acpPC mRNA was measured by quantitative RT-PCR and normalized to the level of the housekeeping gene ub52 transcript (18). No difference in the initial level of acpPC transcript was found between OTcH-1 and CS-73 (data not shown).…”