Translational Regulation during Photomorphogenesis

Overview

Algae and plants depend on light as the primary environmental stimulus regulating their developmental patterns, as well as their primary energy source. As just two examples, light triggers the development of proplastids into functional chloroplasts in photoautotrophs as divergent as Euglena and peas, and regular cycles of alternating light and darkness have the effect of synchronizing reproductive behavior within populations of organisms as divergent as Chlamydomonas and petunias. The phenomena of light-regulated development, or photomorphogenesis, have been extensively reviewed (as exemplified by several books^1–4) and hence no comprehensive summary of them will be given here. Suffice it to say, it is by now well established that marked changes in gene expression occur in a wide range of photoautotrophs in response to light absorbed by one of three categories of photoreceptor pigments (namely, protochlorophyllide, phytochrome, or one of the incompletely defined group of pigments known as “blue-light receptors”). This brief review chapter focuses on the question of what role translational regulation may play in mediating such photoregulated gene expression in plants and algae.

Over the past decade, most attempts to analyze the molecular basis of photomorphogenesis have employed methods specifically designed to detect light-induced changes at the level of messenger RNA (mRNA) accumulation. Not surprisingly, therefore, such effects are by now well established: In many photoregulated systems, changes have been detected in the formation or accumulation, or both, of transcripts from specific nuclear and plastid genes as a consequence of changes in the light quantity or quality (for a recent review see Tobin and Silverthorne⁵). Indeed, in the jargon of the field, the term photogene appears to have become synonymous with a gene for which such transcription-level effects of light have been demonstrated.⁶

The purpose of reviewing the more modest, but growing, body of evidence that translational regulation is centrally important in some photoregulated systems is not to cast doubt on the existence or importance of previously reported transcription-level effects. In many cases, the latter are both clearly established and of obvious importance, and students of gene expression anticipate eagerly the future elucidation of mechanisms whereby absorption of particular wavelengths of light can be transduced into locus-specific transcriptional changes. But demonstration of a regulatory effect at one level never automatically implies absence of regulatory effects at other levels, of course. Indeed, it is now apparent that in many biological systems, multiple levels of control exist side by side. And, as we will see, this is frequently the case in photomorphogenesis.

The emphasis herein will be on systems in which the effects of light at the translational level appear to be more rapid, or quantitatively more important, or both, than changes at the transcriptional level in regulating synthesis of the corresponding protein. However, such results should not be extrapolated to systems other than those in which they have been observed. Generalization of mechanisms that underlie photomorphogenesis appears to be particularly difficult, since (as we will see below) different mechanisms may be involved in regulating the synthesis of related polypeptides within a single cell. Nevertheless, the demonstration that some systems that exhibit photoregulated transcript accumulation also exhibit earlier and/or more substantial effects of light on translation should be sufficient to call into question whether the mere demonstration of a transcription-level effect should ever be considered tantamount to establishing the molecular basis of photomorphogenesis in a system in which the extent of translational regulation has not yet been evaluated.