Photoreceptors in Plant Photomorphogenesis to Date. Five Phytochromes, Two Cryptochromes, One Phototropin, and One Superchrome

Abstract

Plants are bombarded by a myriad of signals, not just from their physical environment, but from friend and foe alike. As a consequence, they have evolved a remarkably sophisticated system of receptors and signal transduction pathways that generate appropriate responses. That light plays a major signaling role in plant development is not surprising. A plant's ability to maximize its photosynthetic productivity depends on its capacity to sense, evaluate, and respond to light quality, quantity, and direction. Likewise, the timing of developmental phenomena, such as flowering or entrance into dormancy, depends on a system of measuring and responding to changes in daylength. This article briefly explores how plant biologists have identified the various photoreceptors and how they have elucidated some of the early events in the transduction of light signals to ultimate plant responses. A red, far-red-reversible chromoprotein, phytochrome, was the first photoreceptor identified. It is now known that multiple phytochromes exist and sometimes act independently of one another, sometimes redundantly, sometimes antagonistically, sometimes at the same time in development, and sometimes at different times. The first blue-light receptors to be identified were the two cryptochromes, chromoproteins that mediate several responses. More recently, another blue-light-absorbing chromoprotein, phototropin, has been identified as a photoreceptor mediating phototropism. A chimeric photoreceptor, phytochrome 3 (phy3), has been identified that contains both phytochrome and phototropin sequence motifs. For each of these photoreceptors, gene sequences are known, and plant biologists are working toward a greater understanding of their roles in plant development. Let us take a brief look at the events leading to our present knowledge of higher plant photoreceptors. Just over 40 years ago, workers at the U.S. Department of Agriculture laboratories (Beltsville, MD) discovered the first signaling photoreceptor in plants, a photoreversible pigment (9) that they called phytochrome (8). In the following years, photomorphogenesis (a study of the influence of light on plant development) developed as a strong subdiscipline of the field of plant physiology. Within this subdiscipline was a sharp division between those pursuing the phytochromes and those pursuing distinct blue-light receptors. Those studying phytochrome(s) had an enormous advantage in having at their disposal all of the classic phytochrome-mediated responses that were activated by brief pulses of red light interrupting darkness: These include activation of seed germination, inhibition of stem elongation in dark-grown seedlings, induction of leaf expansion, and regulation of flowering. In every case, the effect of red light was negated by subsequent immediate exposure to far-red light. This kind of photoreversibility was regarded as unassailable evidence for the participation of phytochrome. Borthwick et al. (3) had already predicted the existence of a photochromic pigment with red- and far-red-absorbing forms, and it was theoretically a simple matter for the Beltsville group to identify such a pigment. (In reality, it was not simple, as it required the development of some incredibly ingenious spectroscopy.) During the mid-1970s it was generally assumed that a single phytochrome mediated the many red-, far-red-reversible photoresponses, and frantic efforts were under way in several laboratories to purify it and carry out its biochemical characterization (7). However, it was only in 1983 that both the Quail and Lagarias laboratories reported the purification of un-degraded phytochrome and in 1987 reported that the first phytochrome gene sequence was published (see 4). By 1989, we knew that there were at least two different phytochromes in pea (1) and five different phytochromes in Arabidopsis (20). All of these phytochromes show varying degrees of amino acid sequence identity and similarity, and all of them carry a bilitriene chromophore phytochromobilin (14, 22). The Lagarias laboratory recently has provided convincing evidence that phytochrome functions as a photoreceptor kinase (an unusual Ser/Thr kinase with two His kinase-like domains; 25). Current work based on molecular genetic studies that rely heavily on photomorphogenic mutants has made significant progress in unraveling downstream elements in the various phytochrome signal transduction pathways. These include signaling components such as heterotrimeric G proteins, cyclic GMP, calcium nucleotide diphosphate kinase 2, and calcium, as well as transcriptional regulators. In addition, both phytochrome A and phytochrome B have been shown to migrate into the nucleus under certain conditions, consistent with their proposed action at the transcriptional level in some of the responses they mediate (for phytochrome references, see 16). After years of frustration, two laboratories have identified potential partners that interact direct