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Molecular Genetic and Biochemical Analysis of Photomorphogenesis
Photosynthetic organisms possess the ability to finely tune their growth and developmental responses to changes in their ambient environment. The perception of light and the photomorphogenetic changes that occur as a response to light signals are among the most important adaptive responses of any organism that uses light for carbon fixation. Our long-term research interest is to understand dynamic molecular processes utilized by photosynthetic organisms for adapting to changes in their photoenvironment. Biliproteins are light-absorbing pigments involved in both photosynthesis and the regulation of photomorphogenesis in cyanobacteria, algae, and plants. In higher plants, the biliprotein phytochromes control many aspects of growth and development, from seed germination through senescence. Functional phytochrome photoreceptors depend upon the convergence of two pathways: apoproteins are encoded by nuclear-localized genes, whereas the light-absorbing chromophore is synthesized in plastids (Figure 1).
Figure 1. Model of phytochrome biosynthesis. Apophytochromes are encoded by a small, nuclear gene family (PHYA-PHYE). The phytochrome chromophore, phytochromobilin (PΦB), is synthesized in plant plastids. Holophytochrome is formed in the cytosol by the binding and subsequent covalent attachment of PΦB to apophytochrome. The impact of plastidic and cytosolic biliverdin reductase (BVR) expression on linear tetrapyrroles biliverdin IXα (BVIXα) and PΦB is shown. BR, bilirubin; PΦR, phytochromorubin.
Although a great deal has been discovered about the roles of individual phytochrome family members and the intracellular signaling mechanisms of phytochromes, our understanding of the distributions and mechanisms of localized pools of phytochrome, which define the sites of phytochrome photoperception and regulate organ-specific light responses within plants, is limited. We are conducting molecular studies to broaden our understanding of organ-specific phytochrome responses in plants. It has been demonstrated previously that constitutive expression of the gene encoding the mammalian enzyme biliverdin IX-alpha reductase (BVR) in transgenic Arabidopsis and tobacco plants alters light-dependent growth and development by metabolically inactivating the precursors of the phytochrome chromophore (Figure 1; Montgomery et al., 1999; 2001). We have adapted transgenic BVR expression as a molecular tool for probing localized phytochrome responses. Recent studies have demonstrated that localized BVR expression affects distinct aspects of light-mediated plant growth and development. The phytochrome-dependent phenotypes that are disrupted differ for lines using constitutive or tissue-specific promoters for BVR expression (Warnasooriya and Montgomery, 2009).
Figure 2. Cells of the cyanobacterium Fremyella diplosiphon appear brick red in color under green light growth conditions (left) owing to the accumulation of GL-absorbing proteins. Under red light growth conditions (right), cells appear blue-green as a result of accumulation of pigments that maximally absorb RL. This response is controlled by a phytochrome-like biliprotein photoreceptor RcaE.
A second area of study focuses on complementary chromatic adaptation (CCA). Cells of the cyanobacterium Fremyella diplosiphon appear brick red in color when grown under green light (GL) due to the accumulation of GL-absorbing proteins (Figure 2, left panel). When grown under red light (RL), cells appear blue-green due to the accumulation of pigments that maximally absorb RL (Figure 2, right panel). CCA, a specific form of photomorphogenesis in some cyanobacteria, is controlled by a biliprotein photoreceptor with significant similarity to plant phytochromes. Biochemical characterization of the light-regulated signal transduction cascade controlling CCA is expanding our knowledge of the complex signaling cascades controlled by phytochrome-like proteins in prokaryotic systems, including recent insight into the regulation of morphology in addition to pigmentation (e.g., Bordowitz and Montgomery, 2010; Pattanaik and Montgomery, 2010b). In summary, our current studies focus on the synthesis of photosensory biliproteins and their physiological roles during selected aspects of photomorphogenesis in the model plant Arabidopsis and in cyanobacteria.