Phytochrome signal transduction pathways are regulated by reciprocal control mechanisms

Three signal transduction pathways, dependent on cGMP and/or calcium, are utilized by phytochrome to control the expression of genes required for chloroplast development and anthocyanin biosynthesis in plant cells. For example, chs is controlled by a cGMP-dependent pathway, cab is controlled by a calcium-dependent pathway, and fnr is regulated by a pathway that requires both cGMP and calcium. Using a soybean photomixotrophic cell culture and microinjection into the cells of a phytochrome-deficient tomato mutant, we have studied the regulatory mechanisms acting within and between these three signaling pathways. We provide evidence that changes in cGMP levels mediate the observed induction and desensitization of chs gene expression in response to light and demonstrate that high cGMP concentrations cause negative regulation of both the calcium- and the calcium/cGMP-dependent pathways. Conversely, high activity of the calcium-dependent pathway can negatively regulate the cGMP-dependent pathway. We have termed these opposing regulatory mechanisms reciprocal control. In all cases, the molecules that are involved appear to be downstream components of the signal transduction pathways, rather than calcium and cGMP themselves. Furthermore, we have found that the calcium/cGMP-dependent pathway has a lower requirement for cGMP than does the cGMP-dependent pathway. The role of these phenomena in the regulation of plant photoresponses is discussed.