Phytochrome signal transduction pathways are regulated by reciprocal control mechanisms.

Abstract

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, cbs is controlled by a cGMP-dependent pathway, cab is controlled by a calcium-dependent pathway, and far 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 cbs 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.

CUE1: A Mesophyll Cell-Specific Positive Regulator of Light-Controlled Gene Expression in Arabidopsis.

“…Using microinjection techniques, Bowler et al (1994aBowler et al ( , 1994b have shown that the CHS gene is regulated by phytochrome via a cyclic GMP-dependent pathway and that the CAB and RBCS genes are regulated by a different downstream pathway that involves calcium and activated calmodulin. These differential effects correlate well with the gene expression pattern of the cue7-7 mutant: both CAB and RBCS gene expression are severely reduced in cue?, whereas CHS expression is normal.…”

“…CA6 and R6CS are positively regulated by light and show tight cell-type specificity, being expressed exclusively in chloroplast-containing cells and at their highest levels during early leaf development (reviewed in Chory and Susek, 1994). Using pharmacological agonists and antagonists that disrupt phytochrome-mediated events, it has been shown recently that phytochrome may act through a signal transduction pathway involving heterotrimeric G proteins and calcium-activated calmodulin to derepress CA6 and RBCSexpression (Bowler et al, 1994a(Bowler et al, , 1994b. Other nuclear genes whose expression is positively regulated by light are not involved in chloroplast functions and are expressed in cells that do not contain chloroplasts.…”

“…The CHS gene is highly expressed in the epidermis very early during leaf development (Schmelzer et al, 1988;Chory and Peto, 1990). The pharmacological studies of Bowler et al (1994aBowler et al ( , 1994b implicate a heterotrimeric G protein and cGMP in mediating phytochrome-regulated CHS gene expression. lnterpreted in the context of the intact seedling, these studies suggest that phytochrome acts through different downstream effectors, which may be specific to the cell type in which light is eliciting a molecular response.…”

A possible tyrosine phosphorylation of phytochrome

“…There have been reports that a mitogenactivated protein Ser/Thr/Tyr kinase (MAPK) is activated in response to plant hormones in Arabidopsis cell cultures [18] and that a raf-like kinase, which is an upstream regulator of MAPKs in mammals, participates in ethylene signal transduction [19]. Furthermore, it has been demonstrated that a tyrosine kinase inhibitor blocks the expression of at least one phytochrome-regulated gene [20]. The activity of RUBISCO may also be regulated by tyrosine phosphorylation [21].…”

Biosíntesis, señalización y modo de acción del óxido nítrico en Arabidopsis thaliana

“…En trabajos iniciales, se describió que la aplicación del donador de NO, nitroprusiato sódico (SNP), promueve la activación de genes de respuesta a luz (Bowler et al, 1994b;Bowler et al, 1994a) a través de la producción de cGMP, un segundo mensajero del NO, que junto al calcio/calmodulina, es indispensable para la señalización por luz dependiente de fitocromos (Bowler et al, 1994a;Bowler et al, 1994b;Neuhaus et al, 1997). El NO podría ser, por tanto, una de las moléculas que descifre la información de la luz después de ser percibida por los fitocromos.…”