Influence of plastids on light signalling and development

In addition to their contribution to metabolism, chloroplasts emit signals that influence the expression of nuclear genes that contribute to numerous plastidic and extraplastidic processes. Plastid-to-nucleus signalling optimizes chloroplast function, regulates growth and development, and affects responses to environmental cues. An incomplete list of plastid signals is available and particular plastid-to-nucleus signalling mechanisms are partially understood. The plastid-to-nucleus signalling that depends on the GENOMES UNCOUPLED (GUN) genes couples the expression of nuclear genes to the functional state of the chloroplast. Analyses of gun mutants provided insight into the mechanisms and biological functions of plastid-to-nucleus signalling. GUN genes contribute to chloroplast biogenesis, the circadian rhythm, stress tolerance, light signalling and development. Some have criticized the gun mutant screen for employing inhibitors of chloroplast biogenesis and suggested that gun alleles do not disrupt significant plastid-to-nucleus signalling mechanisms. Here, I briefly review GUN-dependent plastid-to-nucleus signalling, explain the flaws in the major criticisms of the gun mutant screen and review the influence of plastids on light signalling and development.     

四吡咯代谢中间产物在植物质体向细胞核信号转导中的作用

在植物细胞内,除了顺向的信号转导通路,即核基因控制着质体基因的转录和翻译之外,还存在着逆向的信号转导通路,即质体的代谢状况作为一种信号去调控核基因的表达。过去对这条逆向的信号转导通路,亦称质体因子,研究得非常少。近几年来,随着对基因组解偶联突变体的深入研究,人们对这条通路的认识大大加深了。现着重介绍质体中的四吡咯代谢中间产物参与信号的产生,以及质体向细胞质搬运这些中间产物启动了对编码质体蛋白的核基因的表达调控。     

Photosynthetic redox control of nuclear gene expression

Chloroplasts contain 3000-4000 different proteins but only a small subset of them is encoded in the plastid genome while the majority is encoded in the nucleus. Expression of these genes therefore requires a high degree of co-ordination between nucleus and chloroplast. This is achieved by a bilateral information exchange between both compartments including nucleus-to-plastid (anterograde) and plastid-to-nucleus (retrograde) signals. The latter represent a functional feedback control which couples the expression of nuclear encoded plastid proteins to the actual functional state of the organelle. The efficiency of photosynthesis is a very important parameter in this context since it is influenced by many environmental conditions and therefore represents a sensor for the residing environment. Components of the photosynthetic electron transport chain exhibit significant changes in their reduction/oxidation (redox) state depending on the photosynthetic electron flow and therefore serve as signalling parameters which report environmental influences on photosynthesis. Such redox signals control chloroplast and nuclear gene expression events and play an important role in the co-ordination of both genetic compartments. It is discussed here which photosynthetic parameters are known to control nuclear gene expression, how these signals are transduced toward the nucleus, and how they interact with other plastid retrograde signals and cytosolic light perception systems.     

Light intensity-dependent retrograde signalling in higher plants

Plants are able to acclimate to highly fluctuating light environment and evolved a short- and long-term light acclimatory responses, that are dependent on chloroplasts retrograde signalling. In this review we summarise recent evidences suggesting that the chloroplasts act as key sensors of light intensity changes in a wide range (low, high and excess light conditions) as well as sensors of darkness. They also participate in transduction and synchronisation of systemic retrograde signalling in response to differential light exposure of distinct leaves. Regulation of intra- and inter-cellular chloroplast retrograde signalling is dependent on the developmental and functional stage of the plastids. Therefore, it is discussed in following subsections: firstly, chloroplast biogenic control of nuclear genes, for example, signals related to photosystems and pigment biogenesis during early plastid development; secondly, signals in the mature chloroplast induced by changes in photosynthetic electron transport, reactive oxygen species, hormones and metabolite biosynthesis; thirdly, chloroplast signalling during leaf senescence. Moreover, with a help of meta-analysis of multiple microarray experiments, we showed that the expression of the same set of genes is regulated specifically in particular types of signals and types of light conditions. Furthermore, we also highlight the alternative scenarios of the chloroplast retrograde signals transduction and coordination linked to the role of photo-electrochemical signalling.     

PAPP5 Is Involved in the Tetrapyrrole Mediated Plastid Signalling during Chloroplast Development

The initiation of chloroplast development in the light is dependent on nuclear encoded components. The nuclear genes encoding key components in the photosynthetic machinery are regulated by signals originating in the plastids. These plastid signals play an essential role in the regulation of photosynthesis associated nuclear genes (PhANGs) when proplastids develop into chloroplasts. One of the plastid signals is linked to the tetrapyrrole biosynthesis and accumulation of the intermediates the Mg-ProtoIX and its methyl ester Mg-ProtoIX-ME. Phytochrome-Associated Protein Phosphatase 5 (PAPP5) was isolated in a previous study as a putative Mg-ProtoIX interacting protein. In order to elucidate if there is a biological link between PAPP5 and the tetrapyrrole mediated signal we generated double mutants between the Arabidopsis papp5 and the crd mutants. The crd mutant over-accumulates Mg-ProtoIX and Mg-ProtoIX-ME and the tetrapyrrole accumulation triggers retrograde signalling. The crd mutant exhibits repression of PhANG expression, altered chloroplast morphology and a pale phenotype. However, in the papp5crd double mutant, the crd phenotype is restored and papp5crd accumulated wild type levels of chlorophyll, developed proper chloroplasts and showed normal induction of PhANG expression in response to light. Tetrapyrrole feeding experiments showed that PAPP5 is required to respond correctly to accumulation of tetrapyrroles in the cell and that PAPP5 is most likely a component in the plastid signalling pathway down stream of the tetrapyrrole Mg-ProtoIX/Mg-ProtoIX-ME. Inhibition of phosphatase activity phenocopied the papp5crd phenotype in the crd single mutant demonstrating that PAPP5 phosphatase activity is essential to mediate the retrograde signal and to suppress PhANG expression in the crd mutant. Thus, our results suggest that PAPP5 receives an inbalance in the tetrapyrrole biosynthesis through the accumulation of Mg-ProtoIX and acts as a negative regulator of PhANG expression during chloroplast biogenesis and development.     

The discovery of plastid-to-nucleus retrograde signaling—a personal perspective

DNA and machinery for gene expression have been discovered in chloroplasts during the 1960s. It was soon evident that the chloroplast genome is relatively small, that most genes for chloroplast-localized proteins reside in the nucleus and that chloroplast membranes, ribosomes, and protein complexes are composed of proteins encoded in both the chloroplast and the nuclear genome. This situation has made the existence of mechanisms highly probable that coordinate the gene expression in plastids and nucleus. In the 1970s, the first evidence for plastid signals controlling nuclear gene expression was provided by studies on plastid ribosome deficient mutants with reduced amounts and/or activities of nuclear-encoded chloroplast proteins including the small subunit of Rubisco, ferredoxin NADP+ reductase, and enzymes of the Calvin cycle. This review describes first models of plastid-to-nucleus signaling and their discovery. Today, many plastid signals are known. They do not only balance gene expression in chloroplasts and nucleus during developmental processes but are also generated in response to environmental changes sensed by the organelles.     

Expression of the Arabidopsis Gene Akr Coincides with Chloroplast Development

Reduced expression of a nuclear gene of Arabidopsis thaliana, Akr, results in the formation of chlorotic plants due to a block in the proplastid-to-chloroplast development pathway (H. Zhang, D.C. Scheirer, W. Fowle, H.M. Goodman [1992] Plant Cell 4: 1575-1588). In an effort to discern the function of the Akr gene product in chloroplast development, transgenic plants containing an Akr::[beta]-glucuronidase gene fusion were constructed to monitor the spatial and temporal patterns of Akr expression. Akr is expressed only in chloroplast-containing tissues and maximal expression occurs during the seedling stage, coincident with chloroplast development. This result is consistent with the hypothesis that Akr is required at an early stage of chloroplast development. The effects of an AKR deficiency on the expression of nuclear and plastid genes required for photosynthetic activity were also examined. Within chloroplast-deficient leaves of plants in which Akr expression is limited by the presence of Akr antisense transgenes or truncated Akr sense transgenes, mRNAs for the nuclear genes Cab2, Cab4, RbcS, and GapA are present at wild-type levels; similarly, levels of mRNAs for the plastid genes rbcL and psbA are not affected by the AKR deficiency. Thus, although expression of these photosynthetic genes is tightly coordinated with the development and maintenance of chloroplasts in wild-type plants, their expression is unaffected in AKR-deficient chlorotic leaves. Therefore, we propose that Akr functions in a pathway different from the one controlling the expression and regulation of the photosynthetic genes during chloroplast development, and at a specific developmental stage after the putative plastid factor is made.     

Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis

Plastid signals are among the most potent regulators of genes that encode proteins active in photosynthesis. Plastid signals help coordinate the expression of the nuclear and chloroplast genomes and the expression of genes with the functional state of the chloroplast. Here, we report the isolation of new cryptochrome1 (cry1) alleles from a screen for Arabidopsis thaliana genomes uncoupled mutants, which have defects in plastid-to-nucleus signaling. We also report genetic experiments showing that a previously unidentified plastid signal converts multiple light signaling pathways that perceive distinct qualities of light from positive to negative regulators of some but not all photosynthesis-associated nuclear genes (PhANGs) and change the fluence rate response of PhANGs. At least part of this remodeling of light signaling networks involves converting HY5, a positive regulator of PhANGs, into a negative regulator of PhANGs. We also observed that mutants with defects in both plastid-to-nucleus and cry1 signaling exhibited severe chlorophyll deficiencies. These data show that the remodeling of light signaling networks by plastid signals is a mechanism that plants use to integrate signals describing the functional and developmental state of plastids with signals describing particular light environments when regulating PhANG expression and performing chloroplast biogenesis.