Preface Free

Plants and algae, like all living organisms, are forced continuously to acclimate their metabolism and physiology to the changing environmental conditions. To this end, a network of complex signalling pathways is employed to transduce various signals either within or among different sub-cellular compartments. In the classical view, these signalling pathways lead from different types of receptors, mostly localized at the plasma membrane, either to cytosolic processes or to the nucleus, ultimately aiming at the initiation of transcriptional responses. However, increasing evidence has accumulated over the past two decades that other organelles are also actively involved in co-ordinating the physiological responses to abiotic and biotic stimuli. To provide an overview of our current knowledge on organellar signalling in algae and higher plants, this special issue of the Journal of Experimental Botany contains 12 reviews and 6 accompanying research papers, which were mainly prepared by members of the EU-funded Marie-Curie Initial Training Network (ITN) ‘COSI’ (chloroplast signals, www.univie.ac.at/cosi). One common theme addressed in all the articles is the question of information exchanged within and among different sub-cellular compartments, including aspects of intra-organellar signalling, such as calcium-dependent regulation (reviewed by Stael et al. on pages 1525–1542) and its cross-talk with protein phosphorylation at the thylakoid membrane (Stael et al., pages 1725–1733). By contrast, cross-talk between chloroplasts and mitochondria in diatoms (Prihoda et al.) or the impact of mitochondrial function in retrograde signalling to the nucleus (Schwarzländer et al.) present important aspects of inter-organellar signalling. Protein phosphorylation is a hallmark of all the signalling pathways, however, our knowledge of organellar protein phosphorylation has been limited to a few well-characterized examples, such as the process of state transition (re-distribution of photosynthetic light-harvesting complexes) as a response to fluctuating light conditions. This issue also provides a summary of the current state of knowledge on chloroplast-localized protein kinases (Bayer et al.).

Light signals affect photosynthetic organisms at various levels: they provide the basis for their autotrophic life style and are thus a vital resource that needs to be sensed correctly. On the other hand too much light can damage the photosynthetic machinery and is thus harmful and triggers appropriate stress responses. The balance between these extremes and the cross-talk with other defence pathways is discussed by Kangasjärvi et al. Furthermore, light initiates key developmental switches and, accordingly, the perception of current light conditions, as well as acclimation to fluctuating light conditions is of fundamental importance and a great variety of signalling mechanisms have been established. One example of how organelles as a whole react to light is the process of chloroplast movement to protect themselves from photodamage under high-light conditions. This is dependent on blue light (as discussed by Banas et al.) and also involves secondary messengers like Ca²⁺ ions or phosphoinositides. Blue light is dominating in the marine environment and, correspondingly, blue-light receptors are the most numerous in marine diatoms, as pointed out by Depauw et al. in their review on the molecular basis of light responses in marine diatoms. The recent progress in genomic resources revealed striking structural and functional differences between photoreceptors from diatoms and higher plants and the important role of diatom-specific proteins of the xanthophyll cycle and the LHCX familiy involved in non-photochemical quenching (NPQ). This directly relates to photosynthetic control mechanisms whereby cellular energy requirements regulate photosynthetic electron transport chain activity in response to environmental and metabolic triggers. Foyer et al. discuss transcriptome re-programming occurring in C₃ and C₄ leaves in response to changing atmospheric carbon dioxide (CO₂) availability and describe a relationship between photorespiration and the expression of genes associated with cyclic electron flow pathways. Similarly, the biosynthesis of these components, which perform the initial reactions of photosynthesis and electron transport is adjusted to environmental conditions as well by several control mechanisms. The post-translational regulation of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria, is reviewed by Czarnecki and Grimm. Chloroplast gene expression is regulated on transcriptional, post-transcriptional, and translational levels, and Stoppel and Meurer discuss how ribonucleases act as key players in the control of plastid gene expression. In the end, however, metabolic adjustments in response to stress (i.e. high salt stress, drought, and extreme temperatures) have to be co-ordinated between the different organelles. The metabolic changes, which occur during these adaptation processes at the sub-cellular level are summarized by Krasensky and Jonak, where it becomes evident that our knowledge in this area is still very limited.

Other aspects of organellar signalling covered in this special issue include a new view on plastoglobules (low density lipid droplets inside the chloroplast) described by Eugeni Piller et al., that emerged after determination of its proteome. So far, they have largely been viewed as passive lipid storage droplets, but now it is clear that they are a central site of prenylquinone metabolism and contain a number of metabolic enzymes and regulatory factors such as the ABC kinases (see Bayer et al.). Their size and content is regulated by light and, during development, their function correlates with thylakoid membrane structure and photosynthetic function. Biogenesis of the thylakoid membrane, as the scaffold of the photosynthetic machinery is the focus of two further articles. The transport of proteins across the chloroplast thylakoid membrane is a complex issue as outlined by Albiniak et al. It now appears that some proteins are threaded across the membrane in an unfolded state, while others are transported by a completely different mechanism in a fully folded state. There are interesting indications for control mechanisms in the latter case, suggesting the involvement of a signalling or quality control system.

The relationship between stress and thylakoid membrane synthesis is also part of the article by Vothknecht et al. discussing the role of the vesicle-inducing protein in plastids 1 (Vipp1), which is an essential component in thylakoid membrane formation in chloroplasts and cyanobacteria. Vipp1 evolved from the bacterial stress response protein, pspA, but despite of research over more than a decade, the exact function of Vipp1 in thylakoid biogenesis remains an enigma.