Unravelling the plant signalling machinery: an update on the cellular and genetic basis of plant signal transduction.

Plant signalling is a set of phenomena that serves the transduction of external and internal signals into physiological responses such as modification of enzyme activity, cytoskeleton structure or gene expression. It operates at the level of cell compartments, whole cells, tissues, organs or even plant communities. To achieve this, plants have evolved a network of signalling proteins including plasma membrane receptors and ion transporters, cascades of kinases and other enzymes as well as several second messengers such as cytosolic calcium (Ca2+), reactive oxygen/nitrogen species (ROS/RNS), cyclic nucleotides (cAMP and cGMP) and others. Overall, these systems recognise and decode environmental signals and co-ordinate ontogeny programs. This paper summarises recent progress in the field of plant signalling, which was a major theme of the 4th International Symposium on Plant Signalling and Behaviour, 2016, in Saint Petersburg, Russia. Several novel hypotheses and concepts were proposed during this meeting. First, the concept of ROS-Ca2+ hubs has found further evidence and acceptance. This concept is based on reciprocal activation of NADPH oxidases by cytosolic Ca2+ on the one hand, and Ca2+-permeable channels that are activated by NADPH-produced ROS. ROS-Ca2+ hubs enhance the intensity and duration of originally weak Ca2+ and ROS signals. Hubs are directly involved in ROS- and Ca2+-mediated physiological reactions, such as stress response, growth, programmed cell death, autophagy and long-distance signalling. Second, recent findings have widened the list of cyclic nucleotide-regulated processes and strengthened the biochemical basis of cyclic nucleotide biochemistry by exploring cyclase activities of new receptors such as the Phytosulfokine Receptor 1, the pathogen peptide 1 receptor (atPepR1), the brassinosteroid BRI1 receptor and the cell wall-associated kinase like 10. cGMP and cAMP signalling has demonstrated strong link to Ca2+ signalling, via cyclic nucleotide-gated Ca2+-permeable ion channels (CNGCs), and to ROS and RNS via their nitrosylated forms. Third, a novel role for cytosolic K+ as a regulator of plant autophagy and programmed cell death has emerged. The cell death-associated proteases and endonucleases were demonstrated to be activated by a decrease of cytosolic K+ via ROS-induced stimulation of the plasma membrane K+ efflux channel GORK. Importantly, the origin of ROS for induction of autophagy and cell death varies in different tissues and comprises several pools, including NADPH oxidases, peroxidases, photosynthetic and respiratory electron-transporting chains and peroxisomal enzymes. The peroxisome pool is the 'latest' addition to established cellular ROS-producing machineries and is dependent on the state and abundance of catalase in this compartment. Finally, new aspects of phytohormone signalling, such as regulation of root hydraulic pressure by abscisic acid and rate of mitosis by cytokinins, as well as localising cytokinin receptors in endoplasmic reticulum, are reported. Other observations suggest that melatonin is a hormone-like substance in plants, because it targets Ca2+, ROS and RNS.