Root-to-shoot signalling: integration of diverse molecules, pathways and functions Sergey Shabala A,E , Rosemary G. White B , Michael A. Djordjevic C , Yong-Ling Ruan D and Ulrike Mathesius C A School of Land and Food, University of Tasmania, Private Bag 54, Hobart, Tas. 7001, Australia. B CSIRO Agriculture, GPO Box 1600, Canberra, ACT 2601, Australia. C Plant Science Division, Research School of Biology, Building 134, Linnaeus Way, The Australian National University, Canberra, ACT 2601, Australia. D School of Environmental and Life Sciences, University of Newcastle, University Drive, Callaghan, NSW 2308, Australia. E Corresponding author. Email: sergey.shabala@utas.edu.au Abstract. Plant adaptive potential is critically dependent upon efficient communication and co-ordination of resource allocation and signalling between above- and below-ground plant parts. Plant roots act as gatekeepers that sense and encode information about soil physical, chemical and biological factors, converting them into a sophisticated network of signals propagated both within the root itself, and also between the root and shoot, to optimise plant performance for a specific set of conditions. In return, plant roots receive and decode reciprocal information coming from the shoot. The communication modes are highly diverse and include a broad range of physical (electric and hydraulic signals, propagating Ca 2+ and ROS waves), chemical (assimilates, hormones, peptides and nutrients), and molecular (proteins and RNA) signals. Further, different signalling systems operate at very different timescales. It remains unclear whether some of these signalling systems operate in a priming mode(s), whereas others deliver more specific information about the nature of the signal, or whether they carry the same ‘weight’. This review summarises the current knowledge of the above signalling mechanisms, and reveals their hierarchy, and highlights the importance of integration of these signalling components, to enable optimal plant functioning in a dynamic environment. Additional keywords: assimilates, calcium waves, development, electric signals, hormones, hydraulic signalling, miRNA, nodulation, nutrients, peptides, proteins, ROS, stress, sugars, systemic response. Received 21 August 2015, accepted 6 October 2015, published online 13 November 2015 Essentiality of the root-to-shoot communication Because higher plants are sessile organisms that cannot move to another habitat they have to constantly adapt their metabolism and development in response to a changing environment (Christmann et al. 2013; Robbins et al. 2014). Equally importantly, they cannot select their neighbours and therefore have to compete with other plants for resources such as water, nutrients and light. All of these processes require very efficient communication and co-ordination of resource allocation and signalling between above- and below-ground plant parts (Ruan et al. 2013). It is estimated that between 25 and 50% of the total carbohydrates produced in the shoot are translocated to the root to maintain its growth, development and resource acquisition (Marschner 1995). In return, roots supply the aboveground parts with water and nutrients. In addition to this, plant roots act as gatekeepers that sense and encode information about soil physical (e.g. density, moisture, temperature, oxygen availability, organic matter), chemical (e.g. nutrient availability, pH, cation exchange capacity, redox potential, LMW organic substances), and biological (e.g. beneficial and detrimental microorganisms, root exudates from neighbouring plants) factors, converting them to a sophisticated network of signals propagated both within the root itself, and also between the root and the shoot to enable an orchestrated regulation of a plethora of mechanisms and metabolic pathways to optimise plant performance for a specific set of conditions. The importance of co-ordinating physiological processes at a whole-plant level has been emphasised in a recent review that highlighted how hierarchical integration of signals and their spatio-temporal dynamics can explain emerging properties on a whole-plant level (Lüttge 2013). These signals are highly diverse in nature and include physical (electric and hydraulic signals, and propagating Ca 2+ and reactive oxygen species (ROS) waves), chemical (assimilates, hormones, peptides and nutrients), and molecular (RNA, proteins) signals. Most of these signals travel through the vasculature (Lucas et al. 2013), and they operate at very different timescales: fast (seconds and CSIRO PUBLISHING Functional Plant Biology, 2016, 43, 87–104 Review http://dx.doi.org/10.1071/FP15252 Journal compilation Ó CSIRO 2016 www.publish.csiro.au/journals/fpb