Energy costs of salinity tolerance in crop plants

The global need for increased food production means that agriculture is moving into regions with lower rainfall and saline soils, which occupy over 6% of the world land area (Munns, 2005). The aim of this workshop was to work towards completing an energy budget for the mechanisms of salinity tolerance in crop plants, as a guide to the most cost-effective breeding strategies for increasing salt tolerance and yield of important crops. The discussions took into account the supply of energy from mitochondria and chloroplasts, energy demands for transport of water, Na+, Cl− and K+, as well as for processes involved in growth and osmotic adjustment. The premise of the workshop was that by undertaking an energy budget of salinity tolerance using our current understanding of transport processes and measurements of fluxes, including respiratory fluxes through the cytochrome vs alternative respiratory pathways, we would test our understanding and/or reveal deficiencies in the measurements (Fig. 1). Such energy budget considerations have indicated how energy savings are achieved in rice coleoptiles under the combined stresses of anoxia and salinity (Kurniasih et al., 2017). Understanding energy costs/benefits of specific components will also provide a better foundation for engineering salt tolerance; for example, is it better to increase the number of transporters expressed or the energy efficiency of transport (Greenway & Munns, 1983)? It is becoming increasingly evident that a detailed knowledge of the role, location and mechanism of proteins that help confer salt tolerance is needed. For example, the rice Na+ transporter OsHKT1;4, which prevents Na+ accumulating in shoots to toxic levels, when constitutively overexpressed reduces leaf Na+ but results in higher root Na+ and reduced salt tolerance (Oda et al., 2018). Two major paradoxes that underlie the need to examine the energetics of salinity tolerance were identified. (1) Within nonhalophyte species, genetic variation in salt tolerance is often associated with lower leaf Na+ concentration, that is, with Na+ exclusion from leaves. This presents a paradox in terms of energy use efficiency because osmotic adjustment using Na+ would seem a cheaper option than using organic solutes, for example c. 30 mol ATP mol−1 hexose is locked up (Munns & Gilliham, 2015). This implies that there are significant costs in nonhalophytes of having high Na+ concentrations in leaves. The costs are presumably for transport and intracellular compartmentation. A poor capacity for vacuolar compartmentation (Bonales-Alatorre et al., 2013) or chloroplast exclusion (Bose et al., 2017) could also be a factor in many nonhalophytes. (2) Previous calculations of the energy cost for root membrane transport of Na+, as well as nutrients required for growth such as NO3−, appear to exceed the energy that is available according to our current understanding of the transport processes (Kurimoto et al., 2004; Malagoli et al., 2008). The way that energy budgets can be determined and the components that were discussed are indicated in Fig. 2. Major conclusions from the workshop were: In conclusion, it was agreed that biophysical modelling of salt and water transport in cells (Foster & Miklavcic, 2015), roots (Foster & Miklavcic, 2017) and leaves, incorporating the known transporters and ion gradients, would greatly facilitate our understanding of the energy costs of salinity tolerance in crop plants. These models would also inform experimentalists of the types of measurements required and standardization of units and the normalization of fluxes. The participants acknowledge the financial assistance from the Australian Research Council Centre of Excellence in Plant Energy Biology (CE140100008), the Australian Research Council Industrial Transformation Hub Legumes for Sustainable Agriculture (IH140100013), and the logistical assistance of Rebecca Vandeleur.