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      Energy costs of salt tolerance in crop plants

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          Abstract

          Agriculture is expanding into regions that are affected by salinity. This review considers the energetic costs of salinity tolerance in crop plants and provides a framework for a quantitative assessment of costs. Different sources of energy, and modifications of root system architecture that would maximize water vs ion uptake are addressed. Energy requirements for transport of salt (NaCl) to leaf vacuoles for osmotic adjustment could be small if there are no substantial leaks back across plasma membrane and tonoplast in root and leaf. The coupling ratio of the H+ -ATPase also is a critical component. One proposed leak, that of Na+ influx across the plasma membrane through certain aquaporin channels, might be coupled to water flow, thus conserving energy. For the tonoplast, control of two types of cation channels is required for energy efficiency. Transporters controlling the Na+ and Cl- concentrations in mitochondria and chloroplasts are largely unknown and could be a major energy cost. The complexity of the system will require a sophisticated modelling approach to identify critical transporters, apoplastic barriers and root structures. This modelling approach will inform experimentation and allow a quantitative assessment of the energy costs of NaCl tolerance to guide breeding and engineering of molecular components.

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          Most cited references140

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          Salinity tolerance of crops - what is the cost?

          Soil salinity reduces crop yield. The extent and severity of salt-affected agricultural land is predicted to worsen as a result of inadequate drainage of irrigated land, rising water tables and global warming. The growth and yield of most plant species are adversely affected by soil salinity, but varied adaptations can allow some crop cultivars to continue to grow and produce a harvestable yield under moderate soil salinity. Significant costs are associated with saline soils: the economic costs to the farming community and the energy costs of plant adaptations. We briefly consider mechanisms of adaptation and highlight recent research examples through a lens of their applicability to improving the energy efficiency of crops under saline field conditions.
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            ROS homeostasis in halophytes in the context of salinity stress tolerance.

            Halophytes are defined as plants that are adapted to live in soils containing high concentrations of salt and benefiting from it, and thus represent an ideal model to understand complex physiological and genetic mechanisms of salinity stress tolerance. It is also known that oxidative stress signalling and reactive oxygen species (ROS) detoxification are both essential components of salinity stress tolerance mechanisms. This paper comprehensively reviews the differences in ROS homeostasis between halophytes and glycophytes in an attempt to answer the questions of whether stress-induced ROS production is similar between halophytes and glycophytes; is the superior salinity tolerance in halophytes attributed to higher antioxidant activity; and is there something special about the specific 'pool' of enzymatic and non-enzymatic antioxidants in halophytes. We argue that truly salt-tolerant species possessing efficient mechanisms for Na(+) exclusion from the cytosol may not require a high level of antioxidant activity, as they simply do not allow excessive ROS production in the first instance. We also suggest that H2O2 'signatures' may operate in plant signalling networks, in addition to well-known cytosolic calcium 'signatures'. According to the suggested concept, the intrinsically higher superoxide dismutase (SOD) levels in halophytes are required for rapid induction of the H2O2 'signature', and to trigger a cascade of adaptive responses (both genetic and physiological), while the role of other enzymatic antioxidants may be in decreasing the basal levels of H2O2, once the signalling has been processed. Finally, we emphasize the importance of non-enzymatic antioxidants as the only effective means to prevent detrimental effects of hydroxyl radicals on cellular structures.
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              Aquaporins in Plants.

              Aquaporins are membrane channels that facilitate the transport of water and small neutral molecules across biological membranes of most living organisms. In plants, aquaporins occur as multiple isoforms reflecting a high diversity of cellular localizations, transport selectivity, and regulation properties. Plant aquaporins are localized in the plasma membrane, endoplasmic reticulum, vacuoles, plastids and, in some species, in membrane compartments interacting with symbiotic organisms. Plant aquaporins can transport various physiological substrates in addition to water. Of particular relevance for plants is the transport of dissolved gases such as carbon dioxide and ammonia or metalloids such as boron and silicon. Structure-function studies are developed to address the molecular and cellular mechanisms of plant aquaporin gating and subcellular trafficking. Phosphorylation plays a central role in these two processes. These mechanisms allow aquaporin regulation in response to signaling intermediates such as cytosolic pH and calcium, and reactive oxygen species. Combined genetic and physiological approaches are now integrating this knowledge, showing that aquaporins play key roles in hydraulic regulation in roots and leaves, during drought but also in response to stimuli as diverse as flooding, nutrient availability, temperature, or light. A general hydraulic control of plant tissue expansion by aquaporins is emerging, and their role in key developmental processes (seed germination, emergence of lateral roots) has been established. Plants with genetically altered aquaporin functions are now tested for their ability to improve plant tolerance to stresses. In conclusion, research on aquaporins delineates ever expanding fields in plant integrative biology thereby establishing their crucial role in plants.
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                Author and article information

                Journal
                New Phytologist
                New Phytol
                Wiley
                0028-646X
                1469-8137
                July 11 2019
                July 11 2019
                Affiliations
                [1 ]Australian Research Council (ARC) Centre of Excellence in Plant Energy Biology, and School of Agriculture and Environment The University of Western Australia Crawley WA 6009 Australia
                [2 ]CSIRO Agriculture and Food Canberra ACT 2601 Australia
                [3 ]College of Science and Engineering Flinders University GPO Box 2100 Adelaide South Australia 5001 Australia
                [4 ]School of Biology and Environmental Sciences University College Dublin (UCD) Dublin, 4 Ireland
                [5 ]Plant Sciences Institute of Bio and Geosciences Forschungszentrum JuelichHelmholtz Association 52425Juelich Germany
                [6 ]Southern Cross Plant Science Southern Cross University Lismore NSW 2481 Australia
                [7 ]Australian Research Council (ARC) Centre of Excellence in Plant Energy Biology School of Agriculture, Food and Wine University of Adelaide Glen OsmondSA 5064 Australia
                [8 ]Research School of Biology Australian National University Canberra ACT 2600 Australia
                [9 ]School of Science and Health Western Sydney University Penrith NSW 2751 Australia
                [10 ]Phenomics and Bioinformatics Research Centre School of Information Technology and Mathematical Sciences University of South Australia Mawson Lakes SA 5095 Australia
                [11 ]Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food Urrbrae SA 5064 Australia
                [12 ]School of Agriculture and Food Faculty of Veterinary and Agricultural Sciences The University of Melbourne Melbourne VIC 3010 Australia
                [13 ]Australian Research Council (ARC) Industrial Transformation Research Hub for Wheat in a Hot and Dry Climate School of Agriculture, Food and Wine University of Adelaide Urrbrae SA 5064 Australia
                [14 ]Tasmanian Institute for Agriculture University of Tasmania Private Bag 54 Hobart Tas. 7001 Australia
                [15 ]International Centre for Environmental Membrane Biology Foshan University Foshan528000 China
                [16 ]Australian Research Council (ARC) Centre of Excellence in Plant Energy Biology School of Molecular Sciences and Institute of Agriculture The University of Western Australia Crawley WA 6009 Australia
                [17 ]Biological and Environmental Sciences & Engineering Division (BESE) King Abdullah University of Science and Technology (KAUST) Thuwal23955‐6900 Saudi Arabia
                [18 ]Karlsruhe Institute of TechnologyInstitute for Pulsed Power and Microwave Technology (IHM) D‐76344Eggenstein‐Leopoldshafen Germany
                Article
                10.1111/nph.15864
                31004496
                27a250e1-9516-4241-8777-3ac4f6ec38a4
                © 2019

                http://doi.wiley.com/10.1002/tdm_license_1.1

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