Energy costs of salt tolerance in crop plants

Rana Munns^{1

2}, David A Day³, Wieland Fricke⁴, Michelle Watt⁵, Borjana Arsova⁵, Bronwyn J Barkla⁶, Jayakumar Bose⁷, Caitlin S Byrt^{7

8}, Zhong-Hua Chen⁹, Kylie J Foster¹⁰, Matthew Gilliham⁷, Sam W Henderson¹¹, Colin L D Jenkins³, Herbert J Kronzucker¹², Stanley J Miklavcic¹⁰, Darren Plett¹², Stuart J Roy¹³, Sergey Shabala^{14

15}, Megan C Shelden⁷, Kathleen L Soole³, Nicolas L Taylor¹⁶, Mark Tester¹⁷, Stefanie Wege⁷, Lars H Wegner¹⁸, Stephen D Tyerman⁷

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 Juelich, Helmholtz Association, 52425, Juelich, 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 Osmond, SA, 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, Foshan, 528000, 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), Thuwal, 23955-6900, Saudi Arabia.
¹⁸ Karlsruhe Institute of Technology, Institute for Pulsed Power and Microwave Technology (IHM), D-76344, Eggenstein-Leopoldshafen, Germany.

PMID: 31004496
DOI: 10.1111/nph.15864

Free article

Review

Energy costs of salt tolerance in crop plants

Rana Munns et al. New Phytol. 2020 Feb.

Free article

. 2020 Feb;225(3):1072-1090.

doi: 10.1111/nph.15864. Epub 2019 Jul 11.

Authors

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 Juelich, Helmholtz Association, 52425, Juelich, 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 Osmond, SA, 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, Foshan, 528000, 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), Thuwal, 23955-6900, Saudi Arabia.
¹⁸ Karlsruhe Institute of Technology, Institute for Pulsed Power and Microwave Technology (IHM), D-76344, Eggenstein-Leopoldshafen, Germany.

PMID: 31004496
DOI: 10.1111/nph.15864

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.

Keywords: barley and wheat; energy costs; membrane transport; photosynthesis; respiration; root anatomy; salt tolerance; sodium and chloride transport.

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Comment in

The salinity challenge.
Sanders D. Sanders D. New Phytol. 2020 Feb;225(3):1047-1048. doi: 10.1111/nph.16357. New Phytol. 2020. PMID: 31894589 Free PMC article.

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References

1. Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H. 1998. Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytologist 138: 171-190.
1. Alexova R, Nelson CJ, Jacoby RP, Millar AH. 2015. Exposure of barley plants to low Pi leads to rapid changes in root respiration that correlate with specific alterations in amino acid substrates. New Phytologist 206: 696-708.
1. Amthor JS. 2000. The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Annals of Botany 86: 1-20.
1. Amthor JS, Bar-Even A, Hanson AD, Millar AH, Stitt M, Sweetlove LJ, Tyerman SD. 2019. Engineering strategies to boost crop productivity by cutting respiratory carbon loss. Plant Cell 31: 297-314.
1. Asif MA, Schilling RK, Tilbrook J, Brien C, Dowling K, Rabie H, Short L, Trittermann C, Garcia A, Barrett-Lennard EG et al. 2018. Mapping of novel salt tolerance QTL in an Excalibur × Kukri doubled haploid wheat population. Theoretical and Applied Genetics 131: 2179-2196.

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Energy costs of salt tolerance in crop plants

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Energy costs of salt tolerance in crop plants

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