Salt tolerance evolves more frequently in C4 grass lineages

Journal of Evolutionary Biology

Volumn 27, Issue 3, 2014, Pages 653-659

  Bromham, L ^a   Bennett, T H ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Comparative; Evolution; Halophyte; PACMAD; Phylogeny; Poaceae; Salinity; Trait lability

Indexed keywords

SODIUM CHLORIDE;

ADAPTATION; CLASSIFICATION; PHOTOSYNTHESIS; PHYLOGENY; PHYSIOLOGY; POACEAE;

ADAPTATION, PHYSIOLOGICAL; PHOTOSYNTHESIS; PHYLOGENY; POACEAE; SODIUM CHLORIDE;

EID: 84894230201     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12320     Document Type: Article

References (42)

1. Aronson, J.A. 1989. HALOPH: A Data Base of Salt Tolerant Plants of the World. Office of Arid Land Studies, University of Arizona, Tucson, Arizona.
2. Bennett, T.H., Flowers, T.J. & Bromham, L. 2013. Repeated evolution of salt-tolerance in grasses. Biol. Lett. 9: 20130029.
3. Bouchenak-Khelladi, Y., Verboom, G.A., Savolainen, V. & Hodkinson, T.R. 2010. Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical space and geological time. Biol. J. Linn. Soc. 162: 543-557.
4. Brownell, P. & Crossland, C. 1972. The requirement for sodium as a micronutrient by species having the C4 dicarboxylic photosynthetic pathway. Plant Physiol. 49: 794-797.
5. von Caemmerer, S., Quick, W.P. & Furbank, R.T. 2012. The development of C4 rice: current progress and future challenges. Science 336: 1671-1672.
6. Christin, P.A., Salamin, N., Kellogg, E.A., Vicentini, A. & Besnard, G. 2009. Integrating phylogeny into studies of C4 variation in the Grasses. Plant Physiol. 149: 82.
7. Christin, P.-A., Osborne, C.P., Chatelet, D.S., Columbus, J.T., Besnard, G., Hodkinson, T.R. et al. 2013. Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proc. Natl. Acad. Sci. 110: 1381-1386.
8. Dajic, Z. 2006. Salt stress. In: Physiology and Molecular Biology of Stress Tolerance in Plants (K.V. Madhava Rao, A.S. Raghavendra, K. Janardhan Reddy, eds), pp. 41-99. Springer, Dordrecht, the Netherlands.
9. Des Marais, D.L. & Juenger, T.E. 2010. Pleiotropy, plasticity, and the evolution of plant abiotic stress tolerance. Ann. N. Y. Acad. Sci. 1206: 56-79.
10. Eallonardo, A.S., Leopold, D.J., Fridley, J.D. & Stella, J.C. 2013. Salinity tolerance and the decoupling of resource axis plant traits. J. Veg. Sci. 24: 365-374.
11. Edwards, E.J. & Donoghue, M.J. 2013. Is it easy to move and easy to evolve? Evolutionary accessibility and adaptation J. Exp. Bot. 64: 4047-4052.
12. Edwards, E.J. & Smith, S.A. 2010. Phylogenetic analyses reveal the shady history of C4 grasses. Proc. Natl. Acad. Sci. USA 107: 2532-2537.
13. Edwards, E.J. & Still, C.J. 2008. Climate, phylogeny and the ecological distribution of C4 grasses. Ecol. Lett. 11: 266-276.
14. Edwards, E.J., Still, C.J. & Donoghue, M.J. 2007. The relevance of phylogeny to studies of global change. Trends Ecol. Evol. 22: 243-249.
15. Flowers, T.J. 2004. Improving crop salt tolerance. J. Exp. Bot. 55: 307-319.
16. Flowers, T.J. & Flowers, S.A. 2005. Why does salinity pose such a difficult problem for plant breeders? Agric. Water Manag. 78: 15-24.
17. Flowers, T. & Yeo, A. 1995. Breeding for salinity resistance in crop plants: where next? Funct. Plant Biol. 22: 875-884.
18. Flowers, T.J., Galal, H.K. & Bromham, L. 2010. Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct. Plant Biol. 37: 604-612.
19. Furumoto, T., Yamaguchi, T., Ohshima-Ichie, Y., Nakamura, M., Tsuchida-Iwata, Y., Shimamura, M. et al. 2011. A plastidial sodium-dependent pyruvate transporter. Nature 476: 472-475.
20. Glenn, E.P., Brown, J.J. & Blumwald, E. 1999. Salt tolerance and crop potential of halophytes. Crit. Rev. Plant Sci. 18: 227-255.
21. Grass Phylogeny Working Group II 2012. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol. 193: 304-312.
22. Hibberd, J., Sheehy, J. & Langdale, J. 2008. Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Curr. Opin. Plant Biol. 11: 228.
23. Kadereit, G., Ackerly, D. & Pirie, M.D. 2012. A broader model for C4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.). Proc. Roy. Soc. Lond. B 279: 3304-3311.
24. Kronzucker, H.J., Coskun, D., Schulze, L.M., Wong, J.R. & Britto, D.T. 2013. Sodium as nutrient and toxicant. Plant Soil 369: 1-23.
25. Linder, H.P., Baeza, M., Barker, N.P., Galley, C., Humphreys, A.M., Lloyd, K.M. et al. 2010. A generic classification of the Danthonioideae (Poaceae). Ann. Mo. Bot. Gard. 97: 306-364.
26. Maddison, W.P. & Maddison, D.R. 2006. Mesquite: a modular system for evolutionary analysis. pp., Version 2.72. http://mesquiteproject.org.
27. Munns, R. 2002. Comparative physiology of salt and water stress. Plant, Cell Environ. 25: 239-250.
28. Munns, R. 2011. Plant adaptations to salt and water stress: differences and commonalities. Plant responses to drought and salinity stress: developments in a post-genomic era. Adv. Bot. Res. 57: 1-32.
29. Osborne, C.P. & Freckleton, R.P. 2009. Ecological selection pressures for C4 photosynthesis in the grasses. Proc. Roy. Soc. Lond. B 276: 1753.
30. Pagel, M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. Roy. Soc. Lond. B 255: 37-45.
31. Pau, S., Edwards, E.J. & Still, C.J. 2012. Improving our understanding of environmental controls on the distribution of C3 and C4 grasses. Glob. Change Biol. 19: 184-196.
32. Roy, S.J., Tucker, E.J. & Tester, M. 2011. Genetic analysis of abiotic stress tolerance in crops. Curr. Opin. Plant Biol. 14: 232-239.
33. Rozema, J. & Flowers, T. 2008. Crops for a salinized world. Science 322: 1478-1480.
34. Sage, R. 2001. Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biol. 3: 202-213.
35. Sage, R.F. 2004. The evolution of C4 photosynthesis. New Phytol. 161: 341-370.
36. Sage, R.F. & Monson, R.K. 1999. C4 Plant Biology. Academic Press, San Diego.
37. Sage, R.F. & Zhu, X.-G. 2011. Exploiting the engine of C4 photosynthesis. J. Exp. Bot. 62: 2989-3000.
38. Sage, R.F., Sage, T.L. & Kocacinar, F. 2012. Photorespiration and the evolution of C4 photosynthesis. Annu. Rev. Plant Biol. 63: 19-47.
39. Stromberg, C.A.E. 2011. Evolution of grasses and grassland ecosystems. Annu. Rev. Earth Planet. Sci. 39: 517-544.
40. Subbarao, G., Ito, O., Berry, W. & Wheeler, R. 2003. Sodium, Äîa functional plant nutrient. Crit. Rev. Plant Sci. 22: 391-416.
41. Taylor, S.H., Hulme, S.P., Rees, M., Ripley, B.S., Ian Woodward, F. & Osborne, C.P. 2010. Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment. New Phytol. 185: 780-791.
42. Zhu, X.Ä., Shan, L., Wang, Y. & Quick, W.P. 2010. C4 Rice: an ideal arena for systems biology research. J. Integ. Plant Biol. 52: 762-770.