The convergent evolution of aluminium resistance in plants exploits a convenient currency

Peter R. Ryan; Emmanuel Delhaize

doi:10.1071/FP09261

EVOLUTIONARY REVIEW

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The convergent evolution of aluminium resistance in plants exploits a convenient currency

Peter R. Ryan ^A ^B and Emmanuel Delhaize ^A

+ Author Affiliations

- Author Affiliations

^A CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.

^B Corresponding author. Email: peter.ryan@csiro.au

This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.

Functional Plant Biology 37(4) 275-284 https://doi.org/10.1071/FP09261
Submitted: 30 October 2009 Accepted: 22 January 2010 Published: 26 March 2010

Abstract

Suspicions that soluble aluminium (Al) is detrimental to plant growth were reported more than 100 years ago. The rhizotoxicity of Al³⁺ is now accepted as the major limitation to plant production on acidic soils. Plants differ in their susceptibility to Al³⁺ toxicity and significant variation can occur within species, even in some major crops. The physiology of Al³⁺ resistance in some species has been understood for 15 years but the molecular biology has been elucidated only recently. The first gene controlling Al³⁺ resistance was cloned from wheat (Triticum aestivum L.) in 2004 but others have now been identified in Arabidopsis, barley (Hordeum vulgare L.), rye (Secale cereale L.), sorghum (Sorghum bicolour (L.) Moench) and rice (Oryza sativa L.) with strong additional candidates in wheat and oilseed rape (Brassica napus L.). These genes confer resistance in different ways, but one mechanism occurs in nearly all species examined so far. This mechanism relies on the release of organic anions from roots which bind with the harmful Al³⁺ cations in the apoplast and detoxify them. The genes controlling this response come from at least two distinct families, suggesting that convergent evolution has occurred. We discuss the processes driving this convergence of protein function and offer opinions for why organic anions are central to the mechanisms of resistance in disparate species. We propose that mutations which modify protein expression or their activation by Al³⁺ have played important roles in co-opting different transport proteins from other functions.

Additional keywords: acid soil, aluminum, anion channel, citrate, malate, tolerance, toxicity.

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