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

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.