Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: September 4, 2008
Publication Date: January 15, 2009
Citation: Liu, J., Magalhaes, J., Shaff, J., Kochian, L.V. 2009. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant Journal. 57(3):389-399. Interpretive Summary: Large areas of land within the U.S. and over 40% of the world’s arable lands are acidic. In these acid soils, aluminum (Al) toxicity is the primary factor limiting crop production via Al-induced inhibition of root growth. The physiological and molecular basis for Al tolerance is still poorly understood. Thus, we need a more complete understanding of the mechanisms underlying Al tolerance if we are going to be able to develop more Al tolerant crop plants for improved cultivation on acid soils. In this paper, we used molecular and physiological methods to study Al tolerance in the model plant species, Arabidopsis. The investigation is a continuation of previous work that showed that a gene called AtALMT1 that is a close relative of a recently identified wheat Al tolerance gene is important for Arabidopsis Al tolerance. Here we also show that a second Al tolerance gene, AtMATE1, functions in concert with AtALMT1 to confer the full range of Al tolerance. AtMATE1 is closely related to a sorghum Al tolerance gene, AltSB, we recently identified. AtMATE1 is a transporter that pumps citric acid out of the root in response to toxic Al, and this citrate binds and detoxifies the Al in the soil, allowing the root to continue growing. This transporter works together with AtALMT1, which pumps another organic acid, malic acid, out of the root in response to Al. This research is providing a deeper understanding of the strategies plants use to tolerate toxic Al on acid soils and will help us in developing more Al tolerant crops for agriculture on acid soils that are widespread both in the US and also in developing countries.
Technical Abstract: Aluminum (Al) activated root malate and citrate exudation plays an important role in Al tolerance in many plant species. Here, we report on the identification and characterization of AtMATE, a homolog of the recently discovered sorghum and barley Al tolerance genes, here shown to encode an Al-activated citrate transporter in Arabidopsis. Together with the previously characterized Al-activated malate transporter, AtALMT1 Hoekenga et al., 2006), this discovery allowed us to examine the relationship between members of the two gene families for which Al tolerance genes have been identified functioning in the same plant species. AtMATE is expressed primarily in roots and is induced by Al. An AtMATE T-DNA knockout exhibits very low AtMATE expression and wild-type Al-activated root citrate exudation is abolished. An AtALMT1 AtMATE double mutant lacks both Al-activated root malate and citrate exudation and exhibits greater Al sensitivity than the single AtALMT1 mutant. Therefore, although AtALMT1 is a major contributor to Arabidopsis Al tolerance, AtMATE also makes a significant although smaller contribution. The expression patterns of AtALMT1 and AtMATE and the profiles of Al-activated root citrate and malate exudation are not affected by the presence or absence of the function of the other gene. In addition, STOP1, a transcription factor previously shown to be necessary for AtALMT1 expression and Al-activated malate exudation, is not required for AtMATE expression and Al-activated citrate exudation. These results suggest that AtALMT1-mediated Al-activated malate exudation and AtMATE-mediated Al-activated citrate exudation evolved and function independently in conferring Arabidopsis Al tolerance.