Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/3/2010
Publication Date: 5/27/2010
Citation: Maron, L., Guimaraes, C., Pineros, M., Magalhaes, J., Pleiman, J., Mao, C., Kochian, L.V. 2010. Two functionally distinct members of the MATE (multidrug and toxic compound extrusion) family of transporters potentially underlie two major Al tolerance QTL in maize. Plant Journal. 61:728-740. Interpretive Summary: Over 20% of the US land area and approximately 50% of the world’s arable lands are acidic (pH < 5). On these acid soils, aluminum (Al) toxicity is the primary factor limiting crop production as Al is toxic to plant roots, leading to a damaged and stunted root system. As a large proportion of the acid soils are in the tropics/subtropics where many developing countries are located, Al toxicity limits crop production in the very areas where food security is most tenuous. Because of the importance of this problem to agriculture worldwide, there is considerable interest and research effort by researchers at universities, government agencies, and international agriculture organizations in identifying genes that provide tolerance to Al toxicity in order to improve crop Al tolerance via molecular breeding and biotechnology. In this study we leveraged information regarding our recent cloning of one of the first Al tolerance genes in sorghum to identify a similar gene in maize, which is the number one food crop grown on acid soils worldwide. This gene encodes a transport protein that pumps citric acid out of the growing root tip into the soil, where the citric acid molecules bind and detoxify Al ions in the acid soil. This gene is localized to the growing root tip which is the specific region of the plant that is most sensitive to Al toxicity, and exposure of the root to toxic Al ions activates expression of this gene. This discovery provides critically needed information that will lead to the creation of new maize lines with enhanced Al tolerance, which should increase maize yields on acid soils.
Technical Abstract: Crop yields are significantly reduced by aluminum (Al) toxicity on acidic soils, which comprise up to 50% of the world’s arable land. Al-activated release of ligands (such as organic acids) from the roots is a major plant Al tolerance mechanism. In maize, Al-activated root citrate exudation plays an important role in tolerance. However, maize Al tolerance is a complex trait involving multiple genes and physiological mechanisms. Recently, transporters from the MATE family have been shown to mediate Al-activated citrate exudation in a number of plant species. In this paper we describe the cloning and characterization of two MATE family members in maize, ZmMATE1 and ZmMATE2, which co-localize to major Al tolerance QTL and likely underlie two distinct Al tolerance mechanisms. Both proteins localize to the plasma membrane when transformed into Arabidopsis protoplasts, and mediate significant anion efflux when expressed in Xenopus oocytes. ZmMATE1 expression is mostly concentrated in root tissues, is upregulated by Al exposure and is significantly higher in Al-tolerant maize genotypes. In contrast, ZmMATE2 expression is not specifically localized to any particular tissue and does not respond to Al. [14C]citrate efflux experiments in Xenopus oocytes demonstrate that ZmMATE1 is a citrate transporter. Our data suggests that ZmMATE1 is a functional homolog of the Al tolerance genes recently characterized in sorghum, barley and Arabidopsis, and is likely to underlie the largest maize Al tolerance QTL found on chromosome 6. However, ZmMATE2 most likely does not encode a citrate transporter, and could be involved in a novel Al tolerance mechanism.