|MARON, LYZA - Boyce Thompson Institute|
|GUIMAREAS, CLAUDIA - Embrapa|
|MATIAS, KIRST - University Of Florida|
|ALBERT, PATRICE - University Of Missouri|
|BIRCHLER, JAMES - University Of Missouri|
|Buckler, Edward - Ed|
|COLUCCIO, ALISON - Boyce Thompson Institute|
|DANILOVA, TATIANA - University Of Missouri|
|KUDRNA, DAVID - University Of Arizona|
|MAGALHAES, JURANDIR - Embrapa|
|SCHATZ, MICHAEL - Cold Spring Harbor Laboratory|
|WING, ROD - University Of Arizona|
Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/7/2013
Publication Date: 3/11/2013
Publication URL: http://DOI: 10.1073/pnas.1220766110
Citation: Maron, L., Guimareas, C., Matias, K., Albert, P.S., Birchler, J.A., Bradbury, P., Buckler IV, E.S., Coluccio, A.E., Danilova, T.V., Kudrna, D., Magalhaes, J.V., Pineros, M., Schatz, M.C., Wing, R., Kochian, L.V. 2013. Aluminum tolerance is associated with higher MATE1 gene copy-number in maize. Proceedings of the National Academy of Sciences. 110(13):5241-5246.
Interpretive Summary: Over 20 percent of the U.S. land area and approximately 50 percent of the world’s arable lands are acidic (pH - 5). On these acid soils, aluminum (Al) toxicity is the primary factor limiting agricultural productivity, as toxic Al results in damaged and stunted plant root systems, ultimately resulting in a reduction of crop yields. Given that a large proportion of the acid soils are found in the tropics/subtropics regions where many developing countries are located, Al toxicity limits agricultural productivity 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. The release of organic acid from the root apex in response to Al-stress constitutes a widespread Al-tolerance mechanism by which plant roots are able to ameliorate the toxic levels of Al surrounding the growing root. We previously identified a major Al tolerance gene in maize, ZmMATE1, which encodes a root tip citrate efflux transporter. In the current study, we show that the level of expression of this gene is closely correlated with the degree of Al tolerance in a population of maize lines. We go on to show that the high expression of the ZmMATE1 gene in very Al tolerant maize lines is because in those lines, three functional copies of this gene exist next to each other. In Al sensitive lines, there is only one copy of the ZmMATE1 gene in the maize genome. There is considerable recent interest in variation in the number of copies of specific genes, which is being found to be relatively common in different plant species, as well as in humans and other organisms. This is the first report in plants showing this variation in gene copy number underlies an important agronomic trait.
Technical Abstract: Genome structure variation, including copy-number (CNV) and presence/absence variation (PAV), comprise a large extent of maize genetic diversity but their effect on phenotypes remains largely unexplored. Here we describe how copy-number variation in a major aluminum (Al) tolerance locus contributes to this agronomically important trait. In a recombinant inbred line (RIL) mapping population, copy-number variation of the Al tolerance gene multidrug and toxic compound extrusion1 (MATE1) underlies the QTL of largest effect on phenotypic variation. While the Al-tolerant parent carries three copies of MATE1, the sensitive parent carries only one. RILs segregate in a 1:1 ratio for MATE1 copy-number; individuals with three gene copies are significantly more Al-tolerant and show higher MATE1 expression than those inheriting a single copy. Sequencing of a BAC clone from the Al-tolerant parental line revealed that the three MATE1 copies, which are identical, are part of a tandem triplication. CNV for MATE1 is rare, as only two additional maize inbred lines carrying the three-copy haplotype were identified; these lines are also Al-tolerant, have high MATE1 expression, and share the same geographic origin froma region of highly acidic soils. Our findings indicate that greater MATE1 copy-number drives higher MATE1 expression that results in superior Al tolerance, and suggest a role for structural variation in the broad adaptation of maize to acidic soils in the tropics.