A Rare Gene Copy-Number Variant that Contributes to Maize Aluminum Tolerance and Adaptation to Acid Soils

The extensive phenotypic diversity observed in maize arises from remarkably high levels of genetic polymorphism. Large structural variations, such as copy-number (CNV) and presence/absence variation (PAV), comprise a great extent of this genetic diversity. Here we describe how a rare copy-number variant in a major aluminum (Al) tolerance locus contributes to this agronomically important trait. Aluminum toxicity is a major limitation to plant growth on acid soils. In a recombinant inbred line (RIL) mapping population, copy-number variation of the Al tolerance gene ZmMATE1 is the genetic basis for the QTL of largest effect on phenotypic variation. While the Al-tolerant parent carries three copies of ZmMATE1, the sensitive parent carries only one. RILs segregate in a 1:1 ratio for ZmMATE1 copy-number, and individuals with three gene copies are significantly more Al-tolerant than those inheriting a single copy. Greater copy number is also closely associated with high ZmMATE1 expression, which is controlled in cis, as indicated by eQTL mapping. Sequencing of a BAC clone from the Al-tolerant parental maize line revealed that the three identical ZmMATE1 copies are part of a tandem triplication. CNV for ZmMATE1 is rare, as only two additional maize inbred lines carrying the three-copy haplotype were identified; these lines are also Al-tolerant, have high ZmMATE1 expression, and share the same geographic origin. Our findings indicate that greater ZmMATE1 copy-number drives higher ZmMATE1 expression resulting in superior Al tolerance, and suggest a role for structural variation in the broad adaptation of maize to acidic soils in the tropics.