Journal
GENETICS
Volume 206, Issue 1, Pages 135-150Publisher
GENETICS SOCIETY AMERICA
DOI: 10.1534/genetics.116.198911
Keywords
copy number variation; macro-transposition; maize domestication; transposon rearrangement
Categories
Funding
- National Science Foundation [IOS: 1116561, IOS: 152100]
- United States Department of Agriculture Institute of Food and Agriculture [2011-67003-30215]
- Natural Science Foundation of China (BCT) [91435201]
- NIFA [687293, 2011-67003-30215] Funding Source: Federal RePORTER
- Direct For Biological Sciences
- Division Of Integrative Organismal Systems [1521100] Funding Source: National Science Foundation
- Direct For Biological Sciences
- Div Of Molecular and Cellular Bioscience [1025976] Funding Source: National Science Foundation
- Division Of Integrative Organismal Systems
- Direct For Biological Sciences [1116561] Funding Source: National Science Foundation
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Selection for yellow-and white-grain types has been central to postdomestication improvement of maize. While genetic control of carotenoid biosynthesis in endosperm is attributed primarily to the Yellow1 (Y1) phytoene synthase gene, less is known about the role of the dominant white endosperm factor White Cap (Wc). We show that the Wc locus contains multiple, tandem copies of a Carotenoid cleavage dioxygenase 1 (Ccd1) gene that encodes a carotenoid-degrading enzyme. A survey of 111 maize inbreds and landraces, together with 22 teosinte accessions, reveals that Wc is exclusive to maize, where it is prevalent in white-grain (y1) varieties. Moreover, Ccd1 copy number varies extensively among Wc alleles (from 1 to 23 copies), and confers a proportional range of Ccd1 expression in diverse organs. We propose that this dynamic source of quantitative variation in Ccd1 expression was created in maize shortly after domestication by a two-step, Tam3L transposon-mediated process. First, a chromosome segment containing Ccd1 and several nearby genes duplicated at a position 1.9 Mb proximal to the progenitor Ccd1r locus on chromosome 9. Second, a subsequent interaction of Tam3L transposons at the new locus created a 28-kb tandem duplication, setting up expansion of Ccd1 copy number by unequal crossing over. In this way, transposon-mediated variation in copy number at the Wc locus generated phenotypic variation that provided a foundation for breeding and selection of white-grain color in maize.
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