Structure and Origin of the White Cap Locus and Its Role in Evolution of Grain Color in Maize

Abstract

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.

Genome-Wide Association Study and Pathway-Level Analysis of Kernel Color in Maize

“…Another cleavage enzyme, CCD—encoded by one or more copies of ccd1 within the White Cap ( Wc) locus in maize (Tan et al 2017)—was not detected as being associated with natural variation in this study. The Wc locus was created in some maize accessions by a macrotransposon insertion, with subsequent tandem duplications resulting in the amplification of ccd1 copy number in a subset of those accessions, and has been found to impact endosperm color through the degradation of carotenoids by CCD.…”

“…Notably, the Wc locus was likely identified in the previously conducted analysis of visual scores for gradation in orange kernel color in 10 U.S. maize NAM families. While the ccd1 progenitor locus ( Ccd1r ) was not contained in the QTL support interval identified on chromosome 9 (149.54 to 151.48 Mb, AGP v2), the macrotransposon insertion that created Wc was subsequently characterized in Tan et al (2017), and appears to have been included in the interval. This QTL putatively corresponding to Wc was only significant in two of the 10 NAM families analyzed (Chandler et al 2013), suggesting the possibility of rare variation at the Wc locus which may have precluded its identification in the present study.…”

Genome-Wide Analysis of Genetic Variations and the Detection of Rich Variants of NBS-LRR Encoding Genes in Common Wild Rice Lines

“…The high percentage of SV/CNV variant TEs is reported before in mouse genome (Quinlan et al 2010 ). The transposons played a key regulatory role in plant stress response (Negi et al 2016 ), which are responsible for gene expression change and phenotypic differentiations (Singh et al 2014 ; Dhadi et al 2015 ; Tan et al 2017 ). These SV/CNV variant TEs may cause a dramatic genome rearrangement and have a strong influence on gene expression and resistance level of these three materials.…”

An Overview of Duplicated Gene Detection Methods: Why the Duplication Mechanism Has to Be Accounted for in Their Choice

“…In maize, thousands of tandem gene duplicates were identified that correspond to about 10% of the annotated genes [ 34 ]. Some of them may contribute to a phenotypic variation such as the White Cap locus , which provided the possibility to select white-grain color [ 35 ].…”