Adaptation of Maize to Temperate Climates: Mid-Density Genome-Wide Association Genetics and Diversity Patterns Reveal Key Genomic Regions, with a Major Contribution of the Vgt2 (ZCN8) Locus

Abstract

The migration of maize from tropical to temperate climates was accompanied by a dramatic evolution in flowering time. To gain insight into the genetic architecture of this adaptive trait, we conducted a 50K SNP-based genome-wide association and diversity investigation on a panel of tropical and temperate American and European representatives. Eighteen genomic regions were associated with flowering time. The number of early alleles cumulated along these regions was highly correlated with flowering time. Polymorphism in the vicinity of the ZCN8 gene, which is the closest maize homologue to Arabidopsis major flowering time (FT) gene, had the strongest effect. This polymorphism is in the vicinity of the causal factor of Vgt2 QTL. Diversity was lower, whereas differentiation and LD were higher for associated loci compared to the rest of the genome, which is consistent with selection acting on flowering time during maize migration. Selection tests also revealed supplementary loci that were highly differentiated among groups and not associated with flowering time in our panel, whereas they were in other linkage-based studies. This suggests that allele fixation led to a lack of statistical power when structure and relatedness were taken into account in a linear mixed model. Complementary designs and analysis methods are necessary to unravel the architecture of complex traits. Based on linkage disequilibrium (LD) estimates corrected for population structure, we concluded that the number of SNPs genotyped should be at least doubled to capture all QTLs contributing to the genetic architecture of polygenic traits in this panel. These results show that maize flowering time is controlled by numerous QTLs of small additive effect and that strong polygenic selection occurred under cool climatic conditions. They should contribute to more efficient genomic predictions of flowering time and facilitate the dissemination of diverse maize genetic resources under a wide range of environments.

Association mapping for phenology and plant architecture in maize shows higher power for developmental traits compared with growth influenced traits

“…It displayed marked variation in flowering time, from extremely early materials to photoperiod sensitive tropical materials. These features have contributed to the discovery of interesting associations based on candidate gene approaches such as Vgt1 (Ducrocq et al, 2008), ZmCCT (Ducrocq et al, 2009) and Opaque2 (Manicacci et al, 2009), with a first genome-wide scan in this panel revealing ZCN8 as a major gene corresponding to Vgt2, 8Mb from Vgt1, as well as other QTLs involved in flowering time (Bouchet et al, 2013). Our study highlighted the high variation in this panel regarding plant architecture and grain yield related traits, and contrasted genetic architectures for these traits.…”

“…They were genotyped for 94 simple sequence repeat (SSR) markers and with the 50K Illumina Golden Gate beadchip leading to 43 224 polymorphic SNPs. Conformity check and heterozygosity rate led to a set of 336 maize inbred lines used for association studies (Bouchet et al, 2013). The structure of this panel was analyzed with STRUCTURE software (Pritchard et al, 2001) using 55 tri-nucleotidic SSRs, leading to 5 main genetic groups (Camus-Kulandaivelu et al, 2006).…”

“…Var(u) = 2KVg, where Vg is the genetic variance and K is a matrix of similarity between lines. In order not to use candidate SNPs for population structure and kinship estimations, we used STRUCTURE vectors calculated with 55 SSRs (Q 55SSRs ) and 10 identity by state kinship matrices calculated with~30 K Panzea (http:// www.panzea.org/) SNPs (Bouchet et al, 2013). To test SNPs located on one chromosome, we used a kinship calculated with SNPs belonging to all chromosomes but that one .…”

“…However, substantial variation remains to be explained and exploited for most traits. QTL mapping experiments revealed that plant total height (PTHT) and flowering time are highly heritable polygenic traits and that their variation is controlled by many unlinked genes, each contributing a small additive effect (Buckler et al, 2009;Romay et al, 2013;Bouchet et al, 2013;Peiffer et al, 2014). Many QTL experiments for inflorescence traits showed that they are less heritable (Brown et al, 2011).…”

“…Association studies on diversity panels are effective for identifying genetic variants associated with phenological and morphological traits in maize (Thornsberry et al, 2001;Flint-Garcia et al, 2005;CamusKulandaivelu et al, 2006;Ducrocq et al, 2008Ducrocq et al, , 2009Durand et al, 2012;Romay et al, 2013;Bouchet et al, 2013). In the current study, 375 lines of maize originating from the tropics, USA and Europe were successfully phenotyped for 24 ecologically and agronomically important traits related to (i) phenology, (ii) plant architecture, (iii) ear and yield components and (iv) tassel architecture.…”