Genome-wide haplotype-based association analysis of key traits of plant lodging and architecture of maize identifies major determinants for leaf angle: hapLA4

Abstract

Traits related to plant lodging and architecture are important determinants of plant productivity in intensive maize cultivation systems. Motivated by the identification of genomic associations with the leaf angle, plant height (PH), ear height (EH) and the EH/PH ratio, we characterized approximately 7,800 haplotypes from a set of high-quality single nucleotide polymorphisms (SNPs), in an association panel consisting of tropical maize inbred lines. The proportion of the phenotypic variations explained by the individual SNPs varied between 7%, for the SNP S1_285330124 (located on chromosome 9 and associated with the EH/PH ratio), and 22%, for the SNP S1_317085830 (located on chromosome 6 and associated with the leaf angle). A total of 40 haplotype blocks were significantly associated with the traits of interest, explaining up to 29% of the phenotypic variation for the leaf angle, corresponding to the haplotype hapLA4.04, which was stable over two growing seasons. Overall, the associations for PH, EH and the EH/PH ratio were environment-specific, which was confirmed by performing a model comparison analysis using the information criteria of Akaike and Schwarz. In addition, five stable haplotypes (83%) and 15 SNPs (75%) were identified for the leaf angle. Finally, approximately 62% of the associated haplotypes (25/40) did not contain SNPs detected in the association study using individual SNP markers. This result confirms the advantage of haplotype-based genome-wide association studies for examining genomic regions that control the determining traits for architecture and lodging in maize plants.

Fig 1. Distribution of the 183 inbred maize lines in the two sub-populations (field corn and popcorn) using a subgroup of 5000 SNP markers distributed on all chromosomes.

(A) Genetic structure inferred by a Bayesian clustering model using STRUCTURE and a dendrogram obtained using the neighbor joining based on Nei's genetic distances. The proportion of colored segments light gray and dark gray indicates the proportion of the genome extracted from the two sub-groups (field corn and popcorn, respectively). (B) Principal components analysis (PCA) showing the 183 inbred lines spatially distributed in relation to the first two main components. Values in parentheses indicate the percentage of variation explained by each main component.

Fig 2. Linkage disequilibrium (LD) in tropical maize inbred lines.

(A) LD between all pairs of SNP (38K) (r²) and their distance (Mb). (B) Pattern of LD decay in the 10 chromosomes, with chromosomes 7 and 5 having the fastest and slowest decay (lower and upper margin, respectively).

Fig 3. Manhattan plots of the statistical significance of the SNPs associated with the traits leaf angle (LA), ear height (EH), plant height (PH) and EH/PH ratio, evaluated in an association panel of tropical maize during the growing seasons 2014–2015 and 2015–2016.

The -log10 (P-values) of the SNPs were plotted for all chromosomes as a whole. The SNPs significantly associated with the traits are above the threshold line (P-value > 1.0 × 10⁻³).

Fig 4. Manhattan plots of the statistical significance of the haplotypes associated with the traits leaf angle (LA), ear height (EH), plant height (PH) and EH/PH ratio, evaluated in an association panel of tropical maize during the growing seasons 2014–2015 and 2015–2016.

The -log10 (P-values) of the haplotypes were plotted for all chromosomes as a whole. The haplotypes significantly associated with the traits are above the threshold line (P-value > 1.0 × 10⁻³).