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DArTseq Molecular Markers Associated with the Spiny-Tip Leaf Margin in Pineapple (Ananas comosus L.)

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Abstract

A genome-wide association study (GWAS) and quantitative trait loci (QTL) analysis using two bi-parental (parental cultivars Smooth Cayenne and MD-2) pineapple seedling populations segregating for spiny and spiny-tip leaf margin and 12 wild and pre-Columbian domesticated genotypes were used to identify single nucleotide polymorphism (SNP) and silicoDArT markers associated with the spiny-tip leaf margin phenotype in pineapple. One QTL between the nucleotide positions 14,355,639 and 14,368,806 on linkage group six (LG06) was identified using SNP markers and one QTL between the nucleotide positions 14,330,844 and 14,346,378 using silicoDArT markers. GWAS and QTL analysis methods identified the same most significantly associated SNP and silicoDArT markers. The most significantly associated SNP and silicoDArT markers were positioned at 14,355,639 and 14,341,745 bp respectively, on or very near, a zeaxanthin epoxidase (ZEP) gene, a key gene in the abscisic acid (ABA) pathway. Other associated genes with a high significance by GWAS analysis using at least two algorithms include a detoxification 33-like (DTX) and a resistance gene analog (RGA2-like). It is proposed that a polymorphism in the putative ZEP gene is the main causal variant associated with the spiny-tip leaf margin in ‘Smooth Cayenne’ pineapple and its descendants including ‘MD-2’.

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Abbreviations

ABA:

Abscisic acid

BLAST:

Basic local alignment search tool

CLV:

Clavata

DArT:

Diversity Arrays Technology

DTX:

Detoxification

ECMLM:

Enriched compressed mixed linear model

EMMA:

Efficient mixed model association

ERf:

ERECTA family

FarmCPU:

Fixed and random model circulating probability unification

FPKM:

Fragments per kilobase of transcript per million mapped reads

FTIP:

FT-interacting protein

GA:

Gibberellic acid

GATL:

Galacturonosyltransferase-like

GAUT:

Galacturonosyltransferase

GWAS:

Genome wide association study

KNNi:

k-nearest neighbour imputation

KNOX:

KNOTTED-like homeobox

LD:

Linkage disequilibrium

LG:

Linkage group

LRR:

Leucine-rich repeat

MAF:

Minor allele frequency

MATE:

Multi-drug and toxic extrusion

MLMM:

Multi-locus mixed linear model

MT:

Microtubule

MVP:

Memory-efficient, Visualization-enhanced, and Parallel-accelerated Tool for Genome-Wide Association Study

NBS-LRR:

Nucleotide binding site – Leucine rich repeat

P3D:

Population parameters previously determined

PGD:

Pineapple Genomics Database

QQ plot:

Quantile-Quantile plot

QTL:

Quantitative trait loci

RGA:

Resistance Gene Analog

SAM:

Shoot apical meristem

SK13:

Shaggy-like kinase 13

SNP:

Single nucleotide polymorphism

SUPER:

Settlement of MLM under progressively exclusive relationship

TBCC:

Tubulin binding cofactor

TPR:

Tetratricopeptide repeat-containing

WUS:

Wuschel

ZEP:

Zeaxanthin epoxidase

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Acknowledgements

The author would like to thank D. Innes and K. O’Connor and the reviewers for their helpful comments on the manuscript.

Funding

The project was funded by Horticulture Innovation Australia Pty Ltd. (Hort Innovation) using voluntary contributions from the Department of Agriculture and Fisheries and matched funds from the Australian Government.

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Authors and Affiliations

  1. Queensland Government, Department of Agriculture and Fisheries, Maroochy Research Facility, 47 Mayers Rd Queensland, Nambour, 4560, Australia

    Garth M. Sanewski

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  1. Garth M. Sanewski
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Correspondence to Garth M. Sanewski.

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Communicated by: Yann-Rong Lin

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Electronic Supplementary Material

Fig. S1

Linkage decay curve for LG06. A Loess curve line is shown in pink. The LD decay distance is the point where the X axis corresponds with 50% of the vertical fitted curve maximum as shown. (PNG 1474 kb)

High resolution image (TIFF 44062 kb)

Fig. S2

Linkage haploblocks for LG06 (Haploview 4.2). The pink bar covers the significantly associated loci and up to 300 kb either side of SNP positions (13.6–14.7 Mb). R2 = 1 (black), 0 < r2 < 1 (shades of grey), r2 = 0 (white). (PNG 626 kb)

High resolution image (TIF 12153 kb)

Fig. S3

Haploblocks for the significantly associated region on LG06 (Haploview 4.2). R2 = 1 (black), 0 < r2 < 1 (shades of grey), r2 = 0 (white). Matched, significantly associated SNP markers are surrounded by a coloured frame. (PNG 1327 kb)

High resolution image (TIFF 28695 kb)

Fig. S4

Principal components bi-plot for SNP markers (TASSEL 5). The different coloured symbols indicate the different genotype groups. M × C = ‘MD-2’♀ × ‘Smooth Cayenne’♂; C × M = ‘Smooth Cayenne’♀ × ‘MD-2’♂. (PNG 197 kb)

High resolution image (TIFF 39649 kb)

Figs S5

A and B Scree plots (eigenvalues) for SNPs (A) and silicoDArTs (B). The number of principal components used in the analyses are indicated. (PNG 130 kb)

High resolution image (TIFF 23789 kb)

Table S1

Linkage estimate matrix (r2 and D′) for significant, matched SNPs (Haploview 4.2). D′ values are above the diagonal and r2 below. (DOCX 15 kb)

Table S2

Nucleotide sequences for all significantly associated SNPs (trimmed sequences) using three algorithms in GAPIT. Both the reference and SNP sequences are shown. (DOCX 17 kb)

Table S3

Nucleotide sequences for all significantly associated silicoDArT (trimmed sequences) using three algorithms in GAPIT. (DOCX 13 kb)

Table S4

Predominant allele states for only the most highly significant and matched SNP markers in two seedling populations, the two spiny-tip parent cultivars, MD-2 and Smooth Cayenne and ten other unrelated genotypes. The allele states for SNPs are before imputation of null alleles. The ‘Smooth Cayenne’ genome was used as the reference for markers calls. -Log10P is from ECMLM analysis unless only significant using other algorithms; then it relates to MLMM preferentially. Correct, unambiguous allele states according to the seedling data are coloured similarly (spiny yellow; spiny-tip green). Wild, primitive genotypes are coloured blue in the header and pre-Columbian domesticates are coloured pink except for the two parents which are not coloured. 0 = homozygous reference allele; 1 = homozygous SNP allele; 2 = heterozygous. Redsp = Red Spanish, Roxo = Roxo de Tefe, Parg = Parguazensis, F19 = FRF19, F361 = FRF361, F223 = FRF223 and macro = A. macrodontes. (DOCX 17 kb)

Table S5

Predominant allele states for only the most highly significant and matched silicoDArT markers in two seedling populations, the two spiny-tip parent cultivars, MD-2 and Smooth Cayenne and ten other unrelated genotypes. The ‘Smooth Cayenne’ genome was used as the reference for markers calls. -Log10P is from ECMLM analysis unless only significant using other algorithms; then it relates to MLMM preferentially. Correct, unambiguous allele states according to the seedling data are coloured similarly (spiny yellow; spiny-tip green). Wild, primitive genotypes are coloured blue in the header and pre-Columbian domesticates are coloured pink except for the two parents which are not coloured. 0 = absent; 1 = present. Redsp = Red Spanish, Roxo = Roxo de Tefe, Parg = Parguazensis, F19 = FRF19, F361 = FRF361, F223 = FRF223 and macro = A. macrodontes. (DOCX 14 kb)

Table S6

RNAseq data (FPKM) for genes with a strong positive co-expression with zeaxanthin epoxidase (Aco08515.1) from the Pineapple Genomics Database website of Zhang and Ming (2018) (http://pineapple.angiosperms.org/pineapple/html/index.html) as cited by Xu et al. (2018). Data is a mean of eight samples from cultivar MD-2. Leaf tissues progress from the base to the tip such that S1 = basal white, S2 = white, S3 = white/green, S4 = proximal mid-leaf green, S5-distal mid-leaf green and S6 = tip. Only genes with a positive Pearson correlation of ≥0.8 are shown. (DOCX 26 kb)

Table S7

RNAseq data (FPKM) for genes with a strong negative co-expression with zeaxanthin epoxidase (Aco08515.1) from the Pineapple Genomics Database website of Zhang and Ming (2018) (http://pineapple.angiosperms.org/pineapple/html/index.html) as cited by Xu et al. (2018). Data is a mean of eight samples from cultivar MD-2. Leaf tissues progress from the base to the tip such that S1 = basal white, S2 = white, S3 = white/green, S4 = proximal mid-leaf green, S5-distal mid-leaf green and S6 = tip. Only genes with a negative Pearson correlation of ≤ −0.8 are shown. (DOCX 17 kb)

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Sanewski, G.M. DArTseq Molecular Markers Associated with the Spiny-Tip Leaf Margin in Pineapple (Ananas comosus L.). Tropical Plant Biol. 13, 91–116 (2020). https://doi.org/10.1007/s12042-019-09245-z

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