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. 2013 Apr;64(6):1537-51.
doi: 10.1093/jxb/ert018. Epub 2013 Feb 5.

Association of candidate genes with drought tolerance traits in diverse perennial ryegrass accessions

Xiaoqing Yu  1 , Guihua Bai, Shuwei Liu, Na Luo, Ying Wang, Douglas S Richmond, Paula M Pijut, Scott A Jackson, Jianming Yu, Yiwei Jiang
Affiliations

Association of candidate genes with drought tolerance traits in diverse perennial ryegrass accessions

Xiaoqing Yu et al. J Exp Bot. 2013 Apr.

Abstract

Drought is a major environmental stress limiting growth of perennial grasses in temperate regions. Plant drought tolerance is a complex trait that is controlled by multiple genes. Candidate gene association mapping provides a powerful tool for dissection of complex traits. Candidate gene association mapping of drought tolerance traits was conducted in 192 diverse perennial ryegrass (Lolium perenne L.) accessions from 43 countries. The panel showed significant variations in leaf wilting, leaf water content, canopy and air temperature difference, and chlorophyll fluorescence under well-watered and drought conditions across six environments. Analysis of 109 simple sequence repeat markers revealed five population structures in the mapping panel. A total of 2520 expression-based sequence readings were obtained for a set of candidate genes involved in antioxidant metabolism, dehydration, water movement across membranes, and signal transduction, from which 346 single nucleotide polymorphisms were identified. Significant associations were identified between a putative LpLEA3 encoding late embryogenesis abundant group 3 protein and a putative LpFeSOD encoding iron superoxide dismutase and leaf water content, as well as between a putative LpCyt Cu-ZnSOD encoding cytosolic copper-zinc superoxide dismutase and chlorophyll fluorescence under drought conditions. Four of these identified significantly associated single nucleotide polymorphisms from these three genes were also translated to amino acid substitutions in different genotypes. These results indicate that allelic variation in these genes may affect whole-plant response to drought stress in perennial ryegrass.

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Figures

Fig. 1.
Fig. 1.
Genetic relatedness of 192 perennial ryegrass accessions with 109 simple sequence repeats (SSRs) as analysed by the STRUCTURE program. Numbers on the y-axis indicate the membership coefficient. The colour of the bar indicates the five groups identified through the STRUCTURE program (G1=red, G2=green, G3=blue, G4=yellow, and G5=pink). Accessions with the same colour belong to the same group.
Fig. 2.
Fig. 2.
Linkage disequilibrium (LD) decay in perennial ryegrass. Plots of squared correlations of allele frequencies (r 2) against physical distance between pairs of SNPs in the 13 pooled genes. The LD pattern of individual genes can be found in Supplementary Fig. S5 at JXB online. (This figure is available in colour at JXB online.)
Fig. 3.
Fig. 3.
Phylogenetic tree of the late embryogenesis abundant group 3 protein sequence from plant species. NCBI protein accession numbers were used to indicate homologous proteins except perennial ryegrass (Lolium perenne). Bar=0.1 amino acid substitutions per site. AAA16282.2, wheat (Triticum aestivum); AAM09564.1, rye (Secale cereal); ACJ68104.1, Barley (Hordeum vulgare); BAJ07539.1, Italian ryegrass (Lolium multiflorum); XP_003581642.1, Brachypodium distachyon; AAS49101.1, Arabidopsis thaliana; NP_001053831.1, rice (Oryza sativa); CAK12529.1, Sporobolus stapfianus; NP_001146861.1, maize (Zea mays); and XP_002447073.1, sorghum (Sorghum bicolor).
Fig. 4.
Fig. 4.
Variant alleles and association mapping at LpLEA3. (A) Gene structure and genotypes analysis of LpLEA3: wild type, heterozygous mutation (Hz-M), homozygous mutation (Ho-M), and recombinants one to four (R1–R4) genotypes were identified on the basis of LpLEA3 sequence from 158 perennial ryegrass accessions. The positions of these three significant SNPs were shown using the full-length LpLEA3 gene sequence as reference, with the start codon designated as position zero. The SNP positions at 104, 264, and 312 were located according to the reference mentioned above, whereas 77, 237, and 285 (in parentheses) were SNP positions relative to the SNP calling reference (accession 120 sequence). The proposed wild-type genotype was highlighted in green, Hz-M in red, Ho-M in yellow, and R1–R4 in black, respectively. Values of leaf water content under drought conditions (D-LWC) with the same letter were not significantly different at P < 0.05 for the wild type, Hz-M, and Ho-M. TSS, transcription start site; arrowed band, untranslated region; thick bar, downstream region after the stop codon; blank box, exon; thin line, intron; ATG, start codon; TAA, stop codon; blue shaded area, region sequenced in this study. (B) Leaf water content under drought stress (D-LWC) against its significant associated SNP markers. Values beside dashed blue lines indicate P-values of association mapping results. The wild-type genotype was highlighted in green, Hz-M in red, and Ho-M in yellow, respectively. Values of D-LWC with the same letter were not significantly different at P < 0.05. (C) Amino acid substitutions in LpLEA3 among wild type, Hz-M, and Ho-M. Underlining with 21 asterisks indicate its signal peptide.
Fig. 5.
Fig. 5.
Phylogenetic tree of cytosolic copper-zinc superoxide dismutase sequence from plant species. NCBI protein accession numbers were used to indicate homologous protein except perennial ryegrass (Lolium perenne). Bar=0.1 amino acid substitutions per site. ABF48717.1, populus (Populus suaveolens); NP_001077494.1, Arabidopsis thaliana; NP_001235298.1, soybean (Glycine max); ACI46676.1, cotton (Gossypium arboretum), CAA39444.1, tobacco (Nicotiana plumbaginifolia); AEV43309.1, zoysiagrass (Zoysia japonica); NP_001105704.1, maize (Zea mays); NP_001060564.1, rice (Oryza sativa); ACX94084.1, bamboo (Bambusa oldhamii); XP_003562484.1, Brachypodium distachyon; BAJ94548.1, barley (Hordeum vulgare); and ACO90194.1, wheat (Triticum aestivum).
Fig. 6.
Fig. 6.
Non-synonymous SNPs resulted in amino acid substitutions for putative LpCyt Cu-Zn SOD in perennial ryegrass. WT, wild type; DS, double substitutions. The first amino acid residue substitution from A to E occurred at position 32 (position 40 in reference to Cyt Cu-ZnSOD peptide of other species), which corresponded to an SNP at nucleotide position 287 in reference accession 92; the second amino acid residue substitution from E to V occurred at position 83 (position 91 in reference to Cyt Cu-ZnSOD peptide of other species), which corresponded to SNP at nucleotide position 134 in reference accession 92. This mutation A (E) reversed another mutation from G (A) to C (E) with in the same gene. (This figure is available in colour at JXB online.)
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