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Genome-wide association mapping reveals loci for shelf life and developmental rate of lettuce

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Two major QTL, one for shelf life that corresponds to qSL4 and one, qDEV7, for developmental rate, were identified. Associated markers will be useful in breeding for improved fresh-cut lettuce.

Abstract

Fresh-cut lettuce in packaged salad can have short shelf life, and visible deterioration may start within a week after processing. Yield and developmental rate are an important aspect of lettuce production. Genetic diversity and genome-wide association studies (GWAS) were performed on 493 accessions with the genotypic data of 4615 high-quality single nucleotide polymorphism markers. Population structure (Q), principal component (PC), and phylogenetic analyses displayed genetic relationships associated with lettuce types and geographic distribution. Data for shelf life, yield, developmental rate, and their stability indices were used for statistical analysis, and GWAS was performed by general and mixed linear models. The genetic relationship among the individuals was incorporated into the models using kinship matrix, PC, and Q. Broad-sense heritability (H2) across environments was 0.43 for shelf life, 0.36 for yield, and 0.60 for developmental rate. There was a negative correlation between yield and developmental rate. Significant marker–trait association (SMTA) was detected for shelf life on chromosome 4. The most significant quantitative trait locus (QTL,  qSL4, P = 2.23E−17) explained 24% of the total phenotypic variation (R2). The major QTL for developmental rate was detected on chromosome 7 (qDEV7, P = 2.43E−16, R2 = 17%), while additional QTLs with smaller effect were found in all chromosomes. No SMTA was detected for yield. The study identified lettuce accessions with extended and stable shelf life, stable yield, and desirable developmental rate. Molecular markers closely linked to traits can be applied for selection of preferable genotypes and for identification of genes associated with these traits.

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Acknowledgements

The authors would like to thank Jose Orozco, Rebecca Zhao, Bertha Scholler, Mario Estrada, Leah Rosental, Neil Adhikari, Bullo Erena Mamo, Emi Kuroiwa, Alicia Scholler, Phi Diep, Adrian Maldonado, Claire Richardson, Selena Pereda, Gabriel Ramos, Marc Jacquez, Dorelle Rawlings, Lorraine Landeros, Rosa Marchebout, and Denise Soto for assistance in various phases of this research. This research was supported by the Specialty Crop Block Grant Program of the U.S. Department of Agriculture’s (USDA) Agricultural Marketing Service (AMS) through the California Department of Food and Agriculture (SCB15015) and partly also by funding from the California Leafy Greens Research Board and by Oak Ridge Institute for Science and Education (ORISE) Research Participation Program. The mentioning of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.

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Authors and Affiliations

  1. Crop Improvement and Protection Research Unit, U.S. Department of Agriculture, Agricultural Research Service, 1636 E. Alisal Street, Salinas, CA, 93905, USA

    Jinita Sthapit Kandel, Beiquan Mou & Ivan Simko

  2. The Genome Center and Department of Plant Sciences, University of California, Davis, CA, 95616, USA

    Hui Peng

  3. Forage Seed and Cereal Research Unit, U.S. Department of Agriculture, Agricultural Research Service, 3450 SW Campus Way, Corvallis, OR, 97331, USA

    Ryan J. Hayes

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  1. Jinita Sthapit Kandel
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  4. Beiquan Mou
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  5. Ivan Simko
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Contributions

JSK planned and performed experiments, collected and analyzed data, and drafted the manuscript. HP contributed to performing of experiments, data collection, and analyses. RJH, BM, and IS conceived the project, obtained funding, and supervised the experiments. IS contributed to planning of experiments and data interpretation. All authors edited and approved the final manuscript.

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Correspondence to Jinita Sthapit Kandel or Ivan Simko.

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Communicated by Albrecht E. Melchinger.

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Supplementary Fig. 1

Distribution of 897 single nucleotide polymorphism markers (SNPs) across lettuce chromosomes (TIFF 1872 kb)

Supplementary Fig. 2

Graph of delta K (ΔK) values from the STRUCTURE analysis for best K estimation for the lettuce population of 493 accessions using 897 SNPs (PDF 15 kb)

Supplementary Fig. 3

A neighbor-joining phylogenetic tree (created in TASSEL) of 493 lettuce accessions using 4615 SNPs (PDF 88 kb)

Supplementary Fig. 4

Genome-wide distribution of LD (linkage disequilibrium) r2 across lettuce chromosomes 1 to 9. X-axis shows the position of the SNP markers in each chromosome based on the lettuce genome sequence of L. sativa cv. Salinas V8 (http://lgr.genomecenter.ucdavis.edu). Intensity of LD is as shown in the colored scale of r2 (PDF 1816 kb)

Supplementary Fig. 5

The pattern of AUDePS (Area Under the Deterioration Progress Stairs) for accessions with good and poor shelf life (from Mar17 experiment). Weeks after processing is shown in x-axis with LS means of AUDePS for each accession in y-axis. Salinas, PI 601810, SalVal-107, Floricos, and SalVal-298 were accessions exhibiting good shelf life. PI 491219, Density, PI 491009, PI 491087, and PI 491023 showed poor shelf life (TIFF 649 kb)

Supplementary Fig. 6

Barplots showing allele effects of SNP (single nucleotide polymorphism) markers with significant MTA (marker–trait association) for shelf life in lettuce. Mean AUDePS for alleles were compared for the markers in each experiment (Spe16, Mar17, Spe17, and Gon19). Star above the bar indicates significant difference among the means (TIFF 1400 kb)

Supplementary Fig. 7

Manhattan plots and QQ plots from genome-wide association studies for stability of shelf life, yield, and developmental rate in 493 lettuce accessions using 4615 SNPs in four experiments. a. Shelf life stability– the environmental variance (S2) (Annicchiarico 2002), b. Shelf life stability– the b coefficient (Finlay and Wilkinson 1963), c. Shelf life stability– the Ecovalence W2 (Wricke 1962), d. Shelf life stability – the absolute values of b coefficient, e. Yield stability– the environmental variance (S2) (Annicchiarico 2002), f. Yield stability– the b coefficient (Finlay and Wilkinson 1963), g. Yield stability– the Ecovalence W2 (Wricke 1962), h. Yield stability – the absolute values of b coefficient, i. Developmental rate stability– the environmental variance (S2) (Annicchiarico 2002), j. Developmental rate stability– the b coefficient (Finlay and Wilkinson 1963), k. Developmental rate stability– the Ecovalence W2 (Wricke 1962), l. Developmental rate stability – the absolute values of b coefficient (TIFF 5994 kb)

Supplementary Fig. 8

Manhattan plots and QQ plots from genome-wide association studies for yield (lettuce head fresh weight) in 493 lettuce accessions using 4615 SNPs in three experiments. a. Yield in Marina 2017 (Mar17), b. Yield in Salinas 2017 (Spe17), c. Yield in Gonzales 2017 (Gon17), d. Yield from data across all environments (LS means from three experiments) (TIFF 1852 kb)

Supplementary Fig. 9

Manhattan plots and QQ plots from genome-wide association studies for shelf life from 1 to 5 weeks after salad processing (TIFF 1743 kb)

Supplementary Table 1

List of lettuce accessions used in genome-wide association studies of shelf life and yield (PDF 861 kb)

Supplementary Table 2

Evaluation of different mixed linear models for genome-wide association studies using Mean Square Difference (MSD) for the models for each trait (DOCX 18 kb)

Supplementary Table 3

Pearson correlation coefficients for shelf life and shelf life stability indices in 493 lettuce accessions (DOCX 15 kb)

Supplementary Table 4

Pearson correlation coefficients for yield (head fresh weight) and yield stability indices in 493 lettuce accessions (DOCX 15 kb)

Supplementary Table 5

Pearson correlation coefficients for developmental rate and its stability indices in 493 lettuce accessions (DOCX 15 kb)

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Sthapit Kandel, J., Peng, H., Hayes, R.J. et al. Genome-wide association mapping reveals loci for shelf life and developmental rate of lettuce. Theor Appl Genet 133, 1947–1966 (2020). https://doi.org/10.1007/s00122-020-03568-2

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