GWAS Identifies SNP Markers and Candidate Genes for Off-Flavours and Protein Content in Faba Bean (Vicia faba L.)
Abstract
:1. Introduction
2. Results
2.1. A Large SNP Panel for GWAS
2.2. Reliable NIRS Prediction Models
2.3. Large Phenotypic Variability
2.4. Trait-Specific Genotype-by-Year Interaction (GxY)
2.5. High Heritability (h2) for Oil, Fatty Acids, Protein, and Tannins
2.6. Specific Type-A Additive Genetic Correlations (ρtype-A) Between Traits
2.7. Identification of SNPs via GWAS
2.8. Candidate Genes
3. Discussion
Novel QTLs and Candidate Genes
4. Material and Methods
4.1. Plant Material and Experimental Design
4.2. Phenotyping: NIRS (Near-Infrared Spectroscopy) and Chemical Analysis
4.2.1. NIRS Spectra Acquisition
4.2.2. Sub-Sample Sample Selection (Training Set)
4.2.3. Chemical Analysis of Protein, Oil, and Fatty Acids
4.2.4. Gas Chromatography-Mass Spectrometry (GC-MS) Measurements of Volatile Compounds (VOCs)
4.2.5. Liquid Chromatography-Mass Spectrometry (LC-MS) of Non VOCs
4.2.6. Predictive Models Based on NIRS
4.3. Genetic and Phenotypic Data Analysis
4.3.1. DNA Extraction, Sequencing, and SNP Typing
4.3.2. Genomic Relationship Matrix (G) and Principal Component Analysis (PCA)
4.3.3. Field Trial Analysis: Adjusted Mean, Heritability, Type-B, and Type-A Additive Genetic Correlations
4.3.4. Linkage Disequilibrium Decay
4.3.5. Genome-Wide Association Study (GWAS)
4.3.6. Candidate Gene Identification and Putative SNP Effects
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A. Field Trial Analysis: Adjusted Mean, Heritability, Type-B and Type-A Additive Genetic Correlations
References
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Trait a | Cross-Validation | |
---|---|---|
Tuning Parameter LVs b | rcv c | |
Protein 2021–2022 | 12 | 0.99 |
Oil 2021–2022 | 10 | 0.97 |
C18:1 2021–2022 | 11 | 0.87 |
C18:2 2021–2022 | 11 | 0.82 |
C18:3 2021–2022 | 11 | 0.94 |
Catechin 2021 | 6 | 0.78 |
Catechin 2022 | 5 | 0.80 |
Epicatechin 2021 | 5 | 0.76 |
Epicatechin 2022 | 5 | 0.81 |
Procyanidin B1 2021 | 6 | 0.86 |
Procyanidin B1 2022 | 5 | 0.84 |
Procyanidin B2 2021 | 5 | 0.72 |
Procyanidin B2 2022 | 5 | 0.82 |
2021 | 2022 | ||||||||
---|---|---|---|---|---|---|---|---|---|
Chemical Class | Trait a | Min | Mean | Max | CV% | Min | Mean | Max | CV% |
Oil | Oil | 1.37 | 1.69 | 2.14 | 7.93 | 1.23 | 1.49 | 1.84 | 7.07 |
Protein | Protein | 18.70 | 25.14 | 30.66 | 7.91 | 22.02 | 29.29 | 35.15 | 7.04 |
Fatty acid | C18:1 | 15.74 | 21.17 | 27.11 | 11.19 | 14.81 | 20.05 | 25.12 | 9.23 |
C18:2 | 48.68 | 52.73 | 56.60 | 2.77 | 48.51 | 52.97 | 58.83 | 2.88 | |
C18:3 | 2.50 | 4.79 | 7.37 | 15.15 | 2.57 | 5.20 | 7.40 | 12.60 | |
Tannin | Catechin | 1.04 | 41.93 | 80.17 | 38.28 | 0.28 | 7.22 | 15.51 | 42.20 |
Epicatechin | 0.15 | 37.04 | 70.01 | 39.69 | 1.23 | 11.76 | 21.63 | 37.58 | |
Procyanidin B1 | 1.81 | 77.85 | 121.08 | 33.10 | 0.51 | 16.14 | 31.10 | 37.33 | |
Procyanidin B2 | 0.22 | 90.60 | 224.26 | 32.37 | 1.42 | 32.20 | 60.16 | 37.16 | |
Phenolic acid | p-coumaric acid | 0.05 | 7.16 | 27.45 | 71.03 | 0.01 | 0.06 | 0.17 | 53.00 |
Caffeic acid | 0.04 | 1.46 | 5.58 | 72.98 | 0.02 | 0.56 | 1.97 | 61.30 | |
Ferulic acid | 0.12 | 5.01 | 8.64 | 34.36 | - | - | - | - | |
Flavonoid | Myricetin | 0.01 | 14.98 | 62.09 | 96.12 | 0.06 | 4.92 | 18.84 | 86.01 |
Quercetin | 0.13 | 6.19 | 32.00 | 90.06 | 0.30 | 2.63 | 6.62 | 55.37 | |
Lipid oxidation product | Hexanal | 16.67 | 984.70 | 2797.92 | 62.36 | - | - | - | - |
1-Linoleoyl glycerol | - | - | - | - | 0.01 | 0.19 | 0.62 | 65.84 | |
2-Hydroxyoleic acid (OHOA) | - | - | - | 2.37 | 7.18 | 10.87 | 27.08 | ||
Alkaloid | Convicine | - | - | - | - | 2.31 | 16.67 | 28.42 | 27.90 |
2021 | 2022 | ||
---|---|---|---|
Trait | ρtype-B a | h2 PEV b | h2 PEV |
Oil | 0.74 (0.06) | 0.65 | 0.77 |
C18:1 | 0.81 (0.05) | 0.74 | 0.78 |
C18:2 | 0.73 (0.08) | 0.60 | 0.70 |
C18:3 | 0.87 (0.04) | 0.74 | 0.82 |
Protein | 0.5 (0.12) | 0.45 | 0.70 |
Catechin | 0.64 (0.07) | 0.68 | 0.80 |
Epicatechin | 0.81 (0.04) | 0.72 | 0.87 |
Procyanidin B1 | 0.74 (0.05) | 0.75 | 0.84 |
Procyanidin B2 | 0.55 (0.06) | 0.75 | 0.84 |
p-coumaric acid | 0.34 (0.13) | 0.43 | 0.41 |
Caffeic acid | 0.53 (0.10) | 0.48 | 0.43 |
Ferulic acid | - | 0.07 | - |
Myricetin | 0.44 (0.10) | 0.43 | 0.48 |
Quercetin | 0.82 (0.14) | 0.49 | 0.19 |
Hexanal | - | 0.33 | - |
1-Linoleoyl glycerol | - | - | 0.26 |
2-Hydroxyoleic acid (OHOA) | - | - | 0.39 |
Convicine | - | - | 0.42 |
Compound Class | Trait | Year | SNP ID a | allFreq | p Value | Bonf | Effect | Variance (%) | SNP Location | Protein Impact | Candidate Gene Annotation b |
---|---|---|---|---|---|---|---|---|---|---|---|
Lipid | Oil C18:3 | 2022 | chr1S 1143102257 | 0.93 | 6.77 × 10−6 1.59 × 10−5 | no | −0.09 0.44 | 7.11 4.8 | Intergenic region | Modifier | Cytochrome p450 |
Oil C18:1 | 2022 | chr4 755718730 | 0.91 | 1.27 × 10−9 1.46 × 10−5 | yes | −0.11 −1.18 | 15.11 6 | Synonymous variant | Low | Cytochrome p450 | |
C18:1 | 2022 | chr1L 713263969 | 0.94 | 2.25 × 10−5 | no | −1.31 | 5.38 | Synonymous variant | Low | Tryptophan aminotransferase protein Lipase in LD (~227.7 kbp) | |
C18:3 | 2021/ 2022 | chr1L 1230530421 | 0.94 | 2.46 × 10−5/ 2.02 × 10−5 | no | −0.57/−0.43 | 5.1/4.1 | Missense variant | Moderate | GDT protein 1 chloroplastic | |
C18:3 | 2021/ 2022 | chr3 1234617141 | 0.96 | 3.70 × 10−8/ 2.2 × 10−5 | yes | −0.76/−0.49 | 8.3/4 | Upstream gene variant | Modifier | Ras protein rab | |
C18:3 | 2021/ 2022 | chr5 505151579 | 0.94 | 1.27 × 10−5/ 3.28 × 10−7 | no | 0.55/0.53 | 6.4/7.1 | Missense variant | Moderate | Protein plastid movement impaired Lipid phosphate phosphatase (LPP) in LD (~61.8 kbp) | |
C18:3 | 2021/ 2022 | contig 7845 77914 | 0.96 | 1.23 × 10−6/ 7.65 × 10−6 | no | −0.6/−0.47 | 6/3.98 | Synonymous variant | Low | Unknown | |
C18:3 | 2022 | chr1L 607096754 | 0.94 | 5.57 × 10−6 | no | 0.60 | 4.85 | Intron variant | Modifier | Reticulon protein b21 1-acyl-sn-glycerol−3-phosphate acyltransferase (ATS2) in LD (~188 kbp) | |
C18:3 | 2022 | chr3 353865653 | 0.96 | 6.14 × 10−6 | no | 0.55 | 4.84 | Intron variant | Modifier | 3-oxoacyl-[acyl carrier protein]-synthase (KAS) | |
Lipid- derived | Hexanal | 2021 | chr1L 841732900 | 0.94 | 1.01 × 10−6 | yes | −818 | 21.6 | Missense variant | Moderate | Pentatricopeptide repeat containing protein |
1-Linoleoyl glycerol | 2022 | chr1L 1034384645 | 0.86 | 1.05 × 10−5 | no | −0.12 | 22.77 | Downstream gene variant | Modifier | Phosphopantetheine adenylyltransferase isoform | |
2- Hydroxyoleic acid (OHOA) | 2022 | chr4 1463710346 | 0.78 | 7.78 × 10−6 | no | 1.51 | 19.13 | Missense variant | Moderate | Rab gap tbc domain containing protein | |
Phenolic acid | p-coumaric acid | 2021 | chr2 964372547 | 0.94 | 7.81 × 10−9 | yes | −9.54 | 27.8 | Intron variant | Modifier | Quality protein dual specificity protein phosphatase phs Helix-loop-helix transcription factor (bHLH) 137-LIKE in LD (~450.5 kbp) |
p-coumaric acid | 2022 | chr1S 1040083079 | 0.93 | 1.40 × 10−8 | yes | −0.04 | 27.23 | Missense variant | Moderate | Protein kinase domain containing protein Transcription factor (MYB) in LD (~141.6 kbp) | |
Caffeic acid | 2021 | chr4 6021087 | 0.96 | 2.75 × 10−7 | yes | −2.11 | 28.2 | Downstream gene variant | Modifier | oxygen evolving enhancer protein 3 1 chloroplastic Transcription factor (MYB) in LD (~120 kbp) | |
Caffeic acid | 2022 | chr6 1188716500 | 0.95 | 7.98 × 10−7 | yes | −0.61 | 24.92 | Missense variant | Moderate | Shikimate kinase | |
Flavonoid | Quercetin Myricetin | 2021 | chr4 935741377 | 0.91 | 2.66 × 10−5 1.68 × 10−5 | no | −6.33 −16.5 | 16.7 17.4 | Synonymous variant | Low | Beta amylase |
Tannin | Catechin Epicatechin Procyanidin B1 | 2021/ 2022 | chr2 671378841 | 0.94 | 8.7 × 10−6/ 1.9 × 10−5 5.6 × 10−6/ 5.9 × 10−6 3.8 × 10−6/ 2.6 × 10−5 | no | 14.4/2.5 11.9/3.4 22/4.7 | 8.9/8 10.4/8.5 10.1/7.1 | Missense variant | Moderate | Unknown protein |
Epicatechin | 2021/ 2022 | chr2 826275103 | 0.92 | 5.06 × 10−6/ 1.96 × 10−7 | no | 13.7/3.7 | 13.29/14.9 | Upstream gene variant | Modifier | Auxin responsive protein saur | |
Procyanidin B1 | 2021/ 2022 | chr2 953872991 | 0.89 | 1.22 × 10−8/ 2.75 × 10−5 | no | 21.4/3.5 | 17.9/8.4 | Synonymous variant | Low | Calcium binding mitochondrial carrier protein scamc | |
Procyanidin B1 Procyanidin B2 | 2022 | chr2 953899416 | 0.93 | 3.14 × 10−8 2.59 × 10−5 | no | 4.1 8.5 | 8.15 8.5 | Intron variant | Modifier | Carbonyl reductase [nadph] | |
Catechin Procyanidin B1 Procyanidin B2 | 2022 | chr1L 672262213 | 0.95 | 1.65 × 10−7 1.51 × 10−7 3.6 × 10−7 | yes | 3.1 5.9 11.3 | 10.3 9.7 8.8 | Intron variant | Modifier | Cathepsin | |
Epicatechin | 2022 | chr2 1501542265 | 0.94 | 3.72 × 10−7 | yes | 3.58 | 7.27 | Synonymous variant | Low | Cytochrome p450 | |
Protein | Protein | 2021 | chr5 632641479 | 0.57 | 2.13 × 10−5 | no | −0.87 | 10.7 | Missense variant | Moderate | 50s ribosomal protein l25 Cationic amino acid transporter 4 (CAT4) in LD (~136.8 kbp) |
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Lippolis, A.; Hollebrands, B.; Acierno, V.; de Jong, C.; Pouvreau, L.; Paulo, J.; Gezan, S.A.; Trindade, L.M. GWAS Identifies SNP Markers and Candidate Genes for Off-Flavours and Protein Content in Faba Bean (Vicia faba L.). Plants 2025, 14, 193. https://doi.org/10.3390/plants14020193
Lippolis A, Hollebrands B, Acierno V, de Jong C, Pouvreau L, Paulo J, Gezan SA, Trindade LM. GWAS Identifies SNP Markers and Candidate Genes for Off-Flavours and Protein Content in Faba Bean (Vicia faba L.). Plants. 2025; 14(2):193. https://doi.org/10.3390/plants14020193
Chicago/Turabian StyleLippolis, Antonio, Boudewijn Hollebrands, Valentina Acierno, Catrienus de Jong, Laurice Pouvreau, João Paulo, Salvador A. Gezan, and Luisa M. Trindade. 2025. "GWAS Identifies SNP Markers and Candidate Genes for Off-Flavours and Protein Content in Faba Bean (Vicia faba L.)" Plants 14, no. 2: 193. https://doi.org/10.3390/plants14020193
APA StyleLippolis, A., Hollebrands, B., Acierno, V., de Jong, C., Pouvreau, L., Paulo, J., Gezan, S. A., & Trindade, L. M. (2025). GWAS Identifies SNP Markers and Candidate Genes for Off-Flavours and Protein Content in Faba Bean (Vicia faba L.). Plants, 14(2), 193. https://doi.org/10.3390/plants14020193