The Integration of Genome-Wide Association Study and Homology Analysis to Explore the Genomic Regions and Candidate Genes for Panicle-Related Traits in Foxtail Millet
Abstract
:1. Introduction
2. Results
2.1. Phenotypic Characteristics of Six Panicle-Related Traits in Foxtail Millet
2.2. Genotyping, Population Structure, Principal Component, and Linkage Disequilibrium Analysis
2.3. Quantitative Trait Nucleotides (QTNs) and QTL Regions for Six Panicle-Related Traits
2.4. Candidate Gene Mining and Haplotype Analysis Based on Homology Comparison Strategy
3. Discussion
4. Materials and Methods
4.1. Plant Materials
4.2. Measurement and Statistical Analysis of Panicle-Related Traits
4.3. Genotyping, Population Structure, Principal Component, and Linkage Disequilibrium Analysis
4.4. Genome-Wide Association Study
4.5. Candidate Gene Mining and Haplotype Analysis Based on Homologous Alignment
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Traits | Environments | Range | Mean | SD | CV | h2 | Genotype | Environment |
---|---|---|---|---|---|---|---|---|
Panicle length (PL, cm) | 2015 | 4.50–43.90 | 22.20 | 5.50 | 20% | 0.78 | ** | ** |
2016 | 8.80–40.00 | 19.30 | 4.40 | 20% | ||||
BLUP | 10.72–31.27 | 20.81 | 3.12 | 15% | ||||
Main panicle diameter (MPD, mm) | 2015 | 9.40–48.24 | 23.31 | 6.36 | 27% | 0.74 | ** | ** |
2016 | 10.19–42.82 | 22.63 | 4.69 | 21% | ||||
BLUP | 14.80–35.47 | 22.95 | 3.03 | 13% | ||||
Panicle weight per panicle (PWP, g) | 2015 | 0.58–57.69 | 17.86 | 9.69 | 54% | 0.73 | ** | ** |
2016 | 1.06–35.74 | 14.71 | 5.89 | 40% | ||||
BLUP | 7.64–30.45 | 16.26 | 4.32 | 27% | ||||
Grain weight per panicle (GWP, g) | 2015 | 0.50–48.88 | 15.06 | 8.51 | 57% | 0.74 | ** | ** |
2016 | 1.36–36.34 | 12.51 | 5.29 | 42% | ||||
BLUP | 6.30–26.78 | 13.73 | 3.88 | 28% | ||||
Bristle length (BL, mm) | 2015 | 0.00–14.37 | 4.23 | 2.04 | 48% | 0.91 | ** | * |
2016 | 0.00–10.48 | 3.86 | 1.76 | 46% | ||||
BLUP | 0.35–10.41 | 4.03 | 1.60 | 40% | ||||
Thousand-grain weight (TGW, g) | 2015 | 0.72–3.62 | 2.58 | 0.48 | 19% | 0.81 | ** | ** |
2016 | 1.08–4.36 | 2.76 | 0.44 | 16% | ||||
BLUP | 1.55–3.31 | 2.66 | 0.31 | 11% |
Traits | Environments | Number of Significant SNPs | Range of R2 (%) | Average of R2 (%) |
---|---|---|---|---|
Panicle length | 2015 | 82 | 0.04–12.81 | 4.89 |
2016 | 111 | 0.25–8.04 | 2.62 | |
BLUP | 371 | 4.06–6.63 | 4.90 | |
Main panicle diameter | 2015 | 13 | 0.04–20.21 | 4.37 |
2016 | 41 | 0.06–7.89 | 3.45 | |
BLUP | 55 | 4.03–6.67 | 4.72 | |
Panicle weight per panicle | 2015 | 231 | 0.44–25.85 | 5.69 |
2016 | 28 | 0.01–12.37 | 6.92 | |
BLUP | 36 | 4.06–5.95 | 4.63 | |
Grain weight per panicle | 2015 | 270 | 0.24–25.13 | 5.76 |
2016 | 48 | 0.89–12.41 | 6.02 | |
BLUP | 37 | 4.09–6.27 | 4.62 | |
Bristle length | 2015 | 36 | 0.03–26.78 | 16.01 |
2016 | 24 | 2.33–23.30 | 11.91 | |
BLUP | 320 | 3.99–12.44 | 4.91 | |
Thousand-grain weight | 2015 | 154 | 0.01–11.53 | 1.70 |
2016 | 65 | 0.03–10.08 | 3.13 | |
BLUP | 334 | 3.89–7.35 | 4.61 | |
Total | - | 1830 | 0.01–26.78 | 5.60 |
No. | QTL | Chr | QTL Region (Mb) | No. of QTN | QTN | Pos | R2 (%) | Trait Environment |
---|---|---|---|---|---|---|---|---|
1 | PL_q2-1 | 2 | 26.405–26.442 | 8 | 2:26442425 | 26442425 | 9.30 | PL.15, PL.blup |
2 | PL_q2-2 | 2 | 37.921–37.974 | 112 | 2:37940934 | 37940934 | 6.63 | PL.16, PL.blup |
3 | PL_q2-3 | 2 | 38.066–38.179 | 37 | 2:38117003 | 38117003 | 4.70 | PL.16, PL.blup |
4 | PL_q3-1 | 3 | 14.919–15.034 | 31 | 3:14994886 | 14994886 | 8.21 | PL.15, PL.blup |
5 | PL_q3-4 | 3 | 50.531–50.635 | 9 | 3:50544489 | 50544489 | 4.80 | PL.15, PL.blup |
6 | PL_q6-1 | 6 | 31.569–31.578 | 4 | 6:31578055 | 31578055 | 5.65 | PL.16, PL.blup |
7 | PL_q7-1 | 7 | 13.851–13.948 | 26 | 7:13860822 | 13860822 | 12.81 | PL.15, PL.blup |
8 | PL_q7-2 | 7 | 14.113–14.169 | 6 | 7:14120111 | 14120111 | 10.85 | PL.15, PL.16, PL.blup |
9 | PL_q9-1 | 9 | 45.700–45.712 | 26 | 9:45712081 | 45712081 | 5.62 | PL.15, PL.blup |
10 | PWP_q1-2 | 1 | 37.334–37.415 | 11 | 1:37334234 | 37334234 | 25.28 | PWP.15, PWP.blup |
11 | PWP_q2-1 | 2 | 26.393–26.414 | 4 | 2:26392717 | 26392717 | 4.55 | PWP.16, PWP.blup |
12 | PWP_q7-1 | 7 | 13.928–13.937 | 4 | 7:13927683 | 13927683 | 10.78 | PWP.15, PWP.blup |
13 | GWP_q1-2 | 1 | 37.334–37.415 | 12 | 1:37334234 | 37334234 | 24.66 | GWP.15, GWP.blup |
14 | GWP_q2-4 | 2 | 26.392–26.414 | 4 | 2:26392093 | 26392093 | 4.96 | GWP.16, GWP.blup |
15 | GWP_q7-1 | 7 | 13.853–13.958 | 8 | 7:13927683 | 13927683 | 10.60 | GWP.15, GWP.16, GWP.blup |
16 | BL_q1-4 | 1 | 30.818–30.944 | 16 | 1:30890043 | 30890043 | 12.67 | BL.15, BL.16, BL.blup |
17 | BL_q1-5 | 1 | 31.336–31.388 | 19 | 1:31384418 | 31384418 | 13.65 | BL.15, BL.blup |
18 | BL_q1-6 | 1 | 37.312–37.386 | 190 | 1:37322139 | 37322139 | 23.46 | BL.15, BL.16, BL.blup |
19 | BL_q1-7 | 1 | 37.626–37.728 | 39 | 1:37724771 | 37724771 | 24.65 | BL.15, BL.16, BL.blup |
20 | BL_q1-8 | 1 | 37.730–37.818 | 62 | 1:37751602 | 37751602 | 24.16 | BL.15, BL.16, BL.blup |
21 | BL_q1-9 | 1 | 37.854–37.942 | 15 | 1:37855555 | 37855555 | 12.44 | BL.15, BL.16, BL.blup |
22 | BL_q1-10 | 1 | 38.004–38.100 | 4 | 1:38099726 | 38099726 | 23.57 | BL.15, BL.blup |
23 | BL_q1-11 | 1 | 38.240–38.293 | 20 | 1:38251263 | 38251263 | 21.12 | BL.15, BL.16, BL.blup |
24 | BL_q4-1 | 4 | 0.833–0.893 | 6 | 4:893187 | 893187 | 7.54 | BL.16, BL.blup |
25 | BL_q8-1 | 8 | 1.635–1.668 | 18 | 8:1635250 | 1635250 | 8.93 | BL.16, BL.blup |
26 | BL_q9-1 | 9 | 42.909–42.944 | 20 | 9:42943571 | 42943571 | 14.14 | BL.15, BL.blup |
27 | TGW_q5-1 | 5 | 0.546–0.549 | 4 | 5:545898 | 545898 | 8.32 | TGW.16, TGW.blup |
QTL Regions | Chr | QTL Region (Mb) | Previous Reported QTL | Position of Previous QTL (Mb) | Ref. |
---|---|---|---|---|---|
BL_q1-5 | 1 | 31.336–31.388 | qMPL1.1 (PL), qMPD1.1 (PD), qPWP1.1 (PWP), qGWP1.1 (GWP), qpl1 (PL), qpd1 (PD), C1.31690904 (GY) | 31.728–31.929 | [15,23,25] |
PWP_q1-1, GWP_q1-1 | 1 | 34.970–34.987 | unnamed (BL) | 35.883–35.869 | [24] |
PL_q2-2, PL_2-3 | 2 | 37.921–38.179 | qMPL2.1 (PL) | 39.726 | [15] |
PL_q2-4 | 2 | 49.117–49.200 | unnamed (GY) | 49.065 | [24] |
TGW_q3-1 | 3 | 6.258–6.342 | unnamed (PWP) | 6.768 | [24] |
PWP_q3-1, GWP_q3-1 | 3 | 7.353–7.409 | qGWP3.1 (GWP), unnamed (TGW) | 7.412–7.806 | [24,26] |
PL_q3-1 | 3 | 14.919–15.034 | unnamed (PL) | 14.391 | [23] |
MPD_q3-1, TGW_q3-2 | 3 | 23.616–23.733 | unnamed (GY) | 24.672 | [24] |
PL_q3-2 | 3 | 39.875–39.995 | qPWP3.1 (PWP), qGWP3.2 (GWP) | 39.037 | [26] |
TGW_q3-3 | 3 | 43.160–43.182 | unnamed (PL), unnamed (TGW) | 43.132–43.267 | [23,24] |
MPD_q3-2 | 3 | 47.020–47.023 | qPWP3.3 (PWP) | 46.338–46.477 | [26] |
PL_q3-4 | 3 | 50.531–50.635 | unnamed (GY) | 50.073 | [23] |
BL_q4-1 | 4 | 0.833–0.893 | unnamed (BL) | 0.871 | [24] |
MPD_q4-1 | 4 | 34.740–34.746 | qtgw4 (TGW) | 34.306 | [25] |
MPD_q5-2 | 5 | 45.138–45.166 | qMPD5.2 (MPD), qTGW5.1 (TGW), qpw5 (PWP), qpd5(PD) | 44.125–44.511 | [15,25] |
PWP_q6-1, GWP_q6-1, PWP_q6-2, GWP_q6-2 | 6 | 2.535–2.794 | qPWP6.2 (PWP), unnamed (GY) | 2.631–3.434 | [23,26] |
PWP_q6-7, GWP_q6-7, GWP_q6-9, PWP_q6-8, GWP_q6-9 | 6 | 27.924–28.247 | qPNL6 (PL) | 28.589 | [16] |
TGW_q6-1 | 6 | 34.670–34.733 | qMPD6.1 (PD) | 34.199 | [15] |
PL_q7-1, TGW_q7-1, PWP_q7-1, GWP_q7-1 | 7 | 13.851–13.961 | qGWP7.1 (GWP), qPWP7.2 (PWP) | 13.405–13.643 | [26] |
PL_q7-2, TGW_q7-2, TGW_q7-3 | 7 | 14.113–14.893 | unnamed (GY) | 14.094 | [23] |
TGW_q7-8 | 7 | 18.967–19.040 | unnamed (GY) | 19.465 | [23] |
GWP_q8-1 | 8 | 2.181–2.191 | qGWP8.1 (GWP), qTGW8.1 (TGW) | 2.223–2.605 | [26] |
TGW_q8-1 | 8 | 28.829–28.851 | qPD8.1 (PD) | 29.501 | [16] |
Gene ID | Chr | Position | QTL Region | Homologs in Rice | The Function of Orthologue in Rice |
---|---|---|---|---|---|
Si1g24310 | 1 | 31.649-31.652 | BL_q1-5 | OsPRR1 (LOC_Os02g40510) [27] | Internode length, spike length, tiller number, grain size, and number of primary branches |
Si1g27910 | 1 | 34.867-34.874 | GWP_q1-1 PWP_q1-1 | OsMADS6 (LOC_Os02g45770) [28] | Protein content, sterility or low fertility, gelatinization temperature, amylose content, seed setting rate, grain width, grain length, floral organ development characteristics, and total starch content |
Si1g31910 | 1 | 37.921-37.926 | BL_q1-10 | OsGRF4; GS2; GL2; PT2; LGS1; GLW2(LOC_Os02g47280) [29] | Grain shape, ear length, grain size, grain yield, seed drop, cold tolerance, grain width, grain length, plant dry weight, 1000-grain weight, plant cell size, plant fresh weight, and nitrogen use efficiency |
Si1g34880 | 1 | 40.251-40.252 | PL_q1-2 | OsMKK4; SMG1 (LOC_Os02g54600) [30] | Plant height, grain size, panicle type, filled grains per panicle, grain width, grain length, lignin content, cytokinin content, diterpenoid phytoalexin content, and 1000-grain weight |
Si2g10220 | 2 | 9.256-9.262 | GWP_q2-3 | LLB; pls3; OsMTS1 (LOC_Os07g14350) [31] | Rice blast resistance, bacterial blight resistance, leaf color, chlorophyll content, grain yield, leaf inclination, leaf senescence, lesion-like lesion, hydrogen peroxide, jasmonic acid, and aboveground biomass |
Si2g27120 | 2 | 36.896-36.902 | BL_q2-1 | qGW8; OsSPL16 (LOC_Os08g41940) [32] | Grain shape, cooking quality, grain size, mitotic cycle, and 1000-grain weight |
Si2g43940 | 2 | 49.297-49.308 | PL_q2-4 | DTH7; Ghd7.1; OsPRR37 (LOC_Os07g49460) [33] | Plant height, heading date, photoperiod sensitivity, growth period, and grain number per panicle |
Si3g11190 | 3 | 7.375-7.379 | PWP_q3-1 GWP_q3-1 | GSE5; GW5 (LOC_Os05g09520) [34] | Grain shape, grain size, grain width, grain length, and 1000-grain weight |
Si3g11200 | 3 | 7.390-7.394 | PWP_q3-1 GWP_q3-1 | OsDER1 (LOC_Os05g09550) [35] | Seed development characteristics, grain width, grain length, and 1000-grain weight |
Si3g33230 | 3 | 43.050-43.055 | TGW_q3-3 | OsCSLD4; NRL1; ND1; OsCD1 (LOC_Os12g36890) [36] | Plant height, leaf width, ear length, leaf inclination, leaf roll, grain number per ear, and sugar content |
Si4g02810 | 4 | 1.359-1.363 | TGW_q4-1 | OsACS6; SSG6 (LOC_Os06g03990) [37] | Grain size, grain width, grain length, starch granule shape, 1000-grain weight, chloroplast development, and starch granule size |
Si4g23080 | 4 | 34.377-34.386 | MPD_q4-1 | OsARF19; OsARF7a (LOC_Os06g48950) [38] | Internode length, leaf width, leaf length, grain yield, leaf inclination, floral organ development characteristics, auxin content, 1000-grain weight, and plant cell size |
Si5g01910 | 5 | 0.793-0.800 | TGW_q5-1 | DFO1; CCP1 (LOC_Os01g12890) [39] | Plant height, male sterility, seed morphology and anatomy, ear length, tiller number, lemma morphology and anatomy, seed setting rate, and primary branch number |
Si5g07490 | 5 | 5.957-5.958 | PL_q5-1 | OsLIR1 (LOC_Os01g01340) [40] | Vegetative growth potential, seed setting rate, photosynthetic capacity, and spikelet fertility |
Si5g07510 | 5 | 5.969-5.971 | PL_q5-1 | OsNPF6.1 (LOC_Os01g01360) [41] | Plant height, panicle number, nitrogen content, nitrate transport, yield per plant, and nitrogen use efficiency |
Si5g10260 | 5 | 8.652-8.657 | PWP_q5-1 | OsSQD2.2 (LOC_Os01g04920) [42] | Tiller number, seed setting rate, total starch content, and total soluble sugar content |
Si6g16030 | 6 | 27.100-27.101 | PWP_q6-3 GWP_q6-3 | ONAC106 (LOC_Os08g33670) [43] | Leaf color, fertility, ear length, grain yield, salt tolerance, tiller angle, ear number, grain number per ear, oriented gravity, and 1000-grain weight |
Si6g20480 | 6 | 31.677-31.680 | PL_q6-1 | OsSPL14; IPA1; WFP (LOC_Os08g39890) [44] | Rice blast resistance, bacterial blight resistance, plant height, ear length, tiller number, grain yield, ear branches, grain number per ear, seed setting rate, lodging rate, stem diameter, and 1000-grain weight |
Si6g23990 | 6 | 34.326-34.327 | TGW_q6-1 | OsSAUR45 (LOC_Os09g37400) [45] | Adventitious root number, plant height, root length, leaf width, and seed setting rate |
Si7g07780 | 7 | 15.603-15.606 | TGW_q7-7 | An-1 (LOC_Os04g28280) [46] | Awn length, grain number per ear, and grain length |
Si7g10650 | 7 | 19.276-19.279 | TGW_q7-8 | GIF1; OsCIN2 (LOC_Os04g33740) [47] | Viscous endosperm, grain size, grain yield, amylose content, amylopectin content, and invertase activity |
Si7g20960 | 7 | 27.099-27.101 | MPD_q7-1 | OsPIP1.1; OsPIP1a (LOC_Os02g44630) [48] | Grain yield, salt tolerance, germination rate, and germination rate |
Si7g27560 | 7 | 32.242-32.246 | PL_q7-4 | GS5 (LOC_Os05g06660) [49] | Grain size, characteristics of seed development, grain yield, grain width, and 1000-grain weight |
Si8g15190 | 8 | 28.271-28.275 | TGW_q8-1 | OsFKF1 (LOC_Os11g34460) [50] | Fertility, heading date, number of panicles per plant, number of grains per panicle, and 1000-grain weight |
Si9g12860 | 9 | 8.332-8.335 | PWP_q9-1 | OsNF-YA4; OsHAP2D (LOC_Os03g48970) [51] | Number of ears, number of ears, number of grains per ear, and grain weight |
Si9g13550 | 9 | 8.916-8.920 | GWP_q9-1 | OsFdC2 (LOC_Os03g48040) [52] | Plant height, leaf color, heading date, ear number per plant, grain number per ear, seed setting rate, photosynthetic capacity, carotenoid content, chlorophyll a content, chlorophyll b content, chlorophyll a/b ratio, and chloroplast development |
Si9g39120 | 9 | 45.984-45.994 | PL_q9-1 | VLN2 (LOC_Os03g24220) [53] | Morphological and anatomical characters of root, plant height, leaf angle, panicle type, seed setting rate, grain width, grain thickness, and 1000-grain weight |
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Liu, X.; Yang, Y.; Hou, S.; Men, Y.; Han, Y. The Integration of Genome-Wide Association Study and Homology Analysis to Explore the Genomic Regions and Candidate Genes for Panicle-Related Traits in Foxtail Millet. Int. J. Mol. Sci. 2022, 23, 14735. https://doi.org/10.3390/ijms232314735
Liu X, Yang Y, Hou S, Men Y, Han Y. The Integration of Genome-Wide Association Study and Homology Analysis to Explore the Genomic Regions and Candidate Genes for Panicle-Related Traits in Foxtail Millet. International Journal of Molecular Sciences. 2022; 23(23):14735. https://doi.org/10.3390/ijms232314735
Chicago/Turabian StyleLiu, Xiaodong, Yang Yang, Siyou Hou, Yihan Men, and Yuanhuai Han. 2022. "The Integration of Genome-Wide Association Study and Homology Analysis to Explore the Genomic Regions and Candidate Genes for Panicle-Related Traits in Foxtail Millet" International Journal of Molecular Sciences 23, no. 23: 14735. https://doi.org/10.3390/ijms232314735