Association Study of Symbiotic Genes in Pea (Pisum sativum L.) Cultivars Grown in Symbiotic Conditions
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Material
2.2. Microorganisms
2.3. Vegetation Experiment for Assesment of the Symbiotic Effectiveness of 99 Pea Cultivars
2.4. SNVs Detection and Cultivar Screening
Gene Identifier | Accession | Description |
---|---|---|
IGN1 [28] | KR047192 | Ankyrin-repeat protein with transmembrane regions |
GICP01056763 1 | ||
SEN1 [29] | KY888171 | Control of rhizobial differentiation |
GDTM01047803 2 | ||
SST1 [28] | KC008603 | Symbiotic sulphate transporter |
GDTM01043951 2 | ||
Sym29 | AJ495759 | CLAVATA1-like receptor |
GICP01072631 1 | ||
STR1 | GICP01133083 1 | ABC transporter G family member STR, required for arbuscule development |
STR2 | GICP01179536 1 | ABC transporter G family member STR, required for arbuscule development |
AMT2;3 | PsCam053936 3 | Ammonium transporter |
AMT2;5 | GICP01050721 1 | Ammonium transporter |
2.5. Statistical Analysis
2.6. Analysis of AM Development
3. Results
3.1. General Description of the Dataset
3.2. Correlation Analysis
3.3. Principal Component (PC) Decomposition
3.4. Genotyping of Cultivars
3.5. Association Analysis between the Allelic State of Sym-Genes and Traits
3.6. Regression Analysis of the Association of the AM-Caused Increments with SNVs
3.7. Association of the Root Mycorrhization Level and the Stem Length in Pea Cultivars
4. Discussion
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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Measured Trait | Mean Value, Rh | Mean Value, Rh + AM | Mean Increase (abs) 1 | Mean Increase (rel), % |
---|---|---|---|---|
Shoot weight, g | 1.96, SD = 0.668 | 3.62, SD = 0.725 | 1.67 ± 0.1 | 98.90% |
Shoot length, cm | 65.5, SD = 21.3 | 79.3, SD = 22.3 | 13.8 ± 1.9 | 24.00% |
Pod number | 1.56, SD = 0.43 | 2.61, SD = 0.622 | 1.05 ± 0.097 | 73.10% |
Seed number per plant | 4.87, SD = 1.97 | 10.6, SD = 3.13 | 5.75 ± 0.43 | 133.40% |
Seed weight per plant, g | 0.74, SD = 0.267 | 1.89, SD = 0.364 | 1.15 ± 0.061 | 183.30% |
Thousand-seed weight, g | 160, SD = 49.0 | 190, SD = 55.0 | 30.2 ± 3.7 | 20.30% |
Seed nitrogen content, mg/g | 38, SD = 5.25 | 30.5, SD = 3.17 | −7.54 ± 1.2 | −18.40% |
Seed phosphorus content, mg/g | 0.816, SD = 0.116 | 1.27, SD = 0.283 | 0.453 ± 0.06 | 58.30% |
Measured Trait | Paired t-Test 1 t-Statistic, p-Value | F-Test 2 F-Statistic, p-Value | Pearson Correlation Coefficient (R) | Coefficient of Determination, Adjusted (R2adj) |
---|---|---|---|---|
PW | 31.64, p-value = 3.07 × 10−53 | 1.18, p-value = 0.425 | 0.720, p-value = 4.55 × 10−17 | 0.513 |
PL | 14.71, p-value = 1.53 × 10−26 | 1.09, p-value = 0.659 | 0.910, p-value = 8.37 × 10−39 | 0.826 |
PN | 21.49, p-value = 7.21 × 10−39 | 2.09, p-value = 3.29 × 10−4 | 0.625, p-value = 4.93 × 10−12 | 0.384 |
SN | 26.47, p-value = 1.95 × 10−46 | 2.53, p-value = 6.53 × 10−6 | 0.731, p-value = 8.73 × 10−18 | 0.53 |
SW | 37.32, p-value = 9.76 × 10−60 | 1.86, p-value = 2.45 × 10−3 | 0.560, p-value = 1.62 × 10−9 | 0.307 |
TSW | 16.03, p-value = 3.89 × 10−29 | 1.26, p--value = 0.253 | 0.941, p-value = 1.40 × 10−47 | 0.885 |
NtS | −12.34, p-value = 1.17 × 10−21 | 0.37, p-value = 1.13 × 10−6 | 0.019, p-value = 0.85 | −0.01 |
PhS | 15.05, p-value = 3.23 × 10−27 | 5.96, p-value < 2.2 × 10−16 | 0.052, p-value = 0.611 | −0.008 |
Gene Identifier | Protein Substitutions |
---|---|
IGN1 | D108E |
SEN1 | P22A |
SST1 | S545Y |
Sym29 | F16S |
P43H | |
A53G | |
I171F | |
S618P | |
T623I | |
STR1 | E109K |
P397S | |
A401P | |
H475Y | |
STR2 | T676I |
AMT2;3 | A21P * |
N215I | |
Y385N | |
AMT2;5 | — |
SNV | Trait | p-Value | FDR | SNV | Trait | p-Value | FDR |
---|---|---|---|---|---|---|---|
Le.A229T | PL | 4.00 × 10−38 | 3.20 × 10−37 | SEN1.P22A | PL | 1.24 × 10−3 | 9.92 × 10−3 |
Le.A229T | PW | 9.54 × 10−9 | 3.81 × 10−8 | LykX.L42K | TSW | 1.53 × 10−3 | 8.65 × 10−3 |
Le.A229T | NtS | 7.82 × 10−7 | 2.08 × 10−6 | K1.E90D | TSW | 1.86 × 10−3 | 0.0149 |
LykX.L13V | SN | 4.43 × 10−6 | 3.55 × 10−5 | LykX.L42K | SN | 2.16 × 10−3 | 8.60 × 10−3 |
Le.A229T | PhS | 8.36 × 10−6 | 1.67 × 10−5 | Sym37.L56V | SN | 2.21 × 10−3 | 8.80 × 10−3 |
LykX.L9F | TSW | 1.20 × 10−5 | 9.57 × 10−5 | IGN1.D108E | PN | 2.36 × 10−3 | 9.20 × 10−3 |
LykX.A142I | TSW | 2.35 × 10−5 | 1.88 × 10−4 | IGN1.D108E | PL | 3.47 × 10−3 | 9.20 × 10−3 |
Le.A229T | SW | 3.37 × 10−5 | 5.39 × 10−5 | LykX.A142I | SN | 3.58 × 10−3 | 0.0143 |
LykX.L9F | SN | 4.96 × 10−5 | 1.98 × 10−4 | LykX.S134G | SW | 5.82 × 10−3 | 0.0466 |
LykX.L13V | PN | 1.30 × 10−4 | 5.19 × 10−4 | AMT2;3.N215I | SW | 6.46 × 10−3 | 0.0204 |
LykX.V86I | SN | 1.97 × 10−4 | 1.02 × 10−3 | AMT2;3.N215I | PL | 7.63 × 10−3 | 0.0204 |
LykX.F184S | SN | 1.97 × 10−4 | 1.02 × 10−3 | IGN1.D108E | TSW | 7.68 × 10−3 | 0.0154 |
IGN1.D108E | SN | 2.09 × 10−4 | 1.67 × 10−3 | Sym37.L56V | PN | 8.71 × 10−3 | 0.0232 |
Sym37.S45L | TSW | 2.30 × 10−4 | 1.84 × 10−3 | K1.E90D | SN | 0.0103 | 0.0411 |
LykX.V86I | TSW | 2.54 × 10−4 | 1.02 × 10−3 | AMT2;3.N215I | TSW | 0.0109 | 0.0218 |
LykX.F184S | TSW | 2.54 × 10−4 | 1.02 × 10−3 | LykX.L9F | PN | 0.0119 | 0.0316 |
Le.A229T | SN | 4.29 × 10−4 | 5.72 × 10−3 | LykX.L13V | PL | 0.0136 | 0.0273 |
Sym37.L56V | TSW | 5.40 × 10−4 | 4.32 × 10−3 | Sym37.S45L | PN | 0.0168 | 0.0480 |
Le.A229T | PN | 6.08 × 10−4 | 6.95 × 10−4 | Sym37.S45L | SN | 0.0180 | 0.0480 |
LykX.L13V | TSW | 7.74 × 10−4 | 2.06 × 10−3 | LykX.L13V | SW | 0.0296 | 0.0461 |
AMT2;3.N215I | PW | 1.17 × 10−3 | 9.36 × 10−3 | LykX.L13V | NtS | 0.0346 | 0.0461 |
SNV | PC | p-Value | FDR | SNV | PC | p-Value | FDR |
---|---|---|---|---|---|---|---|
Le.A229T | PC3 | 1.23 × 10−25 | 4.93 × 10−25 | LykX.L42K | PC2 | 2.40 × 10−3 | 9.61 × 10−3 |
Le.A229T | PC1 | 2.04 × 10−13 | 4.08 × 10−13 | IGN1.D108E | PC2 | 3.66 × 10−3 | 0.0130 |
Le.A229T | PC4 | 1.66 × 10−8 | 2.22 × 10−8 | K1.E90D | PC2 | 4.98 × 10−3 | 0.0199 |
LykX.L9F | PC2 | 1.13 × 10−5 | 4.51 × 10−5 | AMT2;3.N215I | PC1 | 5.13 × 10−3 | 0.0205 |
Sym37.S45L | PC2 | 9.71 × 10−5 | 3.88 × 10−4 | IGN1.D108E | PC1 | 6.51 × 10−3 | 0.0130 |
LykX.A142I | PC2 | 2.02 × 10−4 | 8.06 × 10−4 | STR2.T676I | PC2 | 7.70 × 10−3 | 0.0308 |
LykX.L13V | PC2 | 2.21 × 10−4 | 8.85 × 10−4 | LykX.S134G | PC1 | 0.0112 | 0.0450 |
Sym37.L56V | PC2 | 2.48 × 10−4 | 9.90 × 10−4 | SEN1.P22A | PC4 | 0.0145 | 0.0484 |
LykX.F184S | PC2 | 2.85 × 10−4 | 1.14 × 10−3 | K1.E90D | PC4 | 0.0219 | 0.0437 |
LykX.V86I | PC2 | 2.85 × 10−4 | 1.14 × 10−3 | SEN1.P22A | PC3 | 0.0242 | 0.0484 |
LykX.L13V | PC1 | 4.43 × 10−4 | 8.87 × 10−4 | LykX.L13V | PC3 | 0.0353 | 0.0471 |
Trait | The Formula Used in the Model |
---|---|
PW | dPW~PW.Rh + LE |
PL | dPL~PL.Rh + LE |
PN | dPN~LE |
SN | dSN~1 |
SW | dSW~SW.Rh |
TSW | dTSW~LE |
NtS | dNtS~NtS.Rh + LE |
PhS | dPhS~PhS.Rh + LE |
SNV | Trait | p-Value | FDR |
---|---|---|---|
AMT2;3.215NI | dTSW | 0.0050 | 0.0402 |
K1.31LI | dTSW | 0.0047 | 0.0379 |
LykX.16VF | dTSW | 0.0038 | 0.0301 |
LykX.184FS | dTSW | 0.0056 | 0.0447 |
SNV | PC | p-Value | FDR |
---|---|---|---|
AMT2;3.215NI | dPC2 | 0.0061 | 0.0243 |
LykX.16VF | dPC2 | 0.0093 | 0.0371 |
SST1.545SY | dPC1 | 0.0215 | 0.0430 |
SST1.545SY | dPC2 | 0.0164 | 0.0430 |
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Zhukov, V.A.; Zhernakov, A.I.; Sulima, A.S.; Kulaeva, O.A.; Kliukova, M.S.; Afonin, A.M.; Shtark, O.Y.; Tikhonovich, I.A. Association Study of Symbiotic Genes in Pea (Pisum sativum L.) Cultivars Grown in Symbiotic Conditions. Agronomy 2021, 11, 2368. https://doi.org/10.3390/agronomy11112368
Zhukov VA, Zhernakov AI, Sulima AS, Kulaeva OA, Kliukova MS, Afonin AM, Shtark OY, Tikhonovich IA. Association Study of Symbiotic Genes in Pea (Pisum sativum L.) Cultivars Grown in Symbiotic Conditions. Agronomy. 2021; 11(11):2368. https://doi.org/10.3390/agronomy11112368
Chicago/Turabian StyleZhukov, Vladimir A., Aleksandr I. Zhernakov, Anton S. Sulima, Olga A. Kulaeva, Marina S. Kliukova, Alexey M. Afonin, Oksana Y. Shtark, and Igor A. Tikhonovich. 2021. "Association Study of Symbiotic Genes in Pea (Pisum sativum L.) Cultivars Grown in Symbiotic Conditions" Agronomy 11, no. 11: 2368. https://doi.org/10.3390/agronomy11112368
APA StyleZhukov, V. A., Zhernakov, A. I., Sulima, A. S., Kulaeva, O. A., Kliukova, M. S., Afonin, A. M., Shtark, O. Y., & Tikhonovich, I. A. (2021). Association Study of Symbiotic Genes in Pea (Pisum sativum L.) Cultivars Grown in Symbiotic Conditions. Agronomy, 11(11), 2368. https://doi.org/10.3390/agronomy11112368