Rice Science ›› 2025, Vol. 32 ›› Issue (5): 704-716.DOI: 10.1016/j.rsci.2025.06.009
• Research Papers • Previous Articles Next Articles
Sabarinathan Selvaraj1,2, Parameswaran Chidambaranathan1(
), Goutam Kumar Dash1,3, Priyadarsini Sanghamitra1(), Kishor Pundlik Jeughale1, Cayalvizhi Balasubramaniasai1, Devraj Lenka2, Basavantraya Navadagi Devanna1, Seenichamy Rathinam Prabhukarthikeyan4, Sanghamitra Samantaray1, Amaresh Kumar Nayak5
Received:2025-01-27
Accepted:2025-06-19
Online:2025-09-28
Published:2025-10-11
Contact:
Parameswaran Chidambaranathan (Sabarinathan Selvaraj, Parameswaran Chidambaranathan, Goutam Kumar Dash, Priyadarsini Sanghamitra, Kishor Pundlik Jeughale, Cayalvizhi Balasubramaniasai, Devraj Lenka, Basavantraya Navadagi Devanna, Seenichamy Rathinam Prabhukarthikeyan, Sanghamitra Samantaray, Amaresh Kumar Nayak. Long-Range Admixture Linkage Disequilibrium and Allelic Responses of Sub1 and TPP7 under Consecutive Stress in Rice Validated Through Mendelian Randomization[J]. Rice Science, 2025, 32(5): 704-716.
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| Stress response | Score | Survival percentage in GUSa (%) | Plant height in GUSRa (cm) | Plant height in WDa (cm) | Recovery rate in SWDRa (%) | CSESa |
|---|---|---|---|---|---|---|
| Strongly tolerant | 1 | 100 (1) | 26-30 (2) | 26-30 (1) | 90-100 (19) | 0.2-2.0 (0) |
| Tolerant | 3 | 95-99 (0) | 21-25 (2) | 21-25 (4) | 70-89 (7) | 2.1-4.0 (0) |
| Moderately tolerant | 5 | 75-94 (15) | 16-20 (7) | 16-20 (14) | 40-69 (6) | 4.1-6.0 (17) |
| Sensitive | 7 | 50-74 (21) | 10-15 (22) | 10-15 (28) | 20-39 (9) | 6.1-8.0 (57) |
| Highly sensitive | 9 | 0-49 (93) | 0-9 (97) | 0-9 (83) | 0-19 (89) | 8.1-9.0 (56) |
Table 1. Consecutive stress evaluation method.
| Stress response | Score | Survival percentage in GUSa (%) | Plant height in GUSRa (cm) | Plant height in WDa (cm) | Recovery rate in SWDRa (%) | CSESa |
|---|---|---|---|---|---|---|
| Strongly tolerant | 1 | 100 (1) | 26-30 (2) | 26-30 (1) | 90-100 (19) | 0.2-2.0 (0) |
| Tolerant | 3 | 95-99 (0) | 21-25 (2) | 21-25 (4) | 70-89 (7) | 2.1-4.0 (0) |
| Moderately tolerant | 5 | 75-94 (15) | 16-20 (7) | 16-20 (14) | 40-69 (6) | 4.1-6.0 (17) |
| Sensitive | 7 | 50-74 (21) | 10-15 (22) | 10-15 (28) | 20-39 (9) | 6.1-8.0 (57) |
| Highly sensitive | 9 | 0-49 (93) | 0-9 (97) | 0-9 (83) | 0-19 (89) | 8.1-9.0 (56) |
Fig. 1. Box plot analysis of parental and recombinant alleles under consecutive stress conditions. A-C are parental allele comparison, and D-L are parental vs recombinant allele comparison. GUS, Germination under submergence; SWDR, Severe water deficit recovery; WD, Water deficit stress. B2, Bhalum 2; N22, Nagina 22. * indicates significance level at 5% in Mendelian randomization analysis.
Fig. 2. LRLD region analysis under consecutive stresses. A, Meta-QTL analysis for anaerobic germination and submergence tolerance in rice. Co-segregation regions are marked with blue circles. B, QTLs identified for consecutive stress conditions using mapping populations. LOD, Logarithm of the odds score; C, Mendelian randomization analysis for key traits associated with consecutive stress tolerance with exposure and outcome framework. *** indicates high significance. D-F, Genetic association of markers in long-range linkage disequilibrium regions using mendelian randomization analysis. Diagonal line in D-F represents intercept line. GUS, Germination under submergence; GUSR, Germination under submergence recovery; WD, Water deficit; SWDR, Severe water deficit recovery.
| QTL | Trait | Stress condition | Chromosome | LOD | PVE (%) | Additive effect | Left marker | Right marker |
|---|---|---|---|---|---|---|---|---|
| qGSS-1-1 | Survival percentage | GUS | 9 | 2.56 | 2.34 | 2.073 | SUB1BC1 | RM24093 |
| qGSS-1-2 | Survival percentage | GUS | 9 | 2.58 | 2.35 | 2.071 | TPP7_INDEL2 | RM24199 |
| qGSG-1-1 | Germination percentage | GUS | 9 | 2.63 | 1.55 | 2.106 | TPP7_INDEL2 | RM24199 |
| qGSGR-1-1 | Germination rate | GUS | 9 | 2.54 | 1.57 | 1.640 | RM24093 | TPP7_INDEL2 |
| qGSGR-1-2 | Germination rate | GUS | 9 | 2.72 | 1.63 | 1.675 | TPP7_INDEL2 | RM24199 |
| qPHR-1-1 | Plant height | GUSR | 9 | 9.27 | 1.96 | 16.862 | RM24093 | TPP7_INDEL2 |
| qPHR-1-2 | Plant height | GUSR | 9 | 9.41 | 1.97 | 16.993 | TPP7_INDEL2 | RM24199 |
| qPHWD-1-1 | Plant height | WD | 9 | 12.75 | 1.85 | 21.813 | RM24093 | TPP7_INDEL2 |
| qPHWD-1-2 | Plant height | WD | 9 | 13.06 | 1.86 | 21.892 | TPP7_INDEL2 | RM24199 |
| qLLWD-1-1 | Leaf length | WD | 9 | 9.91 | 2.33 | 11.749 | RM24093 | TPP7_INDEL2 |
| qLLWD-1-2 | Leaf length | WD | 9 | 9.50 | 2.33 | 11.795 | TPP7_INDEL2 | RM24199 |
| qLWWD-1-1 | Leaf width | WD | 9 | 3.12 | 2.57 | 0.196 | RM24093 | TPP7_INDEL2 |
| qLWWD-1-2 | Leaf width | WD | 9 | 3.87 | 2.54 | 0.194 | TPP7_INDEL2 | RM24199 |
| qSWD-1-1 | SPAD | WD | 9 | 17.11 | 1.54 | 17.949 | SUB1BC1 | RM24093 |
| qSWD-1-2 | SPAD | WD | 9 | 19.95 | 1.54 | 17.938 | RM24093 | TPP7_INDEL2 |
| qSWD-1-3 | SPAD | WD | 9 | 19.71 | 1.55 | 17.960 | TPP7_INDEL2 | RM24199 |
Table 2. QTLs identified under consecutive stress conditions between Bhalum 2 and Nagina 22 recombinant inbred line populations.
| QTL | Trait | Stress condition | Chromosome | LOD | PVE (%) | Additive effect | Left marker | Right marker |
|---|---|---|---|---|---|---|---|---|
| qGSS-1-1 | Survival percentage | GUS | 9 | 2.56 | 2.34 | 2.073 | SUB1BC1 | RM24093 |
| qGSS-1-2 | Survival percentage | GUS | 9 | 2.58 | 2.35 | 2.071 | TPP7_INDEL2 | RM24199 |
| qGSG-1-1 | Germination percentage | GUS | 9 | 2.63 | 1.55 | 2.106 | TPP7_INDEL2 | RM24199 |
| qGSGR-1-1 | Germination rate | GUS | 9 | 2.54 | 1.57 | 1.640 | RM24093 | TPP7_INDEL2 |
| qGSGR-1-2 | Germination rate | GUS | 9 | 2.72 | 1.63 | 1.675 | TPP7_INDEL2 | RM24199 |
| qPHR-1-1 | Plant height | GUSR | 9 | 9.27 | 1.96 | 16.862 | RM24093 | TPP7_INDEL2 |
| qPHR-1-2 | Plant height | GUSR | 9 | 9.41 | 1.97 | 16.993 | TPP7_INDEL2 | RM24199 |
| qPHWD-1-1 | Plant height | WD | 9 | 12.75 | 1.85 | 21.813 | RM24093 | TPP7_INDEL2 |
| qPHWD-1-2 | Plant height | WD | 9 | 13.06 | 1.86 | 21.892 | TPP7_INDEL2 | RM24199 |
| qLLWD-1-1 | Leaf length | WD | 9 | 9.91 | 2.33 | 11.749 | RM24093 | TPP7_INDEL2 |
| qLLWD-1-2 | Leaf length | WD | 9 | 9.50 | 2.33 | 11.795 | TPP7_INDEL2 | RM24199 |
| qLWWD-1-1 | Leaf width | WD | 9 | 3.12 | 2.57 | 0.196 | RM24093 | TPP7_INDEL2 |
| qLWWD-1-2 | Leaf width | WD | 9 | 3.87 | 2.54 | 0.194 | TPP7_INDEL2 | RM24199 |
| qSWD-1-1 | SPAD | WD | 9 | 17.11 | 1.54 | 17.949 | SUB1BC1 | RM24093 |
| qSWD-1-2 | SPAD | WD | 9 | 19.95 | 1.54 | 17.938 | RM24093 | TPP7_INDEL2 |
| qSWD-1-3 | SPAD | WD | 9 | 19.71 | 1.55 | 17.960 | TPP7_INDEL2 | RM24199 |
Fig. 3. Response of parental lines (Bhalum 2, B2 and Nagina 22, N22) and transgressive segregation lines (BN59 and N104) under submergence conditions. A, Relative expression levels of TPP7, MRLK59, and WAK79 genes of coleoptile at 7 d after sowing. B-G, Biochemical analysis of malondialdehyde (MDA) content (B), proline content (C), superoxide dismutase (SOD) activity (D), protein content (E), catalase (CAT) activity (F), and ascorbate peroxidase (APX) activity (G). Data are mean ± SD (n = 3). Different lowercase letters represent significant difference at the 0.05 level using the honestly significant difference (HSD) test.
| Consecutive stress condition | Trait | Parental line | Transgressive segregation line | ||
|---|---|---|---|---|---|
| Bhalum 2 | Nagina 22 | BN59 | BN104 | ||
| Germination under submergence | Survival percentage (%) | 37.66 ± 2.51 c | 46.66 ± 2.88 b | 95.00 ± 5.00 a | 93.33 ± 2.88 a |
| Germination under submergence recovery | Plant height (cm) | 33.63 ± 2.10 d | 41.40 ± 1.25 b | 37.72 ± 0.98 c | 45.33 ± 0.94 a |
| Water deficit | Plant height (cm) | 38.88 ± 1.20 c | 57.84 ± 1.96 a | 40.76 ± 1.78 c | 51.86 ± 1.47 b |
| Recovery from severe water deficit | Recovery rate (%) | 96.66 ± 5.77 a | 100.00 ± 0.00 a | 78.33 ± 2.88 b | 71.66 ± 2.88 c |
| Recovery after consecutive stress | Plant height (cm) | 117.40 ± 2.53 a | 110.80 ± 2.34 ab | 103.63 ± 5.03 b | 113.63 ± 5.87 a |
| Panicle length (cm) | 21.26 ± 2.59 a | 18.26 ± 0.80 b | 21.73 ± 0.61 a | 18.43 ± 1.13 b | |
| Number of tillers | 22.66 ± 5.13 a | 14.00 ± 1.00 b | 22.66 ± 2.51 a | 30.33 ± 7.09 a | |
| Filled grains | 100.66 ± 8.62 b | 65.66 ± 10.06 c | 154.33 ± 11.15 a | 66.33 ± 5.13 c | |
| Chaffy grains | 20.66 ± 3.78 a | 5.00 ± 1.00 b | 20.66 ± 11.37 a | 11.00 ± 1.00 ab | |
| 1000-grain weight (g) | 20.70 ± 1.70 ab | 19.90 ± 0.20 b | 20.90 ± 0.10 ab | 22.00 ± 0.50 a | |
| Single plant yield (g) | 31.83 ± 0.62 a | 23.93 ± 4.03 b | 36.53 ± 1.25 a | 20.96 ± 4.40 b | |
Table 3. Major consecutive stress tolerance traits and yield-related traits after recovery.
| Consecutive stress condition | Trait | Parental line | Transgressive segregation line | ||
|---|---|---|---|---|---|
| Bhalum 2 | Nagina 22 | BN59 | BN104 | ||
| Germination under submergence | Survival percentage (%) | 37.66 ± 2.51 c | 46.66 ± 2.88 b | 95.00 ± 5.00 a | 93.33 ± 2.88 a |
| Germination under submergence recovery | Plant height (cm) | 33.63 ± 2.10 d | 41.40 ± 1.25 b | 37.72 ± 0.98 c | 45.33 ± 0.94 a |
| Water deficit | Plant height (cm) | 38.88 ± 1.20 c | 57.84 ± 1.96 a | 40.76 ± 1.78 c | 51.86 ± 1.47 b |
| Recovery from severe water deficit | Recovery rate (%) | 96.66 ± 5.77 a | 100.00 ± 0.00 a | 78.33 ± 2.88 b | 71.66 ± 2.88 c |
| Recovery after consecutive stress | Plant height (cm) | 117.40 ± 2.53 a | 110.80 ± 2.34 ab | 103.63 ± 5.03 b | 113.63 ± 5.87 a |
| Panicle length (cm) | 21.26 ± 2.59 a | 18.26 ± 0.80 b | 21.73 ± 0.61 a | 18.43 ± 1.13 b | |
| Number of tillers | 22.66 ± 5.13 a | 14.00 ± 1.00 b | 22.66 ± 2.51 a | 30.33 ± 7.09 a | |
| Filled grains | 100.66 ± 8.62 b | 65.66 ± 10.06 c | 154.33 ± 11.15 a | 66.33 ± 5.13 c | |
| Chaffy grains | 20.66 ± 3.78 a | 5.00 ± 1.00 b | 20.66 ± 11.37 a | 11.00 ± 1.00 ab | |
| 1000-grain weight (g) | 20.70 ± 1.70 ab | 19.90 ± 0.20 b | 20.90 ± 0.10 ab | 22.00 ± 0.50 a | |
| Single plant yield (g) | 31.83 ± 0.62 a | 23.93 ± 4.03 b | 36.53 ± 1.25 a | 20.96 ± 4.40 b | |
Fig. 4. Model for the evaluation of long-range linkage disequilibrium (LRLD) responses under consecutive stress conditions. LRLD is identified in the admixture population and evaluated in a structured population in linkage equilibrium. Consecutive stresses and exposure-outcome framework of mendelian randomization were utilized for the validation. DAS, Days after sowing; GUS, Germination under submergence; GUSR, Germination under submergence recovery; WD, Water deficit.
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