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Rice Science ›› 2025, Vol. 32 ›› Issue (5): 704-716.DOI: 10.1016/j.rsci.2025.06.009

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  • 收稿日期:2025-01-27 接受日期:2025-06-19 出版日期:2025-09-28 发布日期:2025-10-11

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. [J]. Rice Science, 2025, 32(5): 704-716.

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链接本文: http://www.ricesci.org/CN/10.1016/j.rsci.2025.06.009

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图/表 7

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)

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. 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.

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.

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

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.

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.

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

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.

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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