Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (18): 3533-3550.doi: 10.3864/j.issn.0578-1752.2024.18.003

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Phenotypical Variation and Dynamic QTL Mapping of Plant Height in Foxtail Millet at Different Developmental Stages

LIU DeLong1,2(), LI ShiRu1,2, WANG ChuanXing1, GUO ShuQing1, MA ZhiXiu1, WU YongJiang1, HAN HuiBing1, LI YuJie1, ZHANG PanPan2, YANG Pu1()   

  1. 1 College of Agriculture, Northwest A&F University/State Key Laboratory of Crop Stress Biology in Arid Areas, Yangling 712100, Shaanxi
    2 College of Life Science, Yulin University, Yulin 719000, Shaanxi
  • Received:2024-02-27 Accepted:2024-04-10 Online:2024-09-16 Published:2024-09-29
  • Contact: YANG Pu

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Abstract:

【Objective】 Plant height is a trait that plays an important role in the increase of foxtail millet yield. The dynamic changes of foxtail millet plant height at different growth stages were studied, and the QTL loci and effects controlling plant height were identified to provide a theoretical basis for plant type breeding of foxtail millet. 【Method】 In this study, a recombinant inbred line population YRRIL containing 215 lines were used as the research object, and the YRRIL population was planted in two environments, Yulin, Shaanxi and Mizhi, Shaanxi, in May 2023, respectively. The phenotypic values of plant height trait of each family were measured at five stages: seedling, elongation, booting, tasseling, and ripening period, respectively. Combined with the genetic linkage map of the YRRIL population, genetic analysis and dynamic QTL mapping of plant height trait at different growth stages of millet were carried out, and the unconditional QTL and conditional QTL controlling plant height of millet were identified. On this basis, candidate gene prediction for important QTL was carried out using Gene Ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis methods. 【Result】 In the entire growth period of the millet plant height growth trend was the “S” type curve, from the elongation stage to the booting stage, the growth rate of plant height was faster, which was the key stage of plant height development. In the two environments, plant height of each family line of the population showed continuous distribution at different periods. A total of 86 QTL related to plant height were detected at five periods in the two environments, which were distributed on all 9 chromosomes of the foxtail millet genome. It contained 48 unconditional QTL and 38 conditional QTL, and the phenotypic contribution rate of unconditional QTL was 1.13%-17.49%, of which 6 could be detected repeatedly at two growth periods, and the rest were detected only at one growth period. The phenotypic contribution rate of conditional QTL was 1.97%-14.69%, of which one could be detected repeatedly at two growth stages, and the rest were detected only at one growth stage. No QTL that can be detected in three or more periods were present in either unconditional QTL analysis or conditional QTL analysis. A total of 12 major QTL were detected by unconditional QTL and conditional QTL analysis in two environments, of which 6 QTL were newly identified as primary loci in this study. Based on the prediction and analysis of genes within the main effect QTL interval combined with functional annotation of homologous genes screened out 14 candidate genes that might be related to foxtail millet plant height, among which Seita.1G242300.1, Seita.6G110200.1, and Seita.7G143300.1 were all able to directly regulate plant height development. 【Conclusion】 In the two environments, a large number of QTL were detected to be involved in the phenotypic regulation of plant height trait during the whole growth and development of foxtail millet, with 79 (91.86%) played a role in one period and 7 (8.14%) played a role in two periods and there were no QTL detected in three or more periods, including 12 major QTL. The QTL detected by unconditional and conditional analysis methods accounted for 55.81% and 44.19%, respectively, and 16 (18.60%) were both unconditional and conditional QTL. The QTL effects controlling plant height development at different stages varied, with smaller effect in the seedling stage and generally larger effects from the elongation to the tasseling stage.

Key words: foxtail millet, RIL, plant height, plant architecture, QTL, candidate genes

Table 1

Determination time of plant height at different periods and determination method criteria"

时期
Periods		 生育期
Growth periods		 测定时间
Measuring time		 测定方法
Measurement methods		 参考文献
Reference
T1 苗期
Seedling stage		 播种后40 d
40 days after sowing		 自然状态下地面至植株最高叶的距离
The distance from the ground to the highest leaf of the plant under natural conditions		 /
T2 拔节期
Elongation stage		 播种后56 d
56 days after sowing		 地面至植株最上部展开叶叶尖距离
Distance from the ground to the tip of the uppermost unfolded leaf of the plant		 /
T3 孕穗期
Booting stage		 播种后72 d
72 days after sowing		 地面至幼穗顶部距离
Distance from the ground to the top of the spikelet		 /
T4 抽穗期
Tasseling stage		 田间50%的植株穗子完全伸出旗叶鞘
50% of the plants in the field had spikes fully protruding from the flag leaf sheaths		 齐穗后地面至穗子顶端距离
The distance from the ground to the top of the ear after full heading		 [32]
T5 成熟期
Ripening period		 田间50%的植株穂部籽粒完全硬化转成正常颜色
The grains of 50% plants in the field were completely hardened and turned into normal color		 成熟后地面至植株顶端（含穗）距离
The distance from the ground to the top of the plant (including spikes) after ripening		 [32]

Table 2

Phenotypic values of YRRIL population for plant height at different fertility periods"

性状
Trait		 时期
Periods		 环境
Environments		 平均值±标准差
Mean±SD		 变异系数
Coefficient of variation (%)		 最小值
Min value		 最大值
Max value		 偏度
Skewness		 峰度
Kurtosis
株高
PH (cm)		 T1 E1 24.38±2.12 8.70 19.42 30.33 0.30 -0.30
E2 18.81±3.79 20.15 8.88 27.63 -0.06 -0.43
T2 E1 45.58±5.57 12.22 32.50 65.00 0.42 0.19
E2 37.57±9.24 24.59 16.75 65.50 0.26 -0.24
T3 E1 98.16±12.97 13.21 57.50 133.25 0.11 -0.03
E2 94.36±10.31 10.93 71.67 119.33 0.12 -0.51
T4 E1 125.81±11.65 9.26 94.25 150.33 -0.23 -0.32
E2 98.94±11.45 11.57 72.00 136.00 0.33 -0.29
T5 E1 131.31±13.44 10.24 97.50 163.00 0.02 -0.27
E2 100.54±11.79 12.00 75.33 138.00 0.31 -0.22

Fig. 1

Bar chart of net plant height growth of millet YRRIL population in two environments at different growth stage"

Fig. 2

Correlation analysis of net plant height growth and plant height at maturity of YRRIL population under different environments at different fertility periods a: 2023 Yulin; b: 2023 Mizhi"

Table 3

Unconditional QTL for plant height detected in YRRIL population at different fertility periods"

时期
Periods		 环境
Environments		 数量性状位点
QTL		 染色体
Chromosome		 标记区间
Marker interval		 物理区间
Physical interval
(bp)		 LOD 加性效应
Additive effect		 贡献率
R2
(%)
T1 E1 qPH-3-1 Chr.3 c03b143-c03b144 49232103-49249434 5.20 0.70 4.13
qPH-3-2 Chr.3 c03b144-c03b145 49236212-49263886 5.01 0.71 4.27
qPH-4-1 Chr.4 c04b091-c04b092 32103966-32392762 4.90 0.55 2.60
qPH-7-1 Chr.7 c07b111-c07b112 28718452-28977042 10.15 0.97 7.85
qPH-8-1 Chr.8 c08b154-c08b155 35794684-36110021 3.78 -0.91 7.20
qPH-8-2 Chr.8 c08b176-c08b177 38668781-38953634 6.36 0.86 6.29
qPH-9-1 Chr.9 c09b120-c09b121 41372093-41585138 4.49 -0.54 2.44
E2 qPH-4-2 Chr.4 c04b111-c04b112 34316068-34803353 2.98 1.48 2.95
qPH-7-2 Chr.7 c07b143-c07b144 34974931-35164751 2.52 2.37 7.56
T2 E1 qPH-3-3 Chr.3 c03b135-c03b136 48347192-48472348 7.06 2.64 5.75
qPH-3-4 Chr.3 c03b136-c03b137 48422155-48788896 8.51 2.68 5.78
qPH-5-1 Chr.5 c05b044-c05b045 8175113-9040955 3.58 1.50 1.79
qPH-7-3 Chr.7 c07b113-c07b114 29002989-29630484 7.98 2.49 5.13
qPH-9-2 Chr.9 c09b009-c09b010 1065098-1132102 7.18 -1.79 2.64
qPH-9-3 Chr.9 c09b039-c09b040 7371255-7920890 3.02 -1.40 1.66
qPH-9-4 Chr.9 c09b166-c09b167 49092452-49697847 6.47 2.65 5.85
qPH-9-5 Chr.9 c09b167-c09b168 49697847-50189164 4.93 2.75 6.38
E2 qPH-3-5 Chr.3 c03b106-c03b107 40990588-42411342 5.57 2.97 4.83
qPH-4-3 Chr.4 c04b125-c04b126 36452291-36506711 2.74 5.03 14.41
qPH-7-4 Chr.7 c07b082-c07b083 21476252-21704756 3.48 2.29 3.00
qPH-9-6 Chr.9 c09b015-c09b016 1903164-1983343 4.67 -2.71 4.02
T3 E1 qPH-5-2 Chr.5 c05b028-c05b029 6388870-6398535 5.00 3.92 3.35
qPH-7-5 Chr.7 c07b114-c07b115 29307823-30059669 3.48 7.54 12.49
qPH-9-7 Chr.9 c09b008-c09b009 988753-1082109 3.53 -3.22 2.27
E2 qPH-1-1 Chr.1 c01b083-c01b084 26758853-27387031 4.75 3.50 7.65
qPH-3-6 Chr.3 c03b046-c03b047 7367554-7576946 3.51 -2.64 4.35
qPH-3-1 Chr.3 c03b143-c03b144 49232103-49249434 3.75 -2.31 3.42
qPH-4-4 Chr.4 c04b041-c04b042 6913490-7153895 2.96 -2.04 2.68
qPH-7-6 Chr.7 c07b055-c07b056 17909787-18105601 3.60 2.74 4.23
qPH-7-7 Chr.7 c07b090-c07b091 23079209-23253415 8.07 5.22 17.49
T4 E1 qPH-1-2 Chr.1 c01b109-c01b110 31914666-32213218 7.64 5.68 13.60
qPH-2-1 Chr.2 c02b089-c02b090 27836775-28229243 4.38 -5.74 13.79
qPH-3-7 Chr.3 c03b053-c03b054 9220324-9287696 6.40 -3.54 5.02
qPH-5-3 Chr.5 c05b041-c05b042 7885959-8086611 3.01 2.48 2.30
qPH-8-3 Chr.8 c08b057-c08b058 8950445-9240501 2.84 2.26 2.16
qPH-9-8 Chr.9 c09b002-c09b003 526353-660290 4.09 2.77 3.14
E2 qPH-2-2 Chr.2 c02b142-c02b143 44084471-44171197 6.84 6.47 16.32
qPH-5-4 Chr.5 c05b023-c05b024 5494776-5555640 4.14 3.16 3.73
qPH-7-8 Chr.7 c07b084-c07b085 21714345-21892410 7.39 3.53 4.87
qPH-9-9 Chr.9 c09b007-c09b008 983209-988753 3.31 2.35 2.07
qPH-9-10 Chr.9 c09b165-c09b166 49049868-49379087 3.42 6.12 14.41
T5 E1 qPH-1-3 Chr.1 c01b107-c01b108 31556531-31855243 8.23 5.22 7.57
qPH-2-1 Chr.2 c02b089-c02b090 27836775-28229243 6.45 -5.11 7.19
qPH-2-3 Chr.2 c02b115-c02b116 37968852-38141819 4.14 2.67 1.90
qPH-3-7 Chr.3 c03b053-c03b054 9220324-9287696 9.78 -4.16 4.57
qPH-5-5 Chr.5 c05b052-c05b053 12174846-13011016 5.45 3.99 4.15
qPH-7-9 Chr.7 c07b100-c07b101 26617489-26678123 6.11 5.24 7.68
qPH-8-3 Chr.8 c08b057-c08b058 8950445-9240501 2.59 2.01 1.13
qPH-9-11 Chr.9 c09b006-c09b007 803316-983209 8.99 4.02 4.38
qPH-9-12 Chr.9 c09b146-c09b147 45421642-45469731 4.13 -4.85 6.43
qPH-9-13 Chr.9 c09b175-c09b176 54557509-54694792 4.65 4.58 5.76
E2 qPH-2-2 Chr.2 c02b142-c02b143 44084471-44171197 5.42 5.93 12.09
qPH-5-6 Chr.5 c05b073-c05b074 30713393-30861542 3.07 5.19 9.14
qPH-7-8 Chr.7 c07b084-c07b085 21714345-21892410 8.55 4.52 7.03

Table 4

Conditional QTL for plant height detected in YRRIL population at different fertility periods"

阶段
Stages		 环境
Environments		 数量性状位点
QTL		 染色体
Chromosome		 标记区间
Marker interval		 物理区间
Physical interval
(bp)		 LOD 加性效应
Additive effect		 贡献率
R2
(%)
0—T1 E1 qPH-3-1 Chr.3 c03b143-c03b144 49232103-49249434 5.20 0.70 4.13
qPH-3-2 Chr.3 c03b144-c03b145 49236212-49263886 5.01 0.71 4.27
qPH-4-1 Chr.4 c04b091-c04b092 32103966-32392762 4.90 0.55 2.60
qPH-7-1 Chr.7 c07b111-c07b112 28718452-28977042 10.15 0.97 7.85
qPH-8-1 Chr.8 c08b154-c08b155 35794684-36110021 3.78 -0.91 7.20
qPH-8-2 Chr.8 c08b176-c08b177 38668781-38953634 6.36 0.86 6.29
qPH-9-1 Chr.9 c09b120-c09b121 41372093-41585138 4.49 -0.54 2.44
E2 qPH-4-2 Chr.4 c04b111-c04b112 34316068-34803353 2.98 1.48 2.95
qPH-7-2 Chr.7 c07b143-c07b144 34974931-35164751 2.52 2.37 7.56
T1—T2 E1 qPH-3-8 Chr.3 c03b132-c03b133 47561089-47780734 4.74 1.87 8.16
qPH-5-7 Chr.5 c05b043-c05b044 8131712-8175114 2.56 1.05 2.41
qPH-5-8 Chr.5 c05b108-c05b109 43783548-44258277 2.56 1.02 2.35
qPH-9-2 Chr.9 c09b009-c09b010 1065098-1132102 8.38 -1.87 8.16
qPH-9-14 Chr.9 c09b170-c09b171 51639430-52289028 4.58 1.39 4.56
qPH-9-15 Chr.9 c09b171-c09b172 51729253-52624644 3.45 1.21 3.47
E2 qPH-3-5 Chr.3 c03b106-c03b107 40990588-42411342 6.34 2.16 10.16
qPH-7-10 Chr.7 c07b088-c07b089 22843640-23052954 3.35 1.52 5.21
qPH-9-16 Chr.9 c09b014-c09b015 1849233-1941826 6.51 -2.22 10.60
T2—T3 E1 qPH-5-9 Chr.5 c05b019-c05b020 4766716-4845453 3.32 3.39 6.97
E2 qPH-1-4 Chr.1 c01b106-c01b107 31517802-31614766 6.25 6.27 14.24
qPH-1-3 Chr.1 c01b107-c01b108 31556531-31855243 6.53 6.37 14.69
qPH-3-9 Chr.3 c03b043-c03b044 6910556-7238657 4.80 -2.86 2.92
qPH-3-5 Chr.3 c03b106-c03b107 40990588-42411342 7.11 -3.62 4.41
qPH-3-10 Chr.3 c03b140-c03b141 49122420-49193085 3.29 -2.34 1.97
qPH-7-11 Chr.7 c07b052-c07b053 17638287-17791653 5.67 3.31 3.41
qPH-8-4 Chr.8 c08b072-c08b073 12913834-13599376 3.89 2.54 2.33
qPH-9-7 Chr.9 c09b008-c09b009 988753-1082109 6.42 3.46 4.22
T3—T4 E1 qPH-3-11 Chr.3 c03b126-c03b127 46785100-47002469 3.63 -3.55 3.20
qPH-6-1 Chr.6 c06b032-c06b033 3556319-3630370 10.48 -6.06 9.86
qPH-6-2 Chr.6 c06b065-c06b066 12542879-17978220 5.69 6.13 10.09
qPH-8-5 Chr.8 c08b044-c08b045 6087263-6623116 2.58 3.04 2.46
qPH-9-11 Chr.9 c09b006-c09b007 803316-983209 8.96 5.75 8.54
E2 qPH-5-6 Chr.5 c05b073-c05b074 30713393-30861542 3.69 2.51 3.53
qPH-6-3 Chr.6 c06b119-c06b120 32486143-32533796 5.62 3.29 6.40
qPH-9-17 Chr.9 c09b164-c09b165 49027777-49049868 3.35 2.49 3.42
qPH-9-10 Chr.9 c09b165-c09b166 49049868-49379087 3.40 2.42 3.31
T4—T5 E1 qPH-7-12 Chr.7 c07b103-c07b104 27561783-27659941 3.00 2.47 7.00
qPH-9-18 Chr.9 c09b177-c09b178 54969651-55252443 3.35 2.82 7.98
E2 qPH-1-5 Chr.1 c01b122-c01b123 34477733-34973198 3.02 -1.06 6.28

Fig. 3

Distribution of the main effect QTL on the whole genome for plant height in foxtail millet Black represents the unconditional main effect QTL; Green represents the conditional main effect QTL"

Fig. 4

GO and KEGG enrichment analysis of the QTL interval for the main effect of foxtail millet plant height A: GO enrichment analysis of multi-period major QTL; B: Multi-period major QTL KEGG metabolic pathway; C: GO enrichment analysis of single-period major QTL; D: Single-period major QTL KEGG metabolic pathway"

Table 5

Candidate genes within the confidence interval of major QTL for plant height"

数量性状位点
QTL		 染色体
Chromosome		 候选基因
Candidate genes		 GO注释
GO annotation		 拟南芥同源基因
Homologous genes in Arabidopsis		 功能注释
Functional annotation
qPH-2-2 Chr.2 Seita.2G366600.1 GO:0016020,
GO:0009765		 AT3G61470.1 捕光天线蛋白；叶绿素a/b结合蛋白2
LHCA2; light-harvesting complex I chlorophyll a/b binding protein 2
qPH-1-2 Chr.1 Seita.1G242300.1 GO:0055114,
GO:0016491		 AT4G21200.1 赤霉素2-氧化酶8 Gibberellin 2-oxidase 8
qPH-1-3 Chr.1 Seita.1G240300.1 AT2G37040.1 PHE解氨酶1 PHE ammonia lyase 1
Seita.1G240400.1 AT2G37040.1 PHE解氨酶1 PHE ammonia lyase 1
Seita.1G240500.1 AT2G37040.1 PHE解氨酶1 PHE ammonia lyase 1
Seita.1G240600.1 AT2G37040.1 PHE解氨酶1 PHE ammonia lyase 1
Seita.1G240200.1 AT2G37040.1 PHE解氨酶1 PHE ammonia lyase 1
Seita.1G238300.1 GO:0008152,
GO:0003824		 AT2G20420.1 ATP柠檬酸裂解酶（ACL）家族蛋白
ATP citrate lyase (ACL) family protein
qPH-2-1 Chr.2 Seita.2G183600.1 GO:0006412,
GO:0005840,
GO:0003735		 AT2G36170.1 泛素超群；核糖体蛋白L40e
Ubiquitin supergroup; Ribosomal protein L40e
Seita.2G183800.1 GO:0006412,
GO:0005840,
GO:0003735,
GO:0005515		 AT2G36170.1 泛素超群；核糖体蛋白L40e
Ubiquitin supergroup; Ribosomal protein L40e
Seita.2G183700.1 GO:0006412,
GO:0005840,
GO:0003735		 AT2G36170.1 泛素超群；核糖体蛋白L40e
Ubiquitin supergroup; Ribosomal protein L40e
Seita.2G185400.1 GO:0009058,
GO:0008909		 AT1G18870.1 异分支酸合酶2 Isochorismate synthase 2
qPH-3-5 Chr.3 Seita.3G329200.1 AT2G16920.1 泛素结合酶 23 Ubiquitin-conjugating enzyme 23
Seita.3G329400.1 AT2G16920.1 泛素结合酶 23 Ubiquitin-conjugating enzyme 23
Seita.3G329600.1 AT2G16920.1 泛素结合酶 23 Ubiquitin-conjugating enzyme 23
Seita.3G329800.1 AT2G16920.1 泛素结合酶 23 Ubiquitin-conjugating enzyme 23
Seita.3G329900.1 AT2G16920.1 泛素结合酶 23 Ubiquitin-conjugating enzyme 23
qPH-6-2 Chr.6 Seita.6G105300.1 GO:0055114,
GO:0051287,
GO:0016616		 AT5G15490.1 UDP-葡萄糖6-脱氢酶家族蛋白
UDP-glucose 6-dehydrogenase family protein
Seita.6G110200.1 GO:0016157,
GO:0005985		 AT5G20280.1 蔗糖磷酸合酶1F
Sucrose phosphate synthase 1F
Seita.6G105100.1 GO:0055114,
GO:0016616,
GO:0006694,
GO:0003854		 AT1G15950.1 肉桂酰基辅酶a还原酶1
Cinnamoyl coa reductase 1
qPH-7-5 Chr.7 Seita.7G234000.1 GO:0055114,
GO:0016491,
GO:0008270		 AT4G39330.1 肉桂醇脱氢酶9
Cinnamyl alcohol dehydrogenase 9
qPH-7-7 Chr.7 Seita.7G143300.1 GO:0031625,
GO:0006511		 AT2G04660.1 后期促进复合体/环体2
Anaphase-promoting complex/cyclosome 2
qPH-9-10 Chr.9 Seita.9G439100.1 GO:0008641 AT5G06460.1 泛素激活酶2 Ubiquitin activating enzyme 2
Seita.9G440900.1 GO:0006529,
GO:0004066		 AT5G65010.1 天冬酰胺合成酶2 Asparagine synthetase 2
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