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作物学报 ›› 2024, Vol. 50 ›› Issue (12): 2971-2983.doi: 10.3724/SP.J.1006.2024.44071

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

基于转录组分析的低铁胁迫下Bt棉苗杀虫蛋白表达量下降机制

王永慧(), 贺江, 张向向, 娄向弟, 高进, 孙艳茹, 曹婷, 施洋   

  1. 江苏沿海地区农业科学研究所 / 农业农村部沿海盐碱地农业科学观测实验站, 江苏盐城 224001
  • 收稿日期:2024-04-26 接受日期:2024-08-15 出版日期:2024-12-12 网络出版日期:2024-09-02
  • 通讯作者: *王永慧, E-mail: huiyw2008@163.com
  • 基金资助:
    国家自然科学基金项目(31501267);国家自然科学基金项目(CX(20)2065)

Mechanism of reduced insecticidal protein expression in Bt cotton under low-iron stress based on transcriptome analysis

WANG Yong-Hui(), HE Jiang, ZHANG Xiang-Xiang, LOU Xiang-Di, GAO Jing, SUN Yan-Ru, CAO Ting, SHI Yang   

  1. Institute of Agricultural Sciences of Jiangsu Coastal Area / Observation and Experimental Station of Saline land of Costal Area, Ministry of Agriculture and Rural Affairs, Yancheng 224001, Jiangsu, China
  • Received:2024-04-26 Accepted:2024-08-15 Published:2024-12-12 Published online:2024-09-02
  • Contact: *E-mail: huiyw2008@163.com
  • Supported by:
    National Natural Science Foundation of China(31501267);Jiangsu Agriculture Science and Technology Innovation Fund [(CX(20)2065)

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摘要：

研究低铁对Bt棉杀虫蛋白含量的影响及其生理和分子机制, 可为Bt棉抗虫性安全表达提供理论参考。本文以转基因抗虫棉品种中棉50为试验材料, 设置正常铁(CK, 20.0 μmol L-1)和低铁(LI, 0.1 μmol L-1) 2个铁水平处理, 采用水培法研究了低铁胁迫下Bt棉苗期Bt杀虫蛋白含量变化及氮代谢生理特征, 通过转录组测序挖掘差异表达基因及其相关代谢途径, 并采用qRT-PCR方法对测序结果进行验证。结果表明,与对照处理相比, 低铁胁迫下Bt棉根和叶片中杀虫蛋白含量显著下降, 且根中杀虫蛋白含量下降幅度更大。低铁胁迫降低了叶片中NH4+-N和NO3--N含量, 降低根和叶片中可溶性蛋白含量和全氮含量。根和叶片中硝酸还原酶、亚硝酸还原酶和谷氨酸合成酶活性的变化趋势与Bt杀虫蛋白含量表现一致。转录组结果表明, 根和叶片中分别鉴定出11,661个和8972个差异表达基因, 其中有1652个差异表达基因在根和叶片中均下调表达。GO注释表明, 低铁处理根和叶片中差异基因的功能都主要富集于刺激反应、细胞壁、质膜、结合、氧化还原活性等。KEGG富集分析显示, 苯丙烷类物质生物合成、苯丙氨酸代谢、半胱氨酸和蛋氨酸代谢、激素信号转导、玉米素生物合成、氮代谢、淀粉和蔗糖代谢、丙氨酸、天冬氨酸和谷氨酸代谢和酪氨酸代谢等途径在根和叶片中均发生显著变化。低铁胁迫下与氮素还原、同化途径相关的NR、NiR1和GLT1基因表达显著下调。以上结果表明, 低铁胁迫会抑制Bt棉氮代谢相关基因的转录水平, 减弱氮代谢的生理活性, 抑制Bt杀虫蛋白的合成。

关键词: Bt棉, 杀虫蛋白, 低铁胁迫, 转录组

Abstract:

To provide a theoretical basis for the safety of insecticidal efficiency in Bt cotton, this study investigated the effects of low iron on Bt insecticidal protein content and the physiological and molecular mechanisms in Bt cotton. Transgenic Bt cotton cultivar Zhongmian 50 was grown under low iron (LI, 0.1 μmol L-1 Fe(II)-EDTA) and normal iron (CK, 20.0 μmol L-1 Fe(II)-EDTA) conditions in hydroponic culture to assess the impact of low iron stress on Bt insecticidal protein content, activities of nitrogen metabolism-related enzymes, and substances in cotton seedlings. Differentially expressed genes (DEGs) were screened, and their relative expression patterns were analyzed by high-throughput sequencing, with results verified by qRT-PCR. The results showed that, compared with the control, the insecticidal protein contents significantly decreased under low iron conditions, with a more pronounced reduction in roots than in leaves. Iron deficiency decreased NH4+-N and NO3--N levels in leaves and reduced soluble protein and nitrogen contents in both roots and leaves. Significant reductions in the activities of nitrate reductase (NR), nitrite reductase (NiR), and glutamine synthetase (GS) were observed when Bt insecticidal protein contents in roots and leaves were significantly reduced. High-throughput sequencing identified 11,661 DEGs in roots and 8972 in leaves, with 1652 genes down-regulated in both organs. GO annotation revealed that the functions of the differential genes in two organs were mainly concentrated in response to stimulus, cell wall, plasma membrane, binding, and catalytic activity. KEGG enrichment analysis demonstrated significant changes in phenylpropanoid biosynthesis, phenylalanine metabolism, cysteine and methionine metabolism, plant hormone signal transduction, zeatin biosynthesis, nitrogen metabolism, starch and sucrose metabolism, alanine, aspartate and glutamate metabolism, and tyrosine metabolism in both roots and leaves. Genes coding for NR, NiR1, and GLT1 related to the nitrogen reduction and assimilation pathway were significantly down-regulated under iron deficiency treatment. Therefore, low iron stress inhibits the transcription levels of genes related to nitrogen metabolism in Bt cotton, weakens the physiological activities of nitrogen metabolism, and subsequently reduces Bt insecticidal protein.

Key words: Bt cotton, insecticidal protein, low iron, transcriptome

表1

实时荧光定量引物"

基因名称
Gene name		 正向引物
Forward sequence (5′-3′)		 反向引物
Reverse sequence (5′-3′)		 基因 ID
Gene ID
ACT14 CTGGAGACTGCCAAGAGCAGCT CCGGGCAACGGAATCTCTCAGC
NR GAGCATATCCCGGTGGGTTC GCTGCACAGCGAACTGAATC Gh_D02G0815
NiR1 GGGGCAGACATATTCTTGGGA AGCTCCAAAGTGTTCCACCA Gh_A13G0352
GS1.1 CAATTCGTGTTGGGCGAGAC CAAACATGGGCTTCCCCTCA Gh_A13G0512
GLT1 CGGAGGCTTGTGCTGAGTAT TCTGTACAGTGTGGGGCAAG Gh_D12G2422

图1

低铁对Bt棉根和叶片干物重及铁离子含量影响 A: 低铁对Bt棉根和叶片干物重影响; B: 低铁对Bt棉根和叶片铁离子含量影响。CK: 对照处理; LI: 低铁处理。不同小写字母表示处理间差异显著(P < 0.05)。"

图2

低铁对Bt棉根和叶片中杀虫蛋白含量影响 处理同图1。不同小写字母表示处理间差异显著(P < 0.05)。"

表2

低铁胁迫对Bt棉根和叶片中硝酸还原酶、亚硝酸还原酶、谷氨酰胺合成酶和谷氨酸合成酶活性的影响"

器官/处理
Organ/ treatment		 硝酸还原酶活性
Nitrate reductase activities
(μmol g-1 h-1)		 亚硝酸还原酶活性
Nitrite reductase activities
(μmol g-1 h-1)		 谷氨酰胺合成酶活性
Glutamine synthetase
activities
(ΔA g-1 h-1)		 谷氨酸合成酶活性
Glutamate synthase activities
(µmol g-1 min-1)
根系Root
CK 3.35 a 7.85 a 0.77 a 0.76 a
LI 2.79 b 6.97 b 0.34 b 0.44 b
叶片Leaf
CK 5.13 a 10.82 a 0.86 a 1.02 a
LI 3.54 b 9.03 b 0.83 a 0.81 b

表3

低铁胁迫对Bt棉根和叶片中铵态氮、硝态氮、可溶性蛋白和全氮含量的影响"

器官/处理
Organ/ treatment		 铵态氮
NH4+-N
(μg g-1 FW)		 硝态氮
NO3--N
(μmol g-1 FW)		 可溶性蛋白含量
Soluble protein content
(mg g-1 FW)		 全氮含量
N content
(mg g-1 DW)
根系Root
CK 6.6 a 13.4 a 12.7 a 41.4 a
LI 6.8 a 14.1 a 9.3 b 35.8 b
叶片Leaf
CK 13.2 a 26.4 a 21.3 a 57.1 a
LI 10.3 b 17.6 b 17.8 b 51.8 b

表4

转录组测序基础数据统计分析"

样品
Sample		 原始数据
Raw reads		 有效数据
Clean reads		 总映射率
Total mapped rate (%)		 唯一映射率
Uniquely mapped rate (%)		 Q30
(%)		 GC 含量
GC content (%)
RCK_1 46,179,118 45,290,042 98.13 93.01 94.27 42.77
RCK_2 47,909,866 46,989,512 98.17 93.05 94.05 42.76
RCK_3 46,776,936 45,955,806 98.20 93.17 94.41 42.73
RLI_1 36,534,072 35,735,176 96.03 92.59 94.18 43.28
RLI_2 42,611,888 41,690,972 96.02 92.72 94.18 43.29
RID_3 36,994,328 36,155,932 95.98 92.77 94.03 43.30
LCK_1 47,984,028 47,017,502 98.50 91.19 94.25 44.13
LCK_2 54,041,314 53,158,296 98.55 92.01 94.24 44.13
LCK_3 45,829,824 44,978,082 98.55 91.28 94.13 44.15
LLI_1 37,090,636 36,270,280 98.48 91.46 94.09 43.65
LLI_2 46,722,582 45,791,778 98.49 91.67 94.26 43.65
LLI_3 50,516,840 49,554,758 98.46 91.53 94.34 43.62

图3

低铁胁迫下差异表达的基因 A: 上调和下调的DEG数量; B: 差异表达基因Venn图。缩写同表4。"

表5

差异表达基因的GO注释"

GO号
GO ID		 GO功能
GO function		 总基因数目
Total numbers		 RCK vs RLI
差异基因数目
DEG numbers in
RCK vs RLI		 LCK vs LLI
差异基因数目
DEG numbers in
LCK vs LLI		 GO类别
Category
GO:0071555 细胞壁组织
Cell wall organization		 1433 349 319 BP
GO:0071554 细胞壁组织或生物发生
Cell wall organization or biogenesis		 1904 447 398 BP
GO:0050896 刺激反应
Response to stimulus		 15,817 3040 2434 BP
GO:0009725 对激素的反应
Response to hormone		 5317 1134 885 BP
GO:0055072 铁离子平衡
Iron ion homeostasis		 148 62 50 BP
GO:0005576 胞外区
Extracellular region		 2833 733 588 CC
GO:0071944 细胞外围
Cell periphery		 9137 1803 1528 CC
GO:0030312 外部封装结构
External encapsulating structure		 1816 466 387 CC
GO:0005618 细胞壁
Cell wall		 1775 453 375 CC
GO:0005886 质膜
Plasma membrane		 7785 1470 1263 CC
GO:0031226 质膜的内在成分
Intrinsic component of plasma membrane		 922 237 224 CC
GO:0031224 膜的内在成分
Intrinsic component of membrane		 10,103 1841 1646 CC
GO:0031225 膜锚定组件
Anchored component of membrane		 412 122 125 CC
GO:0003700 DNA结合转录因子活性
DNA-binding transcription factor activity		 3821 899 644 MF
GO:0016491 氧化还原酶活性
Oxidoreductase activity		 3512 827 671 MF
GO:0046906 四吡咯结合
Tetrapyrrole binding		 863 246 194 MF
GO:0020037 血红素结合
Heme binding		 736 236 156 MF

图4

KEGG通路富集散点图 缩写同表4。"

图5

氮素转运相关差异基因表达热图 缩写同表4。"

表6

氮代谢途径中差异基因表达分析"

基因ID
Gene ID		 基因功能注释
Gene function annotation		 调控Regulation 基因名称
Gene name
RCK vs RLI LCK vs LLI
Gh_D02G0815 硝酸还原酶[NADH]
Nitrate reductase [NADH]		 ↓ ↓ NR
Gh_A02G0769 硝酸还原酶[NADH]
Nitrate reductase [NADH]		 ↓ ↓ NR
Gh_A01G1586 硝酸还原酶[NADH]
Nitrate reductase [NADH]		 -- ↓ NR
Gh_D01G1872 硝酸还原酶[NADH]
Nitrate reductase [NADH]		 ↑ ↓ NR
Gh_A13G0352 铁氧还蛋白-亚硝酸盐还原酶, 叶绿体 ↓ ↓ NiR1
Ferredoxin-nitrite reductase, chloroplastic
Gh_D07G1773 谷氨酰胺合成酶, 胞质同工酶1 ↑ ↑ GS1;1
Glutamine synthetase, cytosolic isozyme 1
Gh_A13G0512 谷氨酰胺合成酶, 胞质同工酶1 ↑ ↑ GS1;1
Glutamine synthetase, cytosolic isozyme 1
Gh_D13G0620 谷氨酰胺合成酶, 胞质同工酶1 -- ↑ GS1;1
Glutamine synthetase, cytosolic isozyme 1
Gh_D11G3479 谷氨酰胺合成酶, 结节同工酶 ↑ ↓ GS
Glutamine synthetase, nodule isozyme
Gh_D09G1909 谷氨酰胺合成酶, 叶同工酶, 叶绿体 ↓ -- GS
Glutamine synthetase, leaf isozyme, chloroplastic
Gh_A09G1788 谷氨酰胺合成酶, 叶同工酶, 叶绿体 ↓ -- GS
Glutamine synthetase, leaf isozyme, chloroplastic
Gh_D12G2422 谷氨酸合成酶 1 [NADH], 叶绿体 ↓ ↓ GLT1
Glutamate synthase 1 [NADH], chloroplastic
Gh_A12G2272 谷氨酸合成酶 1 [NADH], 叶绿体 ↓ -- GLT1
Glutamate synthase 1 [NADH], chloroplastic

图6

差异基因qRT-PCR验证"

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