甘蓝型油菜盐胁迫响应基因表达谱分析及共表达网络的构建

doi:10.3724/SP.J.1006.2024.34076

Abstract

Abstract:

Brassica napus L. is an important oil crop. Salt stress is one of the major environmental conditions affecting the growth and development of B. napus, which may lead to yield reduction, quality deterioration, and even the death of B. napus. In this study, the B. napus semi-winter cultivar ZS11 was used as the experimental material to perform transcriptome sequencing on the leaf and root tissues with salt stress treatment (0, 0.25, 0.5, 1, 3, 6, 12, and 24 h). The measured 90 RNA-seq data provided the high-resolution time dynamic transcriptional expression spectrum of rapeseed tissues responding to salt stress was obtained. Correlation analysis showed that the samples exhibited significant clustering differences in early response and late response before and after 1 h salt stress treatment. Using DESeq2 for differential gene analysis, we identified 20,462 and 29,334 differential genes for the response of root and leaf tissues, respectively, indicating that the overall response of leaf tissue in rapeseed was more severe than the root. Furthermore, WGCNA was used to construct gene co-expression networks for the salt stress response in root and leaf tissues, respectively, and tan and yellow modules were significantly related to the early response to salt stress, and green and red modules were significantly related to the late response to salt stress. GO enrichment analysis was then performed, and 41 and 26 core transcription factors responding to salt stress at the early and late stages, respectively, were selected from these networks. Functional annotation showed that the known Arabidopsis homologous genes involved in salt stress responses at different stages existed in all four modules, and core genes, such as BnWRKY46 and BnWRKY57, had abundant SNPs variation and haplotypes in 505 salt stress-treated rape population variation data, suggesting that these core transcription factors might be key candidate genes for rape salt stress response. This study provides a reliable data reference and candidate gene resources for improving salt tolerance in B. napus.

Key words: Brassica napus L., RNA-seq, salt stress, WGCNA, gene co-expression networks

YANG Chuang, WANG Ling, QUAN Cheng-Tao, YU Liang-Qian, DAI Cheng, GUO Liang, FU Ting-Dong, MA Chao-Zhi. Relative expression profiles of genes response to salt stress and constructions of gene co-expression networks in Brassica napus L.[J].Acta Agronomica Sinica, 2024, 50(1): 237-250.

Figures/Tables 13

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Table S1

Table S2

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Table S3

Functional annotation of core transcription factors in hub modules"

关键模块 Hub modules	核心转录因子 Core transcription factors	基因别名 Gene aliases	基因名字 Gene names	基因注释 Gene annotation
tan	BnaA03G0475900ZS	WRKY53	AT4G23810	WRKY转录因子家族成员，是叶绿素合成/降解、衰老和气孔导度的拮抗调节因子。
				A member of WRKY transcription factor family which is antagonistic regulators of chlorophyll synthesis/degradation, senescence, and stomatal conductance.
tan	BnaC07G0058300ZS	NAC036	AT2G17040	NAC转录因子家族成员，参与叶和花序茎的形态建成。
				A member of the NAC transcription factor family involved in leaf and inflorescence stem morphogenesis.
tan	BnaC03G0795800ZS	ERF4	AT3G15210	作为JA应答防御基因和对坏死性真菌病原体尖孢镰刀菌抗性的负调节因子，可拮抗JA对根伸长的抑制作用。
				Acts as a negative regulator of JA-responsive defense gene expression and resistance to the necrotrophic fungal pathogen Fusarium oxysporum and antagonizes JA inhibition of root elongation.
tan	BnaA01G0133900ZS	WRKY53	AT4G23810	WRKY转录因子家族成员，是叶绿素合成/降解、衰老和气孔导度的拮抗调节因子。
				A member of WRKY transcription factor family which is antagonistic regulators of chlorophyll synthesis/degradation, senescence, and stomatal conductance.
tan	BnaC01G0172400ZS	WRKY53	AT4G23810	WRKY转录因子家族成员，是叶绿素合成/降解、衰老和气孔导度的拮抗调节因子。
				A member of WRKY transcription factor family which is antagonistic regulators of chlorophyll synthesis/degradation, senescence, and stomatal conductance.
tan	BnaC07G0454200ZS	WRKY53	AT4G23810	WRKY转录因子家族成员，是叶绿素合成/降解、衰老和气孔导度的拮抗调节因子。
				A member of WRKY transcription factor family。
tan	BnaA09G0423300ZS	ERF11	AT1G28370	ERF/AP2转录因子家族中ERF亚家族B-1的一员，该蛋白含有一个AP2结构域。
				A member of the ERF subfamily B-1 of ERF/AP2 transcription factor family which contains one AP2 domain.
tan	BnaC03G0651000ZS	ERF11	AT1G28370	ERF/AP2转录因子家族中ERF亚家族B-1的一员，该蛋白含有一个AP2结构域。
				A member of the ERF subfamily B-1 of ERF/AP2 transcription factor family which contains one AP2 domain.
tan	BnaC03G0042100ZS	NAC081	AT5G08790	具有NAC结构域的假定转录激活因子的大家族成员，可由创伤诱导表达。
				A large family member of putative transcriptional activators with NAC domain, which can be Induced by wounding.
tan	BnaA04G0247200ZS	WRKY33	AT2G38470	WRKY转录因子家族成员，参与对各种非生物胁迫尤其是盐胁迫的反应。能控制根中凋亡屏障的形成，从而赋予耐盐性。
				A member of WRKY transcription factor family. Involved in response to various abiotic stresses especially salt stress.Control apoplastic barrier formation in roots to confer salt tolerance.
tan	BnaC03G0217300ZS	WRKY33	AT2G38470	参与对各种非生物胁迫尤其是盐胁迫的反应。
				Involved in response to various abiotic stresses especially salt stress.
tan	BnaA06G0417500ZS	ERF5	AT5G47230	ERF/AP2转录因子家族(ATERF-5)的ERF亚家族B-3的成员。
				A member of the ERF subfamily B-3 of ERF/AP2 transcription factor family (ATERF-5).
tan	BnaA03G0185200ZS	WRKY33	AT2G38470	WRKY转录因子家族成员，参与对各种非生物胁迫尤其是盐胁迫的反应。
				A member of the plant WRKY transcription factor family. Involved in response to various abiotic stresses - especially salt stress.
tan	BnaA08G0213700ZS	ERF11	AT1G28370	ERF/AP2转录因子家族中ERF亚家族B-1的一员。
				A member of the ERF subfamily B-1 of ERF/AP2 transcription factor family.
tan	BnaC04G0562300ZS	WRKY33	AT2G38470	参与对各种非生物胁迫尤其是盐胁迫的反应。
				Involved in response to various abiotic stresses especially salt stress.
yellow	BnaC09G0432800ZS	ZAT12	AT5G59820	锌指蛋白，参与高光和冷适应。
				A zinc finger protein involved in high light and cold acclimation.
yellow	BnaC08G0297500ZS	NAC062	AT3G49530	作为冷信号和病原体抗性反应之间分子链接的转录因子。
				Transcription factor that serves as a molecular link between cold signals and pathogen resistance responses.
yellow	BnaC02G0323100ZS	WRKY40	AT1G80840	病原体诱导转录因子，与WRKY18或WRKY60共表达会使植物对丁香假单胞菌和灰霉病菌更敏感。
				Pathogen-induced transcription factor. Coexpression with WRKY18 or WRKY60 made plants more susceptible to both P. syringae and B. cinerea.
yellow	BnaA03G0475900ZS	WRKY53	AT4G23810	WRKY转录因子家族成员，是叶绿素合成/降解、衰老和气孔导度的拮抗调节因子。
				A member of WRKY transcription factor family which is antagonistic regulators of chlorophyll synthesis/degradation, senescence, and stomatal conductance.
yellow	BnaA08G0015900ZS	ERF8	AT1G53170	ERF/AP2转录因子家族(ATERF-8)ERF亚家族B-1的一个成员，这种蛋白质含有一个AP2结构域。
				A member of the ERF subfamily B-1 of ERF/AP2 transcription factor family (ATERF-8). The protein contains one AP2 domain.
yellow	BnaC05G0100700ZS	DDF1	AT1G12610	ERF/AP2转录因子家族(DD f1)DREB亚家族A-1的一个成员。这种蛋白质含有一个AP2结构域。该亚家族有6个成员，包括CBF1、CBF2和CBF3。该基因的过表达导致延迟开花和矮化，赤霉酸生物合成减少，以及对高水平盐的耐受性增加。
				A member of the DREB subfamily A-1 of ERF/AP2 transcription factor family (DDF1). The protein contains one AP2 domain. There are six members in this subfamily, including CBF1, CBF2, and CBF3. Overexpression of this gene results in delayed flowering and dwarfism, reduction of gibberellic acid biosynthesis, and increased tolerance to high levels of salt.
yellow	BnaC07G0454200ZS	WRKY53	AT4G23810	WRKY转录因子家族成员，是叶绿素合成/降解、衰老和气孔导度的拮抗调节因子
				A member of WRKY transcription factor family which is antagonistic regulators of chlorophyll synthesis/degradation, senescence, and stomatal conductance.
yellow	BnaA01G0133900ZS	WRKY53	AT4G23810	WRKY转录因子家族成员，是叶绿素合成/降解、衰老和气孔导度的拮抗调节因子
				A member of WRKY transcription factor family which is antagonistic regulators of chlorophyll synthesis/degradation, senescence, and stomatal conductance.
yellow	BnaC03G0795800ZS	ERF4	AT3G15210	作为JA反应性防御应答基因和对坏死性真菌病原体尖孢镰刀菌抗性的负调节因子，能拮抗JA对根伸长的抑制作用。
				Acts as a negative regulator of JA-responsive defense gene expression and resistance to the necrotrophic fungal pathogen Fusarium oxysporum and antagonizes JA inhibition of root elongation.
yellow	BnaA06G0329700ZS	NAC091	AT5G24590	NAC转录因子家族成员,参与调节拟南芥对TCV病毒的防御反应。
				A member of NAC transcription factor family involved in regulating the defense response of Arabidopsis to turnip crinkle virus (TCV).
yellow	BnaC04G0080600ZS	WRKY33	AT2G38470	参与应对各种非生物胁迫，尤其是盐胁迫。
				Involved in response to various abiotic stresses especially salt stress.
yellow	BnaA06G0356400ZS	WRKY48	AT5G49520	一种胁迫和病原体诱导的转录激活因子，会抑制植物的基础防御。
				A stress- and pathogen-induced transcriptional activator that represses plant basal defense.
yellow	BnaC05G0398500ZS	AZF2	AT3G19580	锌指蛋白家族成员，其mRNA水平在响应ABA、高盐和轻度脱水时会上调表达。
				A member of zinc finger protein family whose mRNA levels are upregulated in response to ABA, high salt, and mild desiccation.
yellow	BnaA09G0110600ZS	NAC036	AT2G17040	NAC转录因子家族成员，参与叶和花序茎的形态发生。
				A member of the NAC transcription factor family that involved in leaf and inflorescence stem morphogenesis.
yellow	BnaC09G0112900ZS	NAC036	AT2G17040	NAC转录因子家族成员，参与叶和花序茎的形态发生。
				A member of the NAC transcription factor family involved in leaf and inflorescence stem morphogenesis.
yellow	BnaC07G0433500ZS	LSD1	AT4G20380	锌指蛋白家族成员,负调节基础防御途径,监控超氧化物依赖性信号并负调节植物细胞死亡途径。
				A member of zinc finger family protein that negatively regulates a basal defense pathway, monitors a superoxide-dependent signal and negatively regulates a plant cell death pathway.
yellow	BnaC03G0563400ZS	NAC062	AT3G49530	NAC转录因子家族成员,作为冷信号和病原体抗性反应之间分子链接。
				A member of the NAC transcription factor family that serves as a molecular link between cold signals and pathogen resistance responses.
yellow	BnaC05G0161100ZS	ERF017	AT1G19210	ERF/AP2转录因子家族的DREB亚家族A-5的一个成员,这种蛋白质含有一个AP2结构域。
				A member of the DREB subfamily A-5 of ERF/AP2 transcription factor family. The protein contains one AP2 domain.
yellow	BnaC04G0512500ZS	POSF21	AT2G31370	碱性亮氨酸拉链(bZIP)转录因子家族蛋白。
				Basic-leucine zipper (bZIP) transcription factor family protein.
yellow	BnaA07G0269000ZS	MYBD	AT1G70000	MYB样结构域转录因子，在响应光和细胞分裂素的花青素积累中发挥正调控作用。
				A MYB-like Domain transcription factor that plays a positive role in anthocyanin accumulation in response to light and cytokinin.
yellow	BnaA03G0321600ZS	DREB2B	AT3G11020	ERF/AP2转录因子家族(DREB2B)的DREB亚家族A-2的成员。这种蛋白质含有一个AP2结构域。
				A member of the DREB subfamily A-2 of ERF/AP2 transcription factor family (DREB2B). The protein contains one AP2 domain.
yellow	BnaC03G0264000ZS	WRKY46	AT2G46400	WRKY转录因子，通过调节ABA信号和生长素体内平衡对渗透/盐胁迫依赖性LR抑制进行前馈抑制。
				A WRKY transcription factor that contributes to the feedforward inhibition of osmotic/salt stress-dependent LR inhibition via regulation of ABA signaling and auxin homeostasis.
yellow	BnaA02G0116700ZS	MYB36	AT5G57620	MYB转录因子家族成员，在根发育过程中促进内皮层的分化。
				A member of MYB transcriptional factor family that acts to promote differentiation of the endodermis during root development.
yellow	BnaA04G0034100ZS	BHLH107	AT3G56770	碱性螺旋-环-螺旋(bHLH) DNA结合超家族蛋白质。
				basic helix-loop-helix (bHLH) DNA-binding superfamily protein.
yellow	BnaA06G0158600ZS	NAC062	AT3G49530	NAC转录因子家族成员,作为冷信号和病原体抗性反应之间分子链接。
				A member of the NAC transcription factor family that serves as a molecular link between cold signals and pathogen resistance responses.
yellow	BnaA06G0081500ZS	DDF1	AT1G12610	ERF/AP2转录因子家族(DD f1)DREB亚家族A-1的一个成员,该基因的过表达导致延迟开花和矮化，对高水平盐的耐受性增加。
				A member of the DREB subfamily A-1 of ERF/AP2 transcription factor family (DDF1). Overexpression of this gene results in delayed flowering and dwarfism, and increased tolerance to high levels of salt.
green	BnaA05G0016800ZS	GBF3	AT2G46270	一种bZIP G盒结合蛋白，其表达受ABA、寒冷和缺水诱导。
				A bZIP G-box binding protein, induced by ABA, cold and water deprivation.
green	BnaC03G0260300ZS	SOC1	AT2G45660	控制开花，是一氧化碳促进开花所必需的。
				Controls flowering and is required for CO to promote flowering.
green	BnaC05G0560000ZS	ATHB-1	AT3G01470	一个参与叶和下胚轴发育的同源结构域亮氨酸拉链I类(HD-Zip I)转录激活因子。
				A homeodomain leucine zipper class I (HD-Zip I) transcriptional activator involved in leaf and hypocotyl development.
green	BnaA07G0347200ZS	ATY13	AT1G74650	R2R3因子基因家族成员;与生殖发育有关的蜡调节因子。
				A member of the R2R3 factor gene family; wax regulator associated with reproductive development.
green	BnaC01G0510700ZS	NAC047	AT3G04070	含NAC结构域的蛋白47。
				NAC domain containing protein 47.
green	BnaA09G0409000ZS	NFYA7	AT1G30500	核因子Y，亚单位A7。
				nuclear factor Y, subunit A7.
green	BnaA01G0191600ZS	ARR1	AT3G16857	一种拟南芥反应调节蛋白(ARR )，在细胞分裂素信号途径中与其他B型ARR协同作用。还参与细胞分裂素依赖的下胚轴伸长抑制和细胞分裂素依赖的组织培养中的绿化和抽芽。ARR1、ARR10和ARR12是干旱反应的冗余调节因子，其中ARR1最为关键。
				An Arabidopsis response regulator (ARR) protein that acts in concert with other type-B ARRs in the cytokinin signaling pathway. Also involved in cytokinin-dependent inhibition of hypocotyl elongation and cytokinin-dependent greening and shooting in tissue culture. ARR1, ARR10, and ARR12 are redundant regulators of drought response, with ARR1 being the most critical.
green	BnaC04G0017100ZS	GBF3	AT2G46270	一种bZIP G盒结合蛋白，受ABA、寒冷和缺水诱导。
				A bZIP G-box binding protein induced by ABA, cold and water deprivation.
green	BnaC06G0084400ZS	NFYA5	AT1G54160	CBF-B/NF-YA转录因子家族的成员。响应ABA和干旱，功能丧失突变对干旱高度敏感。
				A member of the CBF-B/NF-YA transcription factor family. Expression is upregulated in response to ABA and drought. Loss of function mutations are hypersensitive to drought.
green	BnaA01G0036700ZS	ATB2	AT4G34590	碱性结构域亮氨酸拉链(bZIP)转录因子bZIP11。蔗糖抑制翻译，导致uORF2中的核糖体停滞。直接调节参与氨基酸代谢的酶编码基因ASN1和ProDH2的基因表达。
				A basic domain leucine zipper (bZIP) transcription factor bZIP11. Translation is repressed by sucrose that results in ribosome stalling in the uORF2. Directly regulates gene expression of ASN1 and ProDH2, which are enzyme-coding genes involved in amino acid metabolism.
green	BnaC05G0008500ZS	——	AT1G01250	ERF/AP2转录因子家族的DREB亚家族A-4的成员。这种蛋白质含有一个AP2结构域。
				A member of the DREB subfamily A-4 of ERF/AP2 transcription factor family. The protein contains one AP2 domain.
green	BnaA09G0663800ZS	NFYC9	AT1G08970	核因子Y C (NF-YC)同系物NF-YC9，调节GA和ABA介导的种子萌发。
				A NUCLEAR FACTOR-Y C (NF-YC) homologue NF-YC9 that modulate GA- and ABA-mediated seed germination.
green	BnaC09G0556700ZS	FLC	AT5G10140	由开花基因座C转录因子编码的MADS-box蛋白，作为花转变的阻遏物并有助于昼夜节律钟的温度补偿。冷处理过程中表达下调。春化、FRI和自主途径都会影响FLC染色质的状态。在体内与SOC1和FT染色质相互作用。
				MADS-box protein encoded by FLOWERING LOCUS C - transcription factor that functions as a repressor of floral transition and contributes to temperature compensation of the circadian clock. Expression is downregulated during cold treatment. The small RNAs are most likely derived from an antisense transcript of FLC. Interacts with SOC1 in vivo.
green	BnaC07G0522500ZS	GATA3	AT4G34680	锌指转录因子GATA因子家族成员。
				A member of the GATA factor family of zinc finger transcription factors.
red	BnaA02G0180600ZS	WRKY57	AT1G69310	WRKY转录因子成员。WRKY57的激活赋予了耐旱性。
				A member of the WRKY Transcription Factor. Activation of WRKY57 confers drought tolerance.
red	BnaC02G0139100ZS	LRL3	AT5G58010	调节根毛发育的碱性螺旋-环-螺旋(bHLH)蛋白。
				A basic helix-loop-helix (bHLH) protein that regulates root hair development.
red	BnaA03G0557900ZS	ATHB40	AT4G36740	同源结构域亮氨酸拉链I类(HD-Zip I)蛋白。
				A homeodomain leucine zipper class I (HD-Zip I) protein.
red	BnaA09G0422600ZS	NAC010	AT1G28470	含NAC结构域的蛋白10。
				NAC domain containing protein 10.
red	BnaC07G0322500ZS	MYB121	AT3G30210	R2R3因子基因家族成员。
				A member of the R2R3 factor gene family.
red	BnaA05G0156300ZS	NFYA5	AT1G54160	CCAAT结合转录因子(CBF-B/NF-YA)家族的成员。响应ABA和干旱。
				A member of the CCAAT-binding transcription factor (CBF-B/NF-YA) family. Expression is upregulated in response to ABA and drought.
red	BnaA07G0311300ZS	ZFHD1	AT1G69600	锌指同源结构域转录因子家族成员ZFHD1。干旱、高盐和脱落酸诱导ZFHD1的表达。
				A member of the zinc finger homeodomain transcriptional factor family. Expression of ZFHD1 is induced by drought, high salinity and abscisic acid.
red	BnaA08G0184300ZS	ATHB40	AT4G36740	同源结构域亮氨酸拉链I类(HD-Zip I)蛋白。
				A homeodomain leucine zipper class I (HD-Zip I) protein.
red	BnaC06G0308100ZS	WRKY57	AT1G69310	WRKY转录因子成员。WRKY57的激活赋予了耐旱性。
				A member of the WRKY Transcription Factor. Activation of WRKY57 confers drought tolerance.
red	BnaC08G0452900ZS	SRS3	AT2G21400	SHI基因家族成员，能促进拟南芥中雌蕊、雄蕊和叶的发育。
				A member of SHI gene family that promote gynoecium, stamen and leaf development in Arabidopsis.
red	BnaA07G0271900ZS	WRKY57	AT1G69310	WRKY转录因子成员。WRKY57的激活赋予了耐旱性。
				A member of the WRKY Transcription Factor. Activation of WRKY57 confers drought tolerance.
red	BnaC09G0556700ZS	FLC	AT5G10140	冷处理过程中表达下调。
				Expression is downregulated during cold treatment.

Table S3

Fig. 10

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模块 Module	基因数目(转录因子数目) Gene_number (TF_number)	模块 Module	基因数目(转录因子数目) Gene_number (TF_number)
cyan	198 (18)	blue	4945 (209)
salmon	242 (36)	pink	775 (22)
green	1654 (138)	purple	466 (59)
red	1148 (73)	tan	260 (75)
turquoise	8651 (559)	black	801 (27)
greenyellow	405 (33)	magenta	556 (45)
brown	3510 (291)	yellow	3101 (184)

模块 Module	基因数目(转录因子数目) Gene_number (TF_number)	模块 Module	基因数目(转录因子数目) Gene_numbe (TF_number)
greenyellow	234 (27)	yellow	2322 (276)
pink	824 (85)	purple	365 (12)
brown	2515 (134)	red	1238 (99)
green	2077 (195)	black	1066 (89)
magenta	651 (41)	turquoise	4058 (393)
blue	3590 (426)

Relative expression profiles of genes response to salt stress and constructions of gene co-expression networks in Brassica napus L.

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