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

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Table S1

Table S2

Fig. 6

Fig. 7

Fig. 8

Fig. 9

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

References 60

[1]	Hazell P, Wood S. Drivers of change in global agriculture. Philosoph Trans Royal Soc B Biol Sci, 2008, 363: 495-515.
[2]	Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas R J, Drechsel P, Noble A D. Economics of salt-induced land degradation and restoration. Nat Resour Forum, 2014, 38: 282-295. doi: 10.1111/narf.2014.38.issue-4
[3]	Park H J, Kim W Y, Yun D J. A new insight of salt stress signaling in plant. Mol Cells, 2016, 39: 447-459. doi: 10.14348/molcells.2016.0083 pmid: 27239814
[4]	Munns R. Comparative physiology of salt and water stress. Plant Cell Environ, 2002, 25: 239-250. doi: 10.1046/j.0016-8025.2001.00808.x
[5]	Tyerman S D, Munns R, Fricke W, Arsova B, Barkla B J, Bose J, Bramley H, Byrt C, Chen Z, Colmer T D, Cuin T, Day D A, Foster K J, Gilliham M, Henderson S W, Horie T, Jenkins C L D, Kaiser B N, Katsuhara M, Plett D, Miklavcic S J, Roy S J, Rubio F, Shabala S, Shelden M, Soole K, Taylor N L, Tester M, Watt M, Wege S, Wegner L H, Wen Z. Energy costs of salinity tolerance in crop plants. New Phytol, 2019, 221: 25-29. doi: 10.1111/nph.15555 pmid: 30488600
[6]	杨劲松, 姚荣江, 王相平, 谢文萍, 张新, 朱伟, 张璐, 孙瑞娟. 中国盐渍土研究: 历程、现状与展望. 土壤学报, 2022, 59: 10-27.
	Yang J S, Yao R J, Wang X P, Xie W P, Zhang X, Zhu W, Zhang L, Sun R J. Research on salt-affected soils in China: history, status quo and prospect. Acta Pedol Sin, 2022, 59: 10-27. (in Chinese with English abstract)
[7]	刘成, 冯中朝, 肖唐华, 马晓敏, 周广生, 黄凤洪, 李加纳, 王汉中. 我国油菜产业发展现状、潜力及对策. 中国油料作物学报, 2019, 41: 485-489. doi: 10.7505/j.issn.1007-9084.2019.04.001
	Liu C, Feng Z C, Xiao T H, Ma X M, Zhou G S, Huang F H, Li J N, Wang H Z. Development, potential and adaptation of Chinese rapeseed industry. Chin J Oil Crop Sci, 2019, 41: 485-489. (in Chinese with English abstract) doi: 10.7505/j.issn.1007-9084.2019.04.001
[8]	何微, 李俊, 王晓梅, 林巧, 杨小薇. 全球油菜产业现状与我国油菜产业问题、对策. 中国油脂, 2022, 47(2): 1-7.
	He W, Li J, Wang X M, Lin Q, Yang X W. Current status of global rapeseed industry and problems, countermeasures of rapeseed industry in China. Chin Oils Fats, 2022, 47(2): 1-7. (in Chinese with English abstract)
[9]	Kumar K, Kumar M, Kim S R, Ryu H, Cho Y G. Insights into genomics of salt stress response in rice. Rice, 2013, 6: 27-39. doi: 10.1186/1939-8433-6-27 pmid: 24280112
[10]	Zhang H, Jiang C, Lei J, Dong J, Ren J, Shi X, Zhong C, Wang X, Zhao X, Yu H. Comparative physiological and transcriptomic analyses reveal key regulatory networks and potential hub genes controlling peanut chilling tolerance. Genomics, 2022, 114: 110285. doi: 10.1016/j.ygeno.2022.110285
[11]	Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C, Zhang J, Theprungsirikul L, Shrift T, Krichilsky B, Johnson D M, Swift G B, He Y, Siedow J N, Pei Z M. OSCA1 mediates osmotic-stress-evoked Ca²⁺ increases vital for osmosensing in Arabidopsis. Nature, 2014, 514: 367-371.
[12]	Hamilton E S, Jensen G S, Maksaev G, Katims A, Sherp A M, Haswell E S. Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science, 2015, 350: 438-441. doi: 10.1126/science.aac6014 pmid: 26494758
[13]	Jiang Z, Zhou X, Tao M, Yuan F, Liu L, Wu F, Wu X, Xiang Y, Niu Y, Liu F, Li C, Ye R, Byeon B, Xue Y, Zhao H, Wang H N, Crawford B M, Johnson D M, Hu C, Pei C, Zhou W, Swift G B, Zhang H, Vo-Dinh T, Hu Z, Siedow J N, Pei Z M. Plant cell-surface GIPC sphingolipids sense salt to trigger Ca²⁺ influx. Nature, 2019, 572: 341-346. doi: 10.1038/s41586-019-1449-z
[14]	Zhu J K. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol, 2002, 53: 247-273. doi: 10.1146/arplant.2002.53.issue-1
[15]	Barragán V, Leidi E O, Andrés Z, Rubio L, De Luca A, Fernández J A, Cubero B, Pardo J M.Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell, 2012, 24: 1127-1142.
[16]	Kim J, Kim H Y. Functional analysis of a calcium-binding transcription factor involved in plant salt stress signaling. FEBS Lett, 2006, 580: 5251-5256. pmid: 16962584
[17]	Bo C, Chen H, Luo G, Li W, Zhang X, Ma Q, Cheng B, Cai R. Maize WRKY114 gene negatively regulates salt-stress tolerance in transgenic rice. Plant Cell Rep, 2020, 39: 135-148. doi: 10.1007/s00299-019-02481-3 pmid: 31659429
[18]	Qin H, Wang J, Chen X, Wang F, Peng P, Zhou Y, Miao Y, Zhang Y, Gao Y, Qi Y, Zhou J, Huang R. Rice OsDOF15 contributes to ethylene-inhibited primary root elongation under salt stress. New Phytol, 2019, 223: 798-813. doi: 10.1111/nph.15824 pmid: 30924949
[19]	Zhang H, Mao L, Xin M, Xing H, Zhang Y, Wu J, Xu D, Wang Y, Shang Y, Wei L, Cui M, Zhuang T, Sun X, Song X. Overexpression of GhABF3 increases cotton (Gossypium hirsutum L.) tolerance to salt and drought. BMC Plant Biol, 2022, 22: 313. doi: 10.1186/s12870-022-03705-7
[20]	Li M, Chen R, Jiang Q, Sun X, Zhang H, Hu Z. GmNAC06, a NAC domain transcription factor enhances salt stress tolerance in soybean. Plant Mol Biol, 2021, 105: 333-345. doi: 10.1007/s11103-020-01091-y pmid: 33155154
[21]	Chowdhury H A, Bhattacharyya D K, Kalita J K. (Differential) co-expression analysis of gene expression: a survey of best practices. IEEE/ACM Trans Comput Biol Bioinform, 2020, 17: 1154-1173. doi: 10.1109/TCBB.2019.2893170 pmid: 30668502
[22]	Zheng J, He C, Qin Y, Lin G, Park W D, Sun M, Li J, Lu X, Zhang C, Yeh C T, Gunasekara C J, Zeng E, Wei H, Schnable P S, Wang G, Liu S. Co-expression analysis aids in the identification of genes in the cuticular wax pathway in maize. Plant J, 2019, 97: 530-543. doi: 10.1111/tpj.14140
[23]	李旭凯, 李任建, 张宝俊. 利用WGCNA鉴定非生物胁迫相关基因共表达网络. 作物学报, 2019, 45: 1349-1364. doi: 10.3724/SP.J.1006.2019.82061
	Li X K, Li R J, Zhang B J. Identification of rice stress-related gene co-expression modules by WGCNA. Acta Agron Sin, 2019, 45: 1349-1364. (in Chinese with English abstract)
[24]	Ye W, Wang T, Wei W, Lou S, Lan F, Zhu S, Li Q, Ji G, Lin C, Wu X, Ma L. The full-length transcriptome of Spartina alterniflora reveals the complexity of high salt tolerance in monocotyledonous halophyte. Plant Cell Physiol, 2020, 61: 882-896. doi: 10.1093/pcp/pcaa013
[25]	Zhao N, Cui S, Li X, Liu B, Deng H, Liu Y, Hou M, Yang X, Mu G, Liu L. Transcriptome and co-expression network analyses reveal differential gene expression and pathways in response to severe drought stress in peanut (Arachis hypogaea L.). Front Genet, 2021, 12: 672884. doi: 10.3389/fgene.2021.672884
[26]	Yang L, Yang L, Zhao C, Liu J, Tong C, Zhang Y, Cheng X, Jiang H, Shen J, Xie M, Liu S. Differential alternative splicing genes and isoform co-expression networks of Brassica napus under multiple abiotic stresses. Front Plant Sci, 2022, 13: 1009998. doi: 10.3389/fpls.2022.1009998
[27]	Yang Z, Wang S, Wei L, Huang Y, Liu D, Jia Y, Luo C, Lin Y, Liang C, Hu Y, Dai C, Guo L, Zhou Y, Yang Q Y. BnIR: a multi-omics database with various tools for Brassica napus research and breeding. Mol Plant, 2023, 16: 775-789.
[28]	Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics, 2016, 32: 3047-3048.
[29]	Kim D, Paggi J M, Park C, Bennett C, Salzberg S L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol, 2019, 37: 907-915. doi: 10.1038/s41587-019-0201-4 pmid: 31375807
[30]	Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics, 2009, 25: 2078-2079. doi: 10.1093/bioinformatics/btp352 pmid: 19505943
[31]	Liao Y, Smyth G K, Shi W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 2014, 30: 923-930. doi: 10.1093/bioinformatics/btt656 pmid: 24227677
[32]	Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 2020, 13: 1194-1202. doi: S1674-2052(20)30187-8 pmid: 32585190
[33]	Love M I, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol, 2014, 15: 550. doi: 10.1186/s13059-014-0550-8
[34]	Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinf, 2008, 9: 559. doi: 10.1186/1471-2105-9-559
[35]	Yu G, Wang L G, Han Y, He Q Y. ClusterProfiler: an R package for comparing biological themes among gene clusters. OMICS, 2012, 16: 284-287. doi: 10.1089/omi.2011.0118 pmid: 22455463
[36]	Shannon P, Markiel A, Ozier O, Baliga N S, Wang J T, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res, 2003, 13: 2498-2504. doi: 10.1101/gr.1239303 pmid: 14597658
[37]	Jiang Y, Deyholos M K. Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol, 2009, 69: 91-105. doi: 10.1007/s11103-008-9408-3
[38]	Ji H, Pardo J M, Batelli G, Van Oosten M J, Bressan R A, Li X. The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant, 2013, 6: 275-286. doi: 10.1093/mp/sst017 pmid: 23355543
[39]	Ali A, Maggio A, Bressan R A, Yun D J. Role and functional differences of HKT1-type transporters in plants under salt stress. Int J Mol Sci, 2019, 20: 1059. doi: 10.3390/ijms20051059
[40]	Luo X, Li C, He X, Zhang X, Zhu L. ABA signaling is negatively regulated by GbWRKY1 through JAZ1 and ABI1 to affect salt and drought tolerance. Plant Cell Rep, 2020, 39: 181-194. doi: 10.1007/s00299-019-02480-4 pmid: 31713664
[41]	Wolny E, Skalska A, Braszewska A, Mur L A J, Hasterok R. Defining the cell wall, cell cycle and chromatin landmarks in the responses of brachypodium distachyon to salinity. Int J Mol Sci, 2021, 22: 949. doi: 10.3390/ijms22020949
[42]	Cai C, Wang W, Ye S, Zhang Z, Ding W, Xiang M, Wu C, Zhu Q. Overexpression of a novel Arabidopsis gene SUPA leads to various morphological and abiotic stress tolerance alternations in Arabidopsis and Poplar. Front Plant Sci, 2020, 11: 560985.
[43]	Oh G G K, O'Leary B M, Signorelli S, Millar A H.Alternative oxidase (AOX) 1a and 1d limit proline-induced oxidative stress and aid salinity recovery in Arabidopsis. Plant Physiol, 2022, 188: 1521-1536.
[44]	Amsbury S, Hunt L, Elhaddad N, Baillie A, Lundgren M, Verhertbruggen Y, Scheller H V, Knox J P, Fleming A J, Gray J E. Stomatal function requires pectin de-methyl-esterification of the guard cell wall. Curr Biol, 2016, 26: 2899-2906. doi: S0960-9822(16)30933-2 pmid: 27720618
[45]	Kang H G, Kim J, Kim B, Jeong H, Choi S H, Kim E K, Lee H Y, Lim P O. Overexpression of FTL1/DDF1, an AP2 transcription factor, enhances tolerance to cold, drought, and heat stresses in Arabidopsis thaliana. Plant Sci, 2011, 180: 634-641. doi: 10.1016/j.plantsci.2011.01.002
[46]	Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K. Arabidopsis Cys2/His2- type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol, 2004, 136: 2734-2746. doi: 10.1104/pp.104.046599 pmid: 15333755
[47]	Yan Z, Wang J, Wang F, Xie C, Lyu B, Yu Z, Dai S, Liu X, Xia G, Tian H, Li C, Ding Z.MPK3/6-induced degradation of ARR1/10/12 promotes salt tolerance in Arabidopsis. EMBO Rep, 2021, 22: e52457.
[48]	Tran L S, Nakashima K, Sakuma Y, Osakabe Y, Qin F, Simpson SD, Maruyama K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K.Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J, 2007, 49: 46-63.
[49]	张国方.甘蓝型油菜耐盐性遗传解析及候选基因功能验证. 华中农业大学博士学位论文, 湖北武汉, 2021.
	Zhang G F. Genetic Analysis of Salt Tolerance andFunctional Verification of Candidate Genes in Brassica napus. PhD Dissertation of Huazhong Agricultural University, Wuhan, Hubei, China, 2021. (in Chinese with English abstract)
[50]	Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg B E, Kudla J, Harter K. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J, 2007, 50: 347-363. doi: 10.1111/j.1365-313X.2007.03052.x pmid: 17376166
[51]	Zhang H, Zhu J, Gong Z, Zhu J K. Abiotic stress responses in plants. Nat Rev Genet, 2022, 23: 104-119. doi: 10.1038/s41576-021-00413-0
[52]	Luo L, Zhang P, Zhu R, Fu J, Su J, Zheng J, Wang Z, Wang D, Gong Q. Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis. Front Plant Sci, 2017, 8: 1459.
[53]	Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G. How plant hormones mediate salt stress responses. Trends Plant Sci, 2020, 25: 1117-1130. doi: 10.1016/j.tplants.2020.06.008 pmid: 32675014
[54]	Glawischnig E. Camalexin. Phytochemistry, 2007, 68: 401-406. doi: 10.1016/j.phytochem.2006.12.005 pmid: 17217970
[55]	Mukherjee R, Mukherjee A, Bandyopadhyay S, Mukherjee S, Sengupta S, Ray S, Majumder A L. Selective manipulation of the inositol metabolic pathway for induction of salt-tolerance in indica rice variety. Sci Rep, 2019, 9: 5358. doi: 10.1038/s41598-019-41809-7 pmid: 30926863
[56]	Le Gall H, Philippe F, Domon J M, Gillet F, Pelloux J, Rayon C. Cell wall metabolism in response to abiotic stress. Plants (Basel), 2015, 4: 112-166. doi: 10.3390/plants4010112
[57]	Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B. Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules, 2019, 24: 2452. doi: 10.3390/molecules24132452
[58]	Krishnamurthy P, Vishal B, Ho W J, Lok F C J, Lee F S M, Kumar P P. Regulation of a cytochrome P450 gene CYP94B1 by WRKY33 Transcription Factor controls apo plastic barrier formation in roots to confer salt tolerance. Plant Physiol, 2020, 184: 2199-2215. doi: 10.1104/pp.20.01054 pmid: 32928900
[59]	Wang Z, Fang H, Chen Y, Chen K, Li G, Gu S, Tan X. Overexpression of BnWRKY33 in oilseed rape enhances resistance to Sclerotinia sclerotiorum. Mol Plant Pathol, 2014, 15: 677-689. doi: 10.1111/mpp.12123 pmid: 24521393
[60]	Cao F Y, DeFalco T A, Moeder W, Li B, Gong Y, Liu X M, Taniguchi M, Lumba S, Toh S, Shan L, Ellis B, Desveaux D, Yoshioka K. Arabidopsis ETHYLENE RESPONSE FACTOR 8 (ERF8) has dual functions in ABA signaling and immunity. BMC Plant Biol, 2018, 18: 211. doi: 10.1186/s12870-018-1402-6

Metrics

Viewed

Full text

Abstract

Cited

Shared

Discussed

Comments

Recommended 0

No Suggested Reading articles found!

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.

RichHTML419

PDF

Review File

Abstract

Cite this article

share this article

Figures/Tables 13

References 60

Related Articles 15

Metrics

Comments

Recommended 0

[1]	Chen Xue-Yan, He Hua-Chuan, Li Zheng-Jia, Dong Xin-Pan, Li Ou-Qi, Liu Xiao-Yun, Li Dan-Ping, Chen Zhi-Wei, Liu Guo-Xia, Lyu Sheng-Yuan, Wu Yin-Ying, Zhao Zhen-Dong, Cao Xin-You, Wan He-Ping. Dynamic changes in root organic acid secretion and its transcriptional regulatory mechanisms in ‘Jimai 60’ seedlings under combined salinity-alkalinity stress in hydroponics [J]. Acta Agronomica Sinica, 2026, 52(6): 1859-1875.
[2]	Zou Yi-Mei, Xu Min, Wang Hai-Yang, Yao Hui, Wang Jia-Feng, Liu Hao, Ren Dai-Sheng. Analysis of transcription factor regulatory networks in two-line male sterile rice seedling roots in response to salt stress [J]. Acta Agronomica Sinica, 2026, 52(6): 1728-1742.
[3]	Song Yu-Zhen, Bheel Chander Kumar, Wang Yue, Zhang Ying-Xing, Guo Juan, Khound Rituraj, Santra Dipak Kumar, Cao Xiao-Ning, Wang Rui-Yun. Genome-wide identification of the AP2 subfamily in broomcorn millet and functional characterization of PmAP2-1 and PmAP2-9 in salt tolerance [J]. Acta Agronomica Sinica, 2026, 52(4): 1127-1139.
[4]	Wang Chu-Rui, Li Kai-Xiang, Zhao Zhi, Xiao Lu, Tang Guo-Yong, Zhao Zhi-Gang, Xu Liang, Du De-Zhi, Liu Hai-Dong. Development and application of KASP markers for functional sites of the early flowering gene BnCRY2 in Brassica napus L. spring rapeseed [J]. Acta Agronomica Sinica, 2026, 52(3): 708-721.
[5]	Qin Yi-Yan, Fu Yao, Su Chang, Li Na, Xu Jing-Ru, Cheng Xiao-Ran, Zhang Qi, Zhao Ming-Hui. Functional analysis of OsST41 regulating salt tolerance in rice seedlings [J]. Acta Agronomica Sinica, 2026, 52(3): 802-812.
[6]	Zhang Qing, Yang Yu, Guo Qian, Yue Pei-Yao, Yin Cong-Cong, Niu Jing-Ping, Zhao Jin-Zhong, Du Wei-Jun, Yue Ai-Qin. Cloning and functional analysis of the soybean GmARA6a gene in response to salt stress [J]. Acta Agronomica Sinica, 2026, 52(2): 480-493.
[7]	Liu Ji-Chang, Li Si-Ye, Li Xue-Ting, Wang Hong-Zhang, Liu Peng, Zhang Ji-Wang, Zhao Bin, Ren Bai-Zhao, Ren Hao. Effects of salt stress on root growth and nutrient absorption efficiency of different salt-tolerant summer maize varieties [J]. Acta Agronomica Sinica, 2026, 52(2): 565-577.
[8]	GAO Yuan, WANG Yu-Qi, JIANG Jia-Ning, ZHAO Jian-Xiong, WANG Xue-He-Yuan, WANG Hao-Yu, ZHANG Rui-Jia, XU Jing-Yu, HE Lin. Identification and functional analysis of low temperature responsive genes ZmNTL1 and ZmNTL5 in maize [J]. Acta Agronomica Sinica, 2025, 51(9): 2318-2329.
[9]	XU Yi-Wei, ZHANG Ying-Ying, LI Rui, YAN Yong-Liang, LIU Yun-Jun, KONG Zhao-Sheng, ZHENG Jun, WANG Yi-Ru. csp2 gene of Deinococcus gobiensis improves drought tolerance in maize [J]. Acta Agronomica Sinica, 2025, 51(8): 1981-1990.
[10]	FANG Ying-Hao, ZHOU Bo, CHEN Ru-Mei, YANG Wen-Zhu, QIN Hui-Min. Integrative analysis of RNA-seq and PER-seq to elucidate regulatory network of ZmHDZ6 expression [J]. Acta Agronomica Sinica, 2025, 51(4): 958-968.
[11]	PAN Ju-Zhong, WEI Ping, ZHU De-Ping, SHAO Sheng-Xue, CHEN Shan-Shan, WEI Ya-Qian, GAO Wei-Wei. Cloning and functional analysis of OsERF104 transcription factor in rice [J]. Acta Agronomica Sinica, 2025, 51(4): 900-913.
[12]	LI Xue-Ting, REN Hao, WANG Hong-Zhang, ZHANG Ji-Wang, ZHAO Bin, REN Bai-Zhao, LIU Ying, YAO Hai-Yan, LIU Peng. Effects of salt stress on photosynthetic performance and dry matter accumulation and distribution in leaves of different salt-tolerant maize varieties [J]. Acta Agronomica Sinica, 2025, 51(4): 1091-1101.
[13]	HUO Ru-Xue, GE Xiang-Han, SHI Jia, LI Xue-Rui, DAI Sheng-Jie, LIU Zhen-Ning, LI Zong-Yun. Functional analysis of the sweetpotato histidine kinase protein IbHK5 in response to drought and salt stresses [J]. Acta Agronomica Sinica, 2025, 51(3): 650-666.
[14]	SUN Cheng-Ming, ZHOU Xiao-Ying, CHEN Feng, ZHANG Wei, WANG Xiao-Dong, PENG Qi, GUO Yue, GAO Jian-Qin, HU Mao-Long, FU San-Xiong, ZHANG Jie-Fu. Functional analysis and prediction of long non-coding RNA (lncRNA) in the regulation of branch angle in Brassica napus L. [J]. Acta Agronomica Sinica, 2025, 51(3): 559-567.
[15]	ZHUANG Yue-Ming, SONG Yi, CHEN Hang-Hang, LU Zhi-Feng, LIAO Shi-Peng, LI Xiao-Kun, CONG Ri-Huan, REN Tao, LU Jian-Wei. Effects of application of nitrogen on endophytic microbiota and seed quality in rapeseed (Brassica napus L.) seeds [J]. Acta Agronomica Sinica, 2025, 51(12): 3357-3368.