Screening and Identification of Interacting Proteins of CsMYC2 and CsMPK6 in Citrus Based on Pull-Down/MS Technique

doi:10.16420/j.issn.0513-353x.2023-0744

Acta Horticulturae Sinica ›› 2024, Vol. 51 ›› Issue (12): 2913-2927.doi: 10.16420/j.issn.0513-353x.2023-0744

• New Technologies and New Methods • Previous Articles Next Articles

Screening and Identification of Interacting Proteins of CsMYC2 and CsMPK6 in Citrus Based on Pull-Down/MS Technique

JIANG Zhenghua¹, LIU Shengjun¹, LIU Wenjie¹, WEI Ranran¹, HE Zhengchen¹, CHENG Chao³, TANG Zheng³, LIU Baoyan³, XIE Zongzhou¹, YE Junli¹, CHAI Lijun¹^,², YUE Pengtao¹(), DENG Xiuxin¹^,²()

¹National Key Laboratory of Germplasm Innovation & Utilization of Horticultural Crops，Department of Horticulture and Forestry，Huazhong Agricultural University，Wuhan 430070，China
²Hubei Hongshan Laboratory，Wuhan 430070，China
³Changjiang Survey，Planning Design and Research Co.，Ltd，Wuhan 430010，China

Received:2024-05-24 Revised:2024-09-12 Online:2024-12-25 Published:2024-12-13
Contact: YUE Pengtao, DENG Xiuxin

Abstract

Abstract:

The purpose of this study is to explore the interaction network of CsMPK6-CsMYC2 module and identify the proteins involved in the citrus peel coloring process mediated by jasmonic acid through the interaction screening with CsMPK6-CsMYC2 module. To this purpose，Pull-Down with mass spectrometry technique（Pull-Down/MS）was performed to screen and identify the CsMPK6-CsMYC2 interacting proteins using the total proteins isolated from MeJA-treated citrus fruit. The interactive proteins were involved in secondary metabolites biosynthesis，plant mitogen-activated protein kinase signaling pathway，ribosome pathway，stress response，hormone response，abiotic stress responses and other biological processes according to bioinformatics analysis. Among them，trihelix transcription factor CsGT2 and germin-like protein CsGLP play important roles in fruit development. Therefore，the interactions of CsGT2 with CsMYC2，CsGLP with CsMPK6 and CsGLP with CsMYC2 were further confirmed. The promoters of CsGT2 and CsGLP contained multiple cis-acting elements involving in light，hormone and stress-response. This work provides a reference for species that are difficult to screen interacting proteins by using yeast two-hybrid system and IP-MS technology. Meanwhile，this work provides gene pool for further study regarding the regulatory network for the jasmonate-induced coloration in citrus fruit.

Key words: citrus, coloration, jasmonates, Pull-Down/MS, protein interaction

JIANG Zhenghua, LIU Shengjun, LIU Wenjie, WEI Ranran, HE Zhengchen, CHENG Chao, TANG Zheng, LIU Baoyan, XIE Zongzhou, YE Junli, CHAI Lijun, YUE Pengtao, DENG Xiuxin. Screening and Identification of Interacting Proteins of CsMYC2 and CsMPK6 in Citrus Based on Pull-Down/MS Technique[J]. Acta Horticulturae Sinica, 2024, 51(12): 2913-2927.

Figures/Tables 11

References 46

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用途	引物名称	引物序列（5′-3′）
Purpose	Primer name	Primer sequence
全长扩增	CsGLP-F	ATGAAGGTAATTCAATTTCTTATAGGTTTT
Full length amplification	CsGLP-R	CTAATTGCCATTAATGAACTTATTTTGAAG
	CsGT2-F	ATGGAAGGCCAATCATCACTAACT
	CsGT2-R	CTAAACTGTTAAATCGTAATCAGCCC
蛋白纯化	CsGLP-C2X-EcoRⅠ-F	GAGGGAAGGATTTCA GAATTCATGAAGGTAATTCAATTTCTTAT
Protein purification	CsGLP-C2X-SalⅠ-R	CAAGCTTGCCTGCAG GTCGACCTAATTGCCATTAATGAACTTATTT
	CsGT2-GST-EcoRⅠ-F	CCGCGTGGATCCCCG GAATTCATGGAAGGCCAATCATCACTAACT
	CsGT2-GST-SalⅠ-R	GATGCGGCCGCTCGA GTCGACCTAAACTGTTAAATCGTAATCAGCCC
荧光素酶互补实验	CsGT2-772-F	TACGCGTCCCGGGGC GGTACCATGGAAGGCCAATCATCACTAACT
Luciferase complementation	CsGT2-772-R	ACGAAAGCTCTGCAG GTCGACCTAAACTGTTAAATCGTAATCAGCCC
assay	CsGLP-771-F	ACGGGGGACGAGCTC GGTACCATGAAGGTAATTCAATTTCTTATAGGTTT
	CsGLP-771-R	CGCGTACGAGATCTG GTCGACCTAATTGCCATTAATGAACTTATTTTGAA

用途	引物名称	引物序列（5′-3′）
Purpose	Primer name	Primer sequence
全长扩增	CsGLP-F	ATGAAGGTAATTCAATTTCTTATAGGTTTT
Full length amplification	CsGLP-R	CTAATTGCCATTAATGAACTTATTTTGAAG
	CsGT2-F	ATGGAAGGCCAATCATCACTAACT
	CsGT2-R	CTAAACTGTTAAATCGTAATCAGCCC
蛋白纯化	CsGLP-C2X-EcoRⅠ-F	GAGGGAAGGATTTCA GAATTCATGAAGGTAATTCAATTTCTTAT
Protein purification	CsGLP-C2X-SalⅠ-R	CAAGCTTGCCTGCAG GTCGACCTAATTGCCATTAATGAACTTATTT
	CsGT2-GST-EcoRⅠ-F	CCGCGTGGATCCCCG GAATTCATGGAAGGCCAATCATCACTAACT
	CsGT2-GST-SalⅠ-R	GATGCGGCCGCTCGA GTCGACCTAAACTGTTAAATCGTAATCAGCCC
荧光素酶互补实验	CsGT2-772-F	TACGCGTCCCGGGGC GGTACCATGGAAGGCCAATCATCACTAACT
Luciferase complementation	CsGT2-772-R	ACGAAAGCTCTGCAG GTCGACCTAAACTGTTAAATCGTAATCAGCCC
assay	CsGLP-771-F	ACGGGGGACGAGCTC GGTACCATGAAGGTAATTCAATTTCTTATAGGTTT
	CsGLP-771-R	CGCGTACGAGATCTG GTCGACCTAATTGCCATTAATGAACTTATTTTGAA

基因ID	注释	基因ID	注释
Gene ID	Annotation	Gene ID	Annotation
CISIN 1g039131mg	MYB-DNA结合结构域蛋白MYB-DNA domain-containing protein（CsGT2）	CISIN 1g027381mg	类萌发素蛋白 Germin-like protein（CsGLP）
CISIN 1g001709mg	含有Lipase 3结构域的蛋白 Lipase 3 domain-containing protein	CISIN 1g031118mg	含VOC结构域的蛋白 VOC domain-containing protein
CISIN 1g028399mg	LEA 2结构域蛋白 LEA_2 domain-containing protein	CISIN 1g011329mg	液泡质子泵亚基B Vacuolar proton pump subunit B
CISIN 1g013829mg	抗坏血酸过氧化酶 L-ascorbate peroxidase	CISIN 1g031168mg	含有Usp结构域的蛋白质 Usp domain-containing protein
Annotation	Gene ID	Annotation
CISIN 1g026316mg	KH 2型结构域蛋白 KH type-2 domain-containing protein	CISIN 1g005713mg	含有Tr型G结构域的蛋白 Tr-type G domain-containing protein
CISIN 1g015012mg	异柠檬酸脱氢酶 Isocitrate dehydrogenase[NADP]	CISIN 1g003492mg	蔗糖合酶 Sucrose synthase
CISIN 1g017413mg	异柠檬酸脱氢酶（NAD）亚基，线粒体 Isocitrate dehydrogenase[NAD]subunit，mitochondrial	CISIN 1g031218mg	含SHSP结构域的蛋白 SHSP domain-containing protein
CISIN 1g032645mg	组蛋白 H3 Histone H3	CISIN 1g015873mg	S-腺苷甲硫氨酸合酶 S-Adenosylmethionine synthase
CISIN 1g013352mg	鸟苷核苷酸二磷酸解离抑制剂 Guanosine nucleotide diphosphate dissociation inhibitor	CISIN 1g012947mg	Sacchrp dh NADP结构域蛋白 Sacchrp dh NADP domain-containing protein
CISIN 1g024728mg	含有GRAM结构域的蛋白 GRAM domain-containing protein	CISIN 1g012719mg	RuvB-like解旋酶 RuvB-like helicase
CISIN 1g027134mg	谷胱甘肽过氧化物酶 Glutathione peroxidase	CISIN 1g007404mg	RNA聚合酶因子 RNA polymerase sigma factor
CISIN 1g028808mg	谷氧还蛋白依赖过氧化物还原酶 Glutaredoxin-dependent peroxiredoxin	CISIN 1g031854mg	含有核糖体s13 n结构域的蛋白 Ribosomal S13 N domain-containing protein
CISIN 1g020203mg	LRRNT 2结构域蛋白 LRRNT 2 domain-containing protein	CISIN 1g036921mg	丙酮酸激酶 Pyruvate kinase
CISIN 1g018326mg	果糖二磷酸醛缩酶 Fructose-bisphosphate aldolase	CISIN 1g026587mg	蛋白酶体亚基 Proteasome subunit beta
CISIN 1g023956mg	铁蛋白 Ferritin	CISIN 1g023059mg	抑制素蛋白 Prohibitin
CISIN 1g027898mg	内质网跨膜蛋白Endoplasmic reticulum transmembrane protein	CISIN 1g027094mg	PMEI结构域蛋白 PMEI domain-containing protein
CISIN 1g027254mg	含EF1 GNE结构域的蛋白 EF1 GNE domain-containing protein	CISIN 1g0180941mg	PKS ER结构域蛋白 PKS ER domain-containing protein
CISIN 1g0075121mg	D-3-磷酸甘油酸脱氢酶 D-3-phosphoglycerate dehydrogenase	CISIN 1g014812mg	Pinin SDK memA结构域蛋白 Pinin SDK memA domain-containing protein
CISIN 1g023850mg	细胞色素b-c1复合体亚基Rieske，线粒体Cytochrome b-c1 complex subunit Rieske，mitochondrial	CISIN 1g043137mg	磷酸丙酮酸水合酶 Phosphopyruvate hydratase
CISIN 1g002012mg	含有Clp R结构域的蛋白 Clp R domain-containing protein	CISIN 1g004579mg	磷脂酶D Phospholipase D
CISIN 1g044386mg	过氧化氢酶 Catalase	CISIN 1g011942mg	磷酸甘油酸酯激酶Phosphoglycerate kinase
CISIN 1g023810mg	C2结构域蛋白 C2 domain-containing protein	CISIN 1g0064861mg	磷酸烯醇丙酮酸羧激酶（ATP） Phosphoenolpyruvate carboxykinase（ATP）
CISIN 1g029006mg	ATP-synt DE N结构域蛋白 ATP-synt DE N domain-containing protein	CISIN 1g000370mg	PHD型结构域蛋白 PHD-type domain-containing protein
CISIN 1g008610mg	ATP合成酶亚基 ATP synthase subunit beta	CISIN 1g038305mg	含PHB型结构域蛋白 PHB domain-containing protein
CISIN 1g035973mg	膜联蛋白 Annexin	CISIN 1g018811mg	过氧化物酶 Peroxidase
CISIN 1g012095mg	Aminotran 1 2结构域蛋白 Aminotran 1 2 domain-containing protein	CISIN 1g011566mg	含有肽酶A1结构域的蛋白 Peptidase A1 domain-containing protein
CISIN 1g018374mg	Aldo ket red结构域蛋白 Aldo ket red domain-containing protein	CISIN 1g014555mg	PCI结构域蛋白 PCI domain-containing protein
CISIN 1g016996mg	ADP/ATP移位酶 ADP/ATP translocase	CISIN 1g022196mg	PAP 原纤维蛋白结构域蛋白 PAP fibrillin domain-containing protein
CISIN 1g011464mg	腺苷高半胱氨酸酶 Adenosyl homocysteinase	CISIN 1g026906mg	核苷二磷酸激酶 Nucleoside diphosphate kinase
CISIN 1g008996mg	丙酮酸脱氢酶复合物的乙酰转移酶组分 Acetyltransferase component of pyruvate dehydrogenase complex	CISIN 1g033151mg	非特异性脂质转移蛋白 Non-specific lipid-transfer protein
CISIN 1g038101mg	AAA结构域蛋白 AAA domain-containing protein	CISIN 1g020296mg	NADH-细胞色素b5还原酶 NADH-cytochrome b5 reductase
CISIN 1g025016mg	60S核糖体蛋白L7a 60S ribosomal protein L7a	CISIN 1g031073mg	V型质子ATP酶蛋白脂亚基 V-type proton ATPase proteolipid subunit
CISIN 1g015722mg	(S)-2-羟酸氧化酶 (S)-2-hydroxy-acid oxidase	CISIN 1g026558mg	Methyl transfer 11结构域蛋白 Methyltransf 11 domain-containing protein
CISIN 1g018314mg	苹果酸脱氢酶 Malate dehydrogenase	CISIN 1g017293mg	Methylthioribose-1-磷酸异构酶 Methylthioribose-1-phosphate isomerase

基因ID	注释	基因ID	注释
Gene ID	Annotation	Gene ID	Annotation
CISIN 1g039131mg	MYB-DNA结合结构域蛋白MYB-DNA domain-containing protein（CsGT2）	CISIN 1g027381mg	类萌发素蛋白 Germin-like protein（CsGLP）
CISIN 1g001709mg	含有Lipase 3结构域的蛋白 Lipase 3 domain-containing protein	CISIN 1g031118mg	含VOC结构域的蛋白 VOC domain-containing protein
CISIN 1g028399mg	LEA 2结构域蛋白 LEA_2 domain-containing protein	CISIN 1g011329mg	液泡质子泵亚基B Vacuolar proton pump subunit B
CISIN 1g013829mg	抗坏血酸过氧化酶 L-ascorbate peroxidase	CISIN 1g031168mg	含有Usp结构域的蛋白质 Usp domain-containing protein
Annotation	Gene ID	Annotation
CISIN 1g026316mg	KH 2型结构域蛋白 KH type-2 domain-containing protein	CISIN 1g005713mg	含有Tr型G结构域的蛋白 Tr-type G domain-containing protein
CISIN 1g015012mg	异柠檬酸脱氢酶 Isocitrate dehydrogenase[NADP]	CISIN 1g003492mg	蔗糖合酶 Sucrose synthase
CISIN 1g017413mg	异柠檬酸脱氢酶（NAD）亚基，线粒体 Isocitrate dehydrogenase[NAD]subunit，mitochondrial	CISIN 1g031218mg	含SHSP结构域的蛋白 SHSP domain-containing protein
CISIN 1g032645mg	组蛋白 H3 Histone H3	CISIN 1g015873mg	S-腺苷甲硫氨酸合酶 S-Adenosylmethionine synthase
CISIN 1g013352mg	鸟苷核苷酸二磷酸解离抑制剂 Guanosine nucleotide diphosphate dissociation inhibitor	CISIN 1g012947mg	Sacchrp dh NADP结构域蛋白 Sacchrp dh NADP domain-containing protein
CISIN 1g024728mg	含有GRAM结构域的蛋白 GRAM domain-containing protein	CISIN 1g012719mg	RuvB-like解旋酶 RuvB-like helicase
CISIN 1g027134mg	谷胱甘肽过氧化物酶 Glutathione peroxidase	CISIN 1g007404mg	RNA聚合酶因子 RNA polymerase sigma factor
CISIN 1g028808mg	谷氧还蛋白依赖过氧化物还原酶 Glutaredoxin-dependent peroxiredoxin	CISIN 1g031854mg	含有核糖体s13 n结构域的蛋白 Ribosomal S13 N domain-containing protein
CISIN 1g020203mg	LRRNT 2结构域蛋白 LRRNT 2 domain-containing protein	CISIN 1g036921mg	丙酮酸激酶 Pyruvate kinase
CISIN 1g018326mg	果糖二磷酸醛缩酶 Fructose-bisphosphate aldolase	CISIN 1g026587mg	蛋白酶体亚基 Proteasome subunit beta
CISIN 1g023956mg	铁蛋白 Ferritin	CISIN 1g023059mg	抑制素蛋白 Prohibitin
CISIN 1g027898mg	内质网跨膜蛋白Endoplasmic reticulum transmembrane protein	CISIN 1g027094mg	PMEI结构域蛋白 PMEI domain-containing protein
CISIN 1g027254mg	含EF1 GNE结构域的蛋白 EF1 GNE domain-containing protein	CISIN 1g0180941mg	PKS ER结构域蛋白 PKS ER domain-containing protein
CISIN 1g0075121mg	D-3-磷酸甘油酸脱氢酶 D-3-phosphoglycerate dehydrogenase	CISIN 1g014812mg	Pinin SDK memA结构域蛋白 Pinin SDK memA domain-containing protein
CISIN 1g023850mg	细胞色素b-c1复合体亚基Rieske，线粒体Cytochrome b-c1 complex subunit Rieske，mitochondrial	CISIN 1g043137mg	磷酸丙酮酸水合酶 Phosphopyruvate hydratase
CISIN 1g002012mg	含有Clp R结构域的蛋白 Clp R domain-containing protein	CISIN 1g004579mg	磷脂酶D Phospholipase D
CISIN 1g044386mg	过氧化氢酶 Catalase	CISIN 1g011942mg	磷酸甘油酸酯激酶Phosphoglycerate kinase
CISIN 1g023810mg	C2结构域蛋白 C2 domain-containing protein	CISIN 1g0064861mg	磷酸烯醇丙酮酸羧激酶（ATP） Phosphoenolpyruvate carboxykinase（ATP）
CISIN 1g029006mg	ATP-synt DE N结构域蛋白 ATP-synt DE N domain-containing protein	CISIN 1g000370mg	PHD型结构域蛋白 PHD-type domain-containing protein
CISIN 1g008610mg	ATP合成酶亚基 ATP synthase subunit beta	CISIN 1g038305mg	含PHB型结构域蛋白 PHB domain-containing protein
CISIN 1g035973mg	膜联蛋白 Annexin	CISIN 1g018811mg	过氧化物酶 Peroxidase
CISIN 1g012095mg	Aminotran 1 2结构域蛋白 Aminotran 1 2 domain-containing protein	CISIN 1g011566mg	含有肽酶A1结构域的蛋白 Peptidase A1 domain-containing protein
CISIN 1g018374mg	Aldo ket red结构域蛋白 Aldo ket red domain-containing protein	CISIN 1g014555mg	PCI结构域蛋白 PCI domain-containing protein
CISIN 1g016996mg	ADP/ATP移位酶 ADP/ATP translocase	CISIN 1g022196mg	PAP 原纤维蛋白结构域蛋白 PAP fibrillin domain-containing protein
CISIN 1g011464mg	腺苷高半胱氨酸酶 Adenosyl homocysteinase	CISIN 1g026906mg	核苷二磷酸激酶 Nucleoside diphosphate kinase
CISIN 1g008996mg	丙酮酸脱氢酶复合物的乙酰转移酶组分 Acetyltransferase component of pyruvate dehydrogenase complex	CISIN 1g033151mg	非特异性脂质转移蛋白 Non-specific lipid-transfer protein
CISIN 1g038101mg	AAA结构域蛋白 AAA domain-containing protein	CISIN 1g020296mg	NADH-细胞色素b5还原酶 NADH-cytochrome b5 reductase
CISIN 1g025016mg	60S核糖体蛋白L7a 60S ribosomal protein L7a	CISIN 1g031073mg	V型质子ATP酶蛋白脂亚基 V-type proton ATPase proteolipid subunit
CISIN 1g015722mg	(S)-2-羟酸氧化酶 (S)-2-hydroxy-acid oxidase	CISIN 1g026558mg	Methyl transfer 11结构域蛋白 Methyltransf 11 domain-containing protein
CISIN 1g018314mg	苹果酸脱氢酶 Malate dehydrogenase	CISIN 1g017293mg	Methylthioribose-1-磷酸异构酶 Methylthioribose-1-phosphate isomerase

基因ID	注释	基因ID	注释
Gene ID	Annotation	Gene ID	Annotation
CISIN 1g027381mg	类萌发素蛋白 Germin-like protein，CsGLP	CISIN 1g010053mg	bHLH结构域蛋白 BHLH domain-containing protein，CsMYC2
CISIN 1g020203mg	LRRNT 2结构域蛋白 LRRNT 2 domain-containing protein	CISIN 1g013165mg	微管蛋白 Tubulin beta chain
CISIN 1g002055mg	LRRNT 2结构域蛋白 LRRNT 2 domain-containing protein	CISIN 1g002012mg	含Clp R结构域的蛋白 Clp R domain-containing protein
CISIN 1g014614mg	无特征的蛋白质 Uncharacterized protein	CISIN 1g024515mg	核糖体L18e/L15P结构域蛋白 Ribosomal L18e/L15P domain-containing protein
CISIN 1g0132372mg	延长因子1-α Elongation factor 1-alpha	CISIN 1g017081mg	无特征的蛋白质 Uncharacterized protein
CISIN 1g017684mg	无特征的蛋白质 Uncharacterized protein	CISIN 1g006297mg	无特征的蛋白质 Uncharacterized protein
CISIN 1g005713mg	含有Tr型G结构域的蛋白 Tr-type G domain-containing protein	CISIN 1g019445mg	甘油醛-3-磷酸脱氢酶 Glyceraldehyde-3-phosphate dehydrogenase

Screening and Identification of Interacting Proteins of CsMYC2 and CsMPK6 in Citrus Based on Pull-Down/MS Technique

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