猕猴桃AcMYB88的鉴定及功能研究

doi:10.13560/j.cnki.biotech.bull.1985.2023-0726

生物技术通报 ›› 2024, Vol. 40 ›› Issue (2): 183-196.doi: 10.13560/j.cnki.biotech.bull.1985.2023-0726

猕猴桃AcMYB88的鉴定及功能研究

苑馨予¹^,²(), 钟彩虹², 张龙², 郑浩², 李吉涛¹(), 张琼²()

1.生物资源保护与利用湖北省重点实验室（湖北民族大学），恩施 445000
2.中国科学院武汉植物园中国科学院植物种质创新与特色农业重点实验室中国科学院猕猴桃产业技术工程实验室，武汉 430074

收稿日期:2023-07-30 出版日期:2024-02-26 发布日期:2024-03-13
通讯作者: 李吉涛，男，博士，讲师，研究方向：园艺植物分子生物学；E-mail: ljtyouth@foxmail.com；
张琼，女，博士，研究员，研究方向：果树分子育种；E-mail: qiongzhang@wbgcas.cn
作者简介:苑馨予，女，硕士研究生，研究方向：猕猴桃分子遗传；E-mail: yuanxinyu0618@foxmail.com
基金资助:
国家重点研发计划项目(2018YFD1000203);中国科学院战略性先导科技专项（A类）(XDA24030404);果树种质创新与利用湖北省重点实验室开放课题(GSSZ202301);湖北省自然科学基金项目(2021CFB555);生物资源保护与利用湖北省重点实验室开放基金项目(KYPT012308);湖北民族大学博士启动基金(MD2019B016);陕西省重点研发计划(2023-ZDLNY-24)

Identification and Function Analysis of AcMYB88 in Kiwifruit （Actinidia chinensis）

YUAN Xin-yu¹^,²(), ZHONG Cai-hong², ZHANG Long², ZHENG Hao², LI Ji-tao¹(), ZHANG Qiong²()

1. Hubei Key Laboratory of Biological Resources Protection and Utilization（Hubei Minzu University）, Enshi 445000
2. Chinese Academy of Sciences Wuhan Botanical Garden, Chinese Academy of Sciences Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Chinese Academy of Sciences Engineering Laboratory for Kiwifruit Industrial Technology, Wuhan 430074

Received:2023-07-30 Published:2024-02-26 Online:2024-03-13

摘要/Abstract

摘要：

【目的】MYB转录因子在猕猴桃花青苷积累中发挥着重要作用，挖掘调控花青苷生物合成的MYB家族转录因子并验证其功能，可进一步明晰花青苷积累的分子机制。【方法】AcMYB110是猕猴桃花青苷生物合成的关键转录因子，通过系统发育树分析猕猴桃中97个MYB家族转录因子，筛选出与AcMYB110高度同源的12个MYB转录因子，采用生物信息学方法分析它们的理化性质、亲疏水性、蛋白磷酸化位点、蛋白质二级结构及其与其他物种的系统进化关系。【结果】12个MYB转录因子编码的氨基酸数目为200-423个；分子量范围为22.3-45.5 kD，均为定位于细胞核的亲水性蛋白。12个候选MYB蛋白的潜在磷酸化位点大多位于丝氨酸残基处；其二级结构以无规则卷曲为主，α-螺旋为辅。在12个候选MYB转录因子中筛选得到1个花青素积累相关的转录因子AcMYB88，在猕猴桃果实发育过程中AcMYB88基因与AcMYB110基因表达模式非常相似。【结论】烟草瞬时过表达研究表明，AcMYB88为花青苷积累的正向调控因子，且能与AcMYB110和AcbHLH42协同作用从而促进花青苷的积累。该研究为猕猴桃花青素生物合成以及育种研究等方面提供理论基础。

关键词: 猕猴桃, MYB, 家族分析, 花青苷

Abstract:

【Objective】 MYB transcription factors play an important role in anthocyanin accumulation of kiwifruit. Identifying MYB transcription factors that regulate anthocyanin biosynthesis and verifying gene functions facilitate elucidating the molecular mechanism of anthocyanin accumulation.【Method】 It was reported that AcMYB110 was a key transcription factor promoting anthocyanin accumulation in kiwifruit. In PlantTFDB database, 12 MYB genes that showing high homology to AcMYB110 were identified from 97 kiwifruit MYB genes by phylogenetic tree analysis. Bioinformatics methods were employed to analyze their physical and chemical properties, hydrophilicity and hydrophobicity, protein phosphorylation sites, protein secondary structures, and phylogenetic relationships with other species.【Result】 The 12 MYB transcription factors encoded amino acids ranging from 200 to 423; their molecular weight ranged from 22.3 to 45.5 kD, and all of them were hydrophilic proteins located in the nucleus. The majority of potential phosphorylation sites in the 12 candidate MYB proteins were found to be at serine residues. Moreover, their secondary structures were primarily composed of random coils with some α-helices. Among the 12 MYB transcription factors, the expression pattern of AcMYB88 gene was very similar to that of AcMYB110 gene during kiwifruit development.【Conclusion】 Transient overexpression experiments in tobacco demonstrate that AcMYB88 acts as a positive regulator of anthocyanin accumulation, and AcMYB88 synergistically promotes anthocyanin accumulation with AcMYB110 and AcbHLH42. This study provides a theoretical foundation for understanding anthocyanin biosynthesis and breeding research in kiwifruit

Key words: Actinidia chinensis, MYB, family analysis, anthocyanins

苑馨予, 钟彩虹, 张龙, 郑浩, 李吉涛, 张琼. 猕猴桃AcMYB88的鉴定及功能研究[J]. 生物技术通报, 2024, 40(2): 183-196.

YUAN Xin-yu, ZHONG Cai-hong, ZHANG Long, ZHENG Hao, LI Ji-tao, ZHANG Qiong. Identification and Function Analysis of AcMYB88 in Kiwifruit （Actinidia chinensis）[J]. Biotechnology Bulletin, 2024, 40(2): 183-196.

图/表 14

表1 试验用到的引物序列

Table 1 Primer sequences used in the experiment

基因名称 Gene name	正向引物 Forward primer（5'-3'）	反向引物 Reverse primer（5'-3'）	备注 Note
Actin	TGAGAGATTCCGTTGCCCAGAAGT	TTCCTTACTCATGCGGTCTGCGAT	实时荧光定量PCR分析所用引物 Primers for real-time RT-qPCR analysis
Achn033551	GCATCCATGACATCACCAGC	AGCATAACCGGTGTCCCAAC
Achn036201	TGACCGGTGGTACAATGTGG	CCTGATGGTTCACCCACTCC
Achn141271	GGGCTCTCGCGATATACGAC	TCTCCAACGTGAACGACGAG
Achn145641	TCCATGACATCACCAGCGTC	AGGAAGCATAACTGGCGTCC
Achn154591	ACGACATCACCACCGTCAAT	GCCGGTCCTTCACTTGGTAG
Achn172831	GGAGTGCTCCTCGGATTGTC	CCACTTTCTGCCACCGATCA
Achn207851	CTGTGGTACCCAGAATGCCT	ATGTCGTGGATGCTTGACCG
Achn212251	AAGGCCAACCGTGAATCTCC	AGGCAATCCGACATGGGTTC
Achn218481	AGAAGTACTTCATCCGGCAGC	GGAATTGCGTTCTTGGATTGG
Achn258201	CCCTGGCAACTTATCCCGAG	CTTGCGTCGCTCCTGATCTA
Achn365361	ACGACGGCAGTGATTATCGG	CTTGTCCTCGAACCTCGTCC
Achn371351	ATTGGAGGAGCATATCGCGG	TGGATGCTTGAACGTCTCCC
Acc00493（AcMYB10）	GCCATCACCACCATCCAACA	TTCCCCAAAATTGGCTCCTCA
Acc19563（AcbHLH42）	TCGTTTAGGGCCGAGTCTAC	TTGAGAGTAGTGCGTGTCGT
pSAK-Achn365361	ACTAGTGGATCCAAAGAATTCATGTATGGCGACGACGGC	AGAAGTACTCTCGAGAAGCTTTACATGGGATAGTTGAAGTTTTGGTACCC	过表达载体构建所用引物 Primers used for overexpression vector construction
pSAK-AcMYB10	ACTAGTGGATCCAAAGAATTCATGGAAAGTGTTACTTTAGGAGTGAGAAAGG	AGAAGTACTCTCGAGAAGCTTTAATCATCACCTAAGAGATCCCAAAGGTTAACA
pSAK-AcbHLH42	ACTAGTGGATCCAAAGAATTCATGGCGGCTCCCCCT	AGAAGTACTCTCGAGAAGCTTCAGGGTATGATTTGGTGTATTGCTCTCT
NtActin	AATGGAACTGGAATGGTCAAGGC	TGCCAGATCTTCTCCATGTCATCCCA	烟草RT-qPCR分析所用引物 Primers for real-time RT-qPCR analysis in tobacco
AcMYB88	ACGACGGCAGTGATTATCGG	CTTGTCCTCGAACCTCGTCC
AcMYB10	GCCATCACCACCATCCAACA	TTCCCCAAAATTGGCTCCTCA
AcbHLH42	TCGTTTAGGGCCGAGTCTAC	TTGAGAGTAGTGCGTGTCGT
NtC4H	ACAACCCGGATCACTGGAAG	ACTGTCCACCTTTCTCCGTG
NtCHS	TTGTTCGAGCTTGTCTCTGC	AGCCCAGGAACATCTTTGAG
NtPAL	TTACGCCCTTCGAACATCCC	GAGGCAAGTGCAAGCCTAGT
Nt4CL	ACTGCCGAAAGGTGTGATGT	AAATCGCTGCTCCGACTCTC
NtCHI	GTCAGGCCATTGAAAAGCTC	CTAATCGTCAATGCCCCAAC
NtF3H	CAAGGCATGTGTGGATATGG	TGTGTCGTTTCAGTCCAAGG
NtDFR	AACCAACAGTCAGGGGAATG	TTGGACATCGACAGTTCCAG
NtANS	TATCCCAAATGCCCCCAACC	ATCTTCTCCTTTGGCGGCTC
NtANR	TTCCATCTCTCATGGCTGGTC	ATATGGGCGCGACAAACATC

表1 试验用到的引物序列

Table 1 Primer sequences used in the experiment

基因名称 Gene name	正向引物 Forward primer（5'-3'）	反向引物 Reverse primer（5'-3'）	备注 Note
Actin	TGAGAGATTCCGTTGCCCAGAAGT	TTCCTTACTCATGCGGTCTGCGAT	实时荧光定量PCR分析所用引物 Primers for real-time RT-qPCR analysis
Achn033551	GCATCCATGACATCACCAGC	AGCATAACCGGTGTCCCAAC
Achn036201	TGACCGGTGGTACAATGTGG	CCTGATGGTTCACCCACTCC
Achn141271	GGGCTCTCGCGATATACGAC	TCTCCAACGTGAACGACGAG
Achn145641	TCCATGACATCACCAGCGTC	AGGAAGCATAACTGGCGTCC
Achn154591	ACGACATCACCACCGTCAAT	GCCGGTCCTTCACTTGGTAG
Achn172831	GGAGTGCTCCTCGGATTGTC	CCACTTTCTGCCACCGATCA
Achn207851	CTGTGGTACCCAGAATGCCT	ATGTCGTGGATGCTTGACCG
Achn212251	AAGGCCAACCGTGAATCTCC	AGGCAATCCGACATGGGTTC
Achn218481	AGAAGTACTTCATCCGGCAGC	GGAATTGCGTTCTTGGATTGG
Achn258201	CCCTGGCAACTTATCCCGAG	CTTGCGTCGCTCCTGATCTA
Achn365361	ACGACGGCAGTGATTATCGG	CTTGTCCTCGAACCTCGTCC
Achn371351	ATTGGAGGAGCATATCGCGG	TGGATGCTTGAACGTCTCCC
Acc00493（AcMYB10）	GCCATCACCACCATCCAACA	TTCCCCAAAATTGGCTCCTCA
Acc19563（AcbHLH42）	TCGTTTAGGGCCGAGTCTAC	TTGAGAGTAGTGCGTGTCGT
pSAK-Achn365361	ACTAGTGGATCCAAAGAATTCATGTATGGCGACGACGGC	AGAAGTACTCTCGAGAAGCTTTACATGGGATAGTTGAAGTTTTGGTACCC	过表达载体构建所用引物 Primers used for overexpression vector construction
pSAK-AcMYB10	ACTAGTGGATCCAAAGAATTCATGGAAAGTGTTACTTTAGGAGTGAGAAAGG	AGAAGTACTCTCGAGAAGCTTTAATCATCACCTAAGAGATCCCAAAGGTTAACA
pSAK-AcbHLH42	ACTAGTGGATCCAAAGAATTCATGGCGGCTCCCCCT	AGAAGTACTCTCGAGAAGCTTCAGGGTATGATTTGGTGTATTGCTCTCT
NtActin	AATGGAACTGGAATGGTCAAGGC	TGCCAGATCTTCTCCATGTCATCCCA	烟草RT-qPCR分析所用引物 Primers for real-time RT-qPCR analysis in tobacco
AcMYB88	ACGACGGCAGTGATTATCGG	CTTGTCCTCGAACCTCGTCC
AcMYB10	GCCATCACCACCATCCAACA	TTCCCCAAAATTGGCTCCTCA
AcbHLH42	TCGTTTAGGGCCGAGTCTAC	TTGAGAGTAGTGCGTGTCGT
NtC4H	ACAACCCGGATCACTGGAAG	ACTGTCCACCTTTCTCCGTG
NtCHS	TTGTTCGAGCTTGTCTCTGC	AGCCCAGGAACATCTTTGAG
NtPAL	TTACGCCCTTCGAACATCCC	GAGGCAAGTGCAAGCCTAGT
Nt4CL	ACTGCCGAAAGGTGTGATGT	AAATCGCTGCTCCGACTCTC
NtCHI	GTCAGGCCATTGAAAAGCTC	CTAATCGTCAATGCCCCAAC
NtF3H	CAAGGCATGTGTGGATATGG	TGTGTCGTTTCAGTCCAAGG
NtDFR	AACCAACAGTCAGGGGAATG	TTGGACATCGACAGTTCCAG
NtANS	TATCCCAAATGCCCCCAACC	ATCTTCTCCTTTGGCGGCTC
NtANR	TTCCATCTCTCATGGCTGGTC	ATATGGGCGCGACAAACATC

表2 农杆菌瞬时转化烟草组合

Table 2 Agrobacterium combinations for tobacco transient transformation

对照组 Control group	试验组 Experimental group
EV	OE10
EV	OE88
EV:OE10 : OE42（1:1:1）	OE88:OE10:OE42（1:1:1）
EV:OE10（1:1）	OE88:OE10（1:1）

图1 猕猴桃MYB蛋白家族系统进化分析

Fig. 1 Phylogenetic analysis of the MYB protein family in kiwifruit

表3 12个猕猴桃MYB转录因子理化性质分析

Table 3 Analysis of the physicochemical properties of 12 kiwifruit MYB transcription factors

蛋白名称 Protein name	拟南芥同源蛋白 Homologous protein of Arabidopsis thaliana	氨基酸数 Number of amino acids	分子量 Molecular weight/Da	等电点 pI	带负电荷残基Asp+GIu	带正电荷残基 Arg+Lys	不稳定指数Instability	脂肪指数 Aliphatic index	亲水性 GRAVY	亚细胞定位Subcellular localization
Achn033551	AT1G49010.1	288	31 272.05	6.67	31	28	57.11	66.81	-0.54	细胞核Nucleus
Achn036201	AT2G38090.1	294	33 491.45	8.99	31	35	51.55	59.69	-0.79	细胞核Nucleus
Achn141271	AT2G38090.1	269	30 463.48	8.27	31	33	46.22	68.10	-0.58	细胞核Nucleus
Achn145641	AT1G49010.1	303	32 847.73	6.88	31	29	59.61	63.43	-0.61	细胞核Nucleus
Achn154591	AT2G38090.1	298	33 813.85	8.77	33	36	52.52	59.60	-0.81	细胞核Nucleus
Achn172831	AT5G58900.1	290	33 039.98	7.24	35	35	65.34	58.14	-0.87	细胞核Nucleus
Achn207851	AT5G08520.1	200	22 325.81	5.97	26	22	51.90	70.65	-0.62	细胞核Nucleus
Achn212251	AT2G38090.1	273	30 842.68	8.99	32	36	48.13	70.73	-0.69	细胞核Nucleus
Achn218481	AT5G58900.1	286	32 870.57	9.22	34	39	59.06	53.22	-1.02	细胞核Nucleus
Achn258201	AT5G08520.1	423	45 538.79	5.84	54	45	52.14	71.18	-0.54	细胞核Nucleus
Achn365361	AT5G04760.1	212	24 232.82	6.07	30	26	42.43	62.97	-0.81	细胞核Nucleus
Achn371351	AT5G08520.1	279	31 022.69	8.46	31	33	62.22	65.02	-0.67	细胞核Nucleus

表4 猕猴桃MYB蛋白的磷酸化位点

Table 4 Phosphorylation sites of MYB proteins in kiwifruit

蛋白名称Protein name	丝氨酸Ser	苏氨酸Thr	酪氨酸Tyr
Achn033551	21	7	1
Achn036201	19	15	1
Achn141271	15	12	1
Achn145641	27	7	1
Achn154591	22	11	1
Achn172831	19	10	2
Achn207851	16	7	2
Achn212251	18	11	2
Achn218481	19	13	6
Achn258201	38	11	1
Achn365361	11	9	3
Achn371351	29	14	4

表5 12个猕猴桃MYBs蛋白的二级结构数量统计

Table 5 Secondary structure statistics of 12 AcMYBs %

蛋白名称 Protein name	α-螺旋 α-helix	延伸链 Extended stran	β-转角 β-turn	无规则卷曲 Random coil
Achn033551	22.22	12.50	3.47	61.81
Achn036201	22.79	10.88	3.40	62.93
Achn141271	24.16	11.52	2.97	61.34
Achn145641	19.80	12.54	3.96	63.70
Achn154591	23.83	11.74	2.68	61.74
Achn172831	24.14	15.17	3.79	56.90
Achn207851	25.50	13.00	5.00	56.50
Achn212251	23.81	13.55	3.66	58.97
Achn218481	20.63	15.03	3.15	61.19
Achn258201	27.19	13.95	4.49	54.37
Achn365361	26.89	11.32	5.19	56.60
Achn371351	21.51	12.54	2.15	63.80

图2 12个MYB蛋白二级结构预测

Fig. 2 Secondary structure prediction of 12 MYB proteins

图3 12个MYB蛋白motif 分析和保守结构域分析

Fig. 3 Motif prediction and conserved domain analysis of 12 AcMYB proteins

图4 12 AcMYBs上游启动子元件的种类和数量

Fig. 4 Types and numbers of promoter elements in the upstream regions of 12 AcMYBs

图5 ‘东红’果实不同发育时期14个MYB基因表达聚类热图 DAF：花后天数。每个基因用一行表示，每个发育时期用一列表示。数字表示该基因相对表达量。暗红色表示相对表达量较高，而相对表达量较低的基因用深蓝色表示

Fig. 5 Expression heatmap of 14 MYB genes during different development stage of ‘Donghong’ DAF: The day after flower. Each gene is indicated by a row and each developmental period is indicated by a column. The figure represents relative expression level of genes. Dark red color indicates high relative expression, while genes with low relative expression are indicated in dark blue

图6 Achn365361转录因子的系统进化分析

Fig. 6 Phylogenetic analysis of Achn365361 transcription factor in Actinidia chinensis

图7 过表达AcMYB10和AcMYB88促进烟草花青苷积累及相关基因表达 A：过表达AcMYB10、AcMYB88和EV烟草叶片的表型；B：转基因烟草叶片中花青苷含量；C：花青苷相关结构基因在转基因烟草叶片中的表达水平； EV：空载；OE88：过表达- AcMYB88；OE10：过表达-AcMYB10；PAL：苯丙氨酸裂解酶；C4H：肉桂酸-4-羟化酶；4CL：4-香豆酸辅酶 A 连接酶；CHS：查尔酮合成酶；CHI：查尔酮异构酶；F3H：黄烷酮-3-羟化酶；DFR：二氢黄酮醇-4-还原酶；LDOX：无色花青苷双加氧酶；ANR：花青苷还原酶；ANS：无色花青苷合成酶；所有图表均采用独立样本t检验。*：P < 0.05；**：P < 0.01。下同

Fig. 7 Overexpression of AcMYB10 and AcMYB88 promotes tobacco anthocyanin accumulation and related gene expression A: Phenotypes of tobacco leaves overexpressing AcMYB10, AcMYB88 and EV. B: Anthocyanin content in transgenic tobacco leaves. C: Expression levels of anthocyanin-related structural genes in transgenic tobacco leaves. EV: Empty vector. OE88: Overexpression-AcMYB88. OE10: Overexpressive-AcMYB10. PAL: Phenylalaninammo-nialyase. C4H: cinnamate-4-hydroxylase. 4CL: 4-coumaryl. CoA: Ligase. CHS: Chalcone synthase. CHI: Chalcone isomerase. F3H: Flavonol-3-hydroxylase. DFR: Dihydroflavonol reductase. LDOX: Leucoanthocyanidin dioxygenase. ANR: Anthocyanidin reductase. ANS: Anthocyanidin synthase. All graphs are based on independent samples t test. *: P < 0.05; **: P < 0.01. The same below

图8 过表达EV+OE10+OE42和OE88+OE10+OE42促进烟草花青苷积累及相关基因表达 A：过表达EV+OE10+OE42和OE88+OE10+OE42烟草叶片的表型；B：转基因烟草叶片中花青苷含量；C：花青苷相关结构基因在转基因烟草叶片中的表达水平； EV+OE10 +OE42：空载+过表达-AcMYB10+过表达-bHLH42（1:1:1）；OE88+OE10+OE42：过表达-AcMYB88+过表达-AcMYB10+过表达-bHLH42（1:1:1）

Fig. 8 Overexpression of EV+OE10+OE42 and OE88+OE10+OE42 promotes tobacco anthocyanin accumulation and related gene expression A: Phenotypes of tobacco leaves overexpressing EV+OE10+OE42 and OE88+OE10+OE42. B: Anthocyanin content in transgenic tobacco leaves. C: Expression levels of anthocyanin-related structural genes in transgenic tobacco leaves. Achn365361：AcMYB88；EV+OE10 +OE42: Empty vector+Overexpression-AcMYB10+Overexpression-bHLH42（1:1:1）. OE88+OE10+OE42: Overexpression-AcMYB88+Overexpression-AcMYB10+Overexpression-bHLH42（1:1:1）

图9 过表达EV+10和88+10促进烟草花青苷积累及相关基因表达 A：过表达EV+10和88+10烟草叶片的表型；B：转基因烟草叶片中花青苷含量；C：花青苷相关结构基因在转基因烟草叶片中的表达水平；EV+10：空载+过表达-AcMYB10（1:1）；88+10：过表达-AcMYB88+过表达-AcMYB10（1:1） A: Phenotypes of tobacco leaves overexpressing EV+10和88+10. B: Anthocyanin content in transgenic tobacco leaves. C: Expression levels of anthocyanin-related structural genes in transgenic tobacco leaves. Achn365361: AcMYB88; EV+10: Empty vector+Overexpression-AcMYB10（1:1）. OE88+10: Overexpression-AcMYB88+Overexpression-AcMYB10（1:1）

Fig. 9 Overexpression of EV+10 and 88+10 promotes tobacco anthocyanin accumulation and related gene expression

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猕猴桃AcMYB88的鉴定及功能研究

Identification and Function Analysis of AcMYB88 in Kiwifruit （Actinidia chinensis）

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