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作物学报 ›› 2023, Vol. 49 ›› Issue (1): 46-61.doi: 10.3724/SP.J.1006.2023.24005

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

甘蔗割手密种NAC转录因子ATAF亚家族鉴定及栽培品种ScNAC2基因的功能分析

王恒波(), 张畅(), 吴明星, 李湘, 蒋钟莉, 林容潇, 郭晋隆, 阙友雄()   

  1. 福建农林大学农业 / 农村部福建甘蔗生物学与遗传育种重点实验室 / 国家甘蔗工程技术研究中心, 福建福州 350002
  • 收稿日期:2022-01-04 接受日期:2022-03-25 出版日期:2023-01-12 网络出版日期:2022-04-20
  • 通讯作者: 阙友雄
  • 作者简介:王恒波, E-mail: wanghengbo_0354@126.com;
    张畅, E-mail: 1223134902@qq.com第一联系人：**同等贡献
  • 基金资助:
    国家重点研发计划项目(2018YFD1000503);福建省自然科学基金项目(2022J01160);财政部和农业农村部国家现代农业产业技术体系建设专项(Sugar Crop, CARS-17)

Genome-wide identification of NAC transcription factors ATAF subfamily in Sacchrum spontaneum and functional analysis of its homologous gene ScNAC2 in sugarcane cultivar

WANG Heng-Bo(), ZHANG Chang(), WU Ming-Xing, LI Xiang, JIANG Zhong-Li, LIN Rong-Xiao, GUO Jin-Long, QUE You-Xiong()   

  1. Key Laboratory of Sugarcane Biology and Genetic Breeding (Fujian), Ministry of Agriculture and Rural Affairs / Fujian Agriculture and Forestry University / National sugarcane Engineering Technology Research, Fuzhou 350002, Fujian, China
  • Received:2022-01-04 Accepted:2022-03-25 Published:2023-01-12 Published online:2022-04-20
  • Contact: QUE You-Xiong
  • About author:First author contact:**Contributed equally to this work
  • Supported by:
    National Key Research and Development Program of China(2018YFD1000503);Natural Science Foundation of Fujian Province, China(2022J01160);China Agriculture Research System of MOF and MARA(Sugar Crop, CARS-17)

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摘要：

NAC (NAM, ATAF和CUC)是陆生植物特有的转录因子家族, 包含18个亚家族, 其中ATAF亚家族成员广泛参与生物和非生物胁迫应答过程。本研究基于甘蔗割手密种基因组数据和栽培品种ROC22的cDNA文库, 首先, 通过比较基因组学方法, 对ATAF亚家族成员进行鉴定、蛋白多序列比对、系统进化分析及启动子区域顺式作用元件预测; 其次, 从甘蔗栽培品种克隆获得割手密种ATAF亚家族成员SsNAC2的同源基因ScNAC2, 在生物信息学分析基础上, 采用qRT-PCR技术分析该基因的组织特异性表达模式, 及其在不同外源胁迫下的表达特性; 最后, 对ScNAC2基因的编码蛋白进行亚细胞定位和转录激活活性试验。结果表明, 一共鉴定到6个ATAF亚家族成员, 开放读阅读框在889~1017 bp之间, 相对分子量介于32.067~35.819 kD之间, 理论等电点分布在5.09~8.92之间, 所有成员的编码蛋白被预测均定位于细胞核上。这些基因的Ka/Ks比值均小于1, 表明纯化选择在进化过程中起重要作用。蛋白的氨基酸序列比对显示, ATAF亚家族成员都含NAM保守结构域(由I、II、III、IV和V亚结构域组成)。系统进化分析揭示, 禾本科的甘蔗、高粱、玉米与水稻亚家族成员都聚类在一起, 表明有较近的亲缘关系, 同时拟南芥、水稻、玉米和高粱等40个ATAF亚家族成员分为两个组(Group A和Group B), 其中玉米ATAF亚家族发生明显的基因扩增现象。此外, ATAF亚家族成员启动子区域均包含响应低温、干旱和激素等逆境胁迫的顺式作用元件, 推测其参与多种生物和非生物胁迫的应答过程。进一步, 从甘蔗栽培品种ROC22中克隆获得ScNAC2基因的cDNA全长序列(GenBank登录号为OL982539), 其开放读码框为891 bp, 编码296个氨基酸残基; 该基因的编码蛋白与割手密种ATAF亚家族Group B 中SsNAC2蛋白的氨基酸序列相似性为97.99%。qRT-PCR表达分析结果表明, ScNAC2基因在甘蔗不同组织中组成型表达, 在蔗叶和蔗皮中表达量高于蔗肉、蔗芽和蔗根; 在水杨酸和茉莉酸甲酯胁迫下, 表达量显著下调; 在脱落酸、4℃低温和氯化钠胁迫下, ScNAC2基因的表达呈现由低到高的模式, 且差异达显著水平。亚细胞定位结果显示, ScNAC2-GFP融合蛋白定位在细胞核上。转录激活活性试验表明, ScNAC2蛋白不具有转录自激活活性。以上结果为深入解析甘蔗NAC-ATAF亚家族成员在响应生物和非生物胁迫应答中的生物学功能奠定了基础, 为甘蔗抗性分子育种提供潜在的基因资源。

关键词: 甘蔗, 转录因子, NAC基因家族, 生物和非生物胁迫, 表达模式

Abstract:

NAC (NAM, ATAF, and CUC) is a family of transcription factors unique to terrestrial plants, including 18 subfamilies, of which ATAF subfamily members are mainly involved in the response processes of biotic and abiotic stresses, such as salicylic acid (SA), methyl jasmonate acid (MeJA), abscisic acid (ABA), pathogenic bacteria, mechanical damage, low temperature, and sodium chloride (NaCl). The data were from the genomic database of Saccharum spontaneum and the cDNA library of a sugarcane cultivar ROC22. Firstly, the ATAF subfamily members in Saccharum were identified and analyzed for their protein multiple sequence alignment, phylogenetic tree construction, and promoter region cis-acting element prediction using comparative genomics methods and various bioinformatics methods. Secondly, one homologous gene of the ATAF subfamily SsNAC2, ScNAC2, was cloned from a prevalent sugarcane cultivar ROC22 in China. The qRT-PCR was used to detect the tissue-specific expression pattern and the relative expression levels of ScNAC2 gene under different exogenous stresses. Finally, the subcellular localization and the transactivation analysis of ScNAC2 protein were performed. The results showed that six members of the ATAF subfamily were identified with the open read reading frames between 889 bp and 1017 bp, relative molecular weights between 32.067 and 35.819 kD, the theoretical isoelectric points from 5.09 to 8.92, and the proteins of all members were predicted to localize on the nucleus. In addition, the Ka/Ks ratios of six gene pairs were all less than 1, indicating that purification selection played an important role during evolution. The amino acid sequence alignment indicated that all members of the ATAF subfamily contained the NAM conserved domains, consisting of I, II, III, IV, and V subdomains. Phylogenetic analysis revealed that the members from sugarcane, sorghum, maize, and rice, that belonged to Gramineae, were clustered together, indicating that they had a close evolutionary relationship. Forty members of the ATAF subfamily from Arabidopsis, rice, maize, and sorghum were divided into two groups (Group A and Group B), in which the subfamily members of maize had obvious gene expansion. Furthermore, the promoter regions of ATAF subfamily members all contained cis-acting elements that responded to stresses such as low temperature, drought, and hormones, and we thus speculated that they were involved in the response processes of a variety of biotic and abiotic stresses. Furthermore, the full-length cDNA sequence of the ScNAC2 gene (GenBank accession number: OL982539) was cloned from the sugarcane cultivar ROC22, with an open reading frame of 891 bp and encoding 296 amino acid residues. The similarity of amino acid sequence between ScNAC2 and SsNAC2 proteins both from ATAF subfamily Group B was 97.99%. The qRT-PCR showed that the ScNAC2 gene was constitutively expressed in different tissues of sugarcane, and its expression level in sugarcane leaves and stem epidermis was higher than that in stem piths, buds, and roots. Besides, the relative expression level of ScNAC2 gene was significantly down-regulated under SA and MeJA stresses, however, it showed an expression pattern from low to high and varied to significant levels under the stress of ABA, 4℃, and NaCl. Subcellular localization revealed that the ScNAC2-GFP fusion protein was localized in the cell nucleus of Nicotiana benthamiana leaves. Furthermore, the transactivation experiment showed that ScNAC2 protein did not have the transcriptional self-activation activity. The above results established the foundation for identifying the biological functions of sugarcane NAC-ATAF subfamily members in response to biotic and abiotic stresses and provided potential genetic resources for sugarcane resistance molecular breeding.

Key words: sugarcane, transcription factor, NAC gene family, biotic and abiotic stress, the relative expression pattern

表1

本研究所用引物序列"

名称 Primer name 引物序列 Primer sequence (5'-3') 备注 Note
ScNAC2-F GCAGCGAGGAACAGTCAAGA 基因克隆
Gene cloning
ScNAC2-R CTTCAATCTTAACTGACCGGC
ScNAC2-qF CAAGGAGGAGGTGGAGGA qRT-PCR
ScNAC2-qR CGAGCATGTTGCCAAAGAAG
GAPDH-F CACGGCCACTGGAAGCA 内参基因
Internal reference gene
GAPDH-R TCCTCAGGGTTCCTGATGCC
ScNAC2-gate-F GGGGACAAGTTTGTACAAAAAAGC
AGGCTTCATGGCGATGGCGACGGTGCA		 入门载体构建
Construction of entry vector
ScNAC2-gate-R GGGGACCACTTTGTACAAGAAAGC
TGGGTCGAAGAACGGGAAGCCGGCGT
ScNAC2-yeast-F ATGGGAGTGCCGGTGAGGAGGGA 酵母载体构建
Construction of yeast vector
ScNAC2-yeast-R TCAGCTCAGAATGGCCCCAACCC

表2

甘蔗割手密种SsNAC-ATAF成员的理化性质分析"

基因名称
Gene name		 基因ID
Gene ID		 开放阅读框
Opening
reading frame		 相对分子量
Molecular weight (kD)		 理论等电点
pI		 不稳定系数
Instability coefficient		 高粱直系同源基因
Orthologous gene
from sorghum		 非同义和同义替换率
Ka/Ks
SsNAC1 Sspon.001B0024840 960 35.429 6.33 34.38 Sobic.001G040200.1 0.083
SsNAC2 Sspon002C0028310 898 33.557 5.73 48.48 Sobic.002G080100.1 0.150
SsNAC3 Sspon003B0009183 937 34.974 8.58 39.64 Sobic.003G334600.1 0.314
SsNAC4 Sspon004D0012621 889 32.641 8.47 54.78 Sobic.003G379700.1 0.239
SsNAC5 Sspon005B0021590 882 32.067 5.09 43.21 Sobic.005G064600.2 0.225
SsNAC6 Sspon007C0007910 1017 35.819 8.92 51.50 Sobic.009G142200.1 0.532

图1

甘蔗和拟南芥NAC-ATAF亚家族蛋白的序列比对"

图2

NAC-ATAF的系统进化树的构建与保守基序的预测 NAC-ATAF成员分别来自: 玉米: ZmNAC; 拟南芥: ANAC或ATAF1/2; 水稻: OsNAC; 高粱: SbNAC; 大豆: AAX85979.1, GmNAC; 石兰属梭梭: AIS71992.1, HaNAC1; 芒属南荻: AIS74872.1, MlNAC5; 甘蔗热带种: AAW62955.1, SsNAC23; 甘蔗栽培品种: ScNAC2; 大麦: HORVU1Hr1G063740.1, HvNAC6。"

图3

顺式作用元件预测"

图4

ScNAC2的核酸序列及推导的氨基酸序列 下画线部分: ScNAC2蛋白的NAM保守结构域。*: 代表终止密码子。"

图5

ScNAC2基因在甘蔗不同组织的表达量 R: 蔗根; B: 蔗芽; SP: 蔗肉; SE: 蔗皮; L: 蔗叶。误差线为每组处理的标准误差(n = 3)。不同小写字母表示表示5%水平下差异的显著性。"

图6

ScNAC2基因在甘蔗不同逆境胁迫的表达模式 ScNAC2基因在水杨酸、茉莉酸甲酯、脱落酸、氯化钠和4℃低温处理下的表达量。纵坐标代表基因的表达量; 横坐标代表不同处理时间。误差线为每组处理的标准误差(n = 3)。不同小写字母表示表示5%水平下差异的显著性。"

图7

ScNAC2蛋白的亚细胞定位 该结果包含明场、绿色荧光、叠加场3个视野下拍摄的照片。35S::GFP 代表空载的GV3101菌液注射本氏烟叶片的结果; 35S::ScNAC2::GFP重组载体的GV3101菌液注射本氏烟叶片的结果。"

图8

ScNAC2转录激活活性验证 SD/-Trp: 色氨酸营养缺陷型平板培养基; SD/-Trp-His (+X-α-Gal+AbA): 色氨酸+组氨酸营养缺陷型平板培养基(添加5-溴-4-氯-3-吲哚- α-D-半乳糖苷和金担子素A); SD/-Trp-His-Ade (+X-α-Gal+AbA): 色氨酸+组氨酸+腺嘌呤营养缺陷型平板培养基(添加5-溴-4-氯-3-吲哚-α-D-半乳糖苷和金担子素A)。"

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