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Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (1): 46-61.doi: 10.3724/SP.J.1006.2023.24005

• CROP GENETICS & BREEDING · GERMPLASM RESOURCES · MOLECULAR GENETICS • Previous Articles     Next Articles

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 Online:2023-01-12 Published:2022-04-20
  • Contact: QUE You-Xiong E-mail:wanghengbo_0354@126.com;1223134902@qq.com;queyouxiong@126.com
  • 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)

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

Table 1

Primers used in this study"

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

Table 2

Physicochemical properties of SsNAC-ATAF members in Saccharum spontaneum"

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

Fig. 1

Sequence alignment of NAC-ATAF subfamily proteins from sugarcane and Arabidopsis"

Fig. 2

Phylogenetic tree of NAC-ATAF subfamily members from some species with the prediction of these conserved motifs These NAC-ATAF members are from different species. ZmNAC: Zea mays; ANAC or ATAF1/2: Arabidopsis thaliana; Oryza sativa: OsNAC; SbNAC: Sorghum bicolor; AAX85979.1, GmNAC: Glycine max; AIS71992.1, HaNAC1: Haloxylon ammodendron; AIS74872.1, MlNAC5: Miscanthus lutarioriparius; AAW62955.1, SsNAC23: Saccharum officinarum; ScNAC2: S. hybrid; HORVU1Hr1G063740.1, HvNAC6: Hordeum vulgare."

Fig. 3

Cis-acting elements prediction"

Fig. 4

Nucleic acid sequence and deduced amino acid sequence of ScNAC2 Underlined: the NAM conserved domain of ScNAC2 protein. *: stop codon."

Fig. 5

Relative expression level of ScNAC2 gene in different tissues of sugarcane R: root; B: bud; SP: stem pith; SE: stem epidermis; L: leaf. The error bar represents the standard error of each group treatment (n = 3). Different lowercase letters indicate significant differences at the 5% probability level."

Fig. 6

Relative expression level of ScNAC2 gene under different exogenous stresses The relative expression level of ScNAC2 gene under SA, MeJA, ABA, sodium chloride, and 4℃ cold temperatures. Y-axis represents the relative expression level of ScNAC2 gene; X-axis represents the different treatment times. The error bar represents the standard error of each group treatment (n = 3). Different lowercase letter indicates the significant differences at the 5% probability level."

Fig. 7

Subcellular localization of ScNAC2 protein The results contained photographs taken in three fields of view, visual field, green fluorescence, and merged field. 35S::GFP: GV3101 bacterial solution injection in N. benthamiana leaf by empty vector; 35S::ScNAC2::GFP: GV3101 bacterial solution injection in N. benthamiana leaf by recombinant vector."

Fig. 8

Transcriptional activation activity validation of ScNAC2 protein SD/-Trp: the synthetic dropout medium without tryptophan plate; SD/-Trp-His (+X-α-Gal+AbA): the synthetic dropout medium without tryptophan and histidine plate (add 5-Bromo-4-chloro-3-indolyl-alpha-D-galactopyranoside and Aureobasidin A); SD/-Trp-His-Ade (+X-α- Gal+AbA): the synthetic dropout medium without tryptophan, histidine, and adenine plate (add 5-Bromo-4-chloro-3-indolyl-alpha-D-galactopyranoside and Aureobasidin A)."

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