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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)."

[1] Duval M, Hsieh T F, Kim S Y, Thomas T L. Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol Biol, 2002, 50: 237-248.
doi: 10.1023/A:1016028530943
[2] Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res, 2003, 10: 239-247.
doi: 10.1093/dnares/10.6.239
[3] Souer E, van Houwelingen A, Kloos D, Mol J, Koes R. The no apical meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell, 1996, 85: 159-170.
pmid: 8612269
[4] Takada S, Hibara K, Ishida T, Tasaka M. The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development, 2001, 128: 1127-1135.
doi: 10.1242/dev.128.7.1127
[5] Aida M, Ishida T, Tasaka M. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development, 1999, 126: 1563-1570.
doi: 10.1242/dev.126.8.1563
[6] Christianson J A, Dennis E S, Llewellyn D J, Wilson I W. ATAF NAC transcription factors: regulators of plant stress signaling. Plant Signal Behav, 2010, 5: 428-432.
doi: 10.4161/psb.5.4.10847 pmid: 20118664
[7] Delessert C, Kazan K, Wilson I W, Van Der Straeten D, Manners J, Dennis E S, Dolferus R. The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J, 2005, 43: 745-757.
doi: 10.1111/j.1365-313X.2005.02488.x
[8] Jensen M K, Rung J H, Gregersen P L, Gjetting T, Fuglsang A T, Hansen M, Joehnk N, Lyngkjaer M F, Collinge D B. The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol Biol, 2007, 65: 137-150.
doi: 10.1007/s11103-007-9204-5
[9] 马雪祺, 阴艳红, 冯婧娴, 陈万生, 孙连娜, 肖莹. 植物NAC转录因子研究进展. 植物生理学报, 2021, 57: 2225-2234.
Ma X Q, Yin Y H, Feng J X, Chen W S, Sun L N, Xiao Y. Research progress of NAC transcription factors in plant. Plant Physiol J, 2021, 57: 2225-2234 (in Chinese with English abstract).
[10] Olsen A N, Ernst H A, Leggio L L, Skriver K. DNA-binding specificity and molecular functions of NAC transcription factors. Plant Sci, 2005, 169: 785-797.
doi: 10.1016/j.plantsci.2005.05.035
[11] 李桂玲, 李思云, 刘卫群. 转录因子NAC及其在植物生长发育中的作用. 分子植物育种, 2019, 17: 811-826.
Li G L, Li S Y, Liu W Q. Transcription factor NAC and its role in plant growth and development. Mol Plant Breed, 2019, 17: 811-826. (in Chinese with English abstract)
[12] Nakashima K, Tran L S, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K. Functional analysis of a NAC-type transcription factor OsNAC6involved in abiotic and biotic stress-responsive gene expression in rice. Plant J, 2007, 51: 617-630.
pmid: 17587305
[13] Jin H, Huang F, Cheng H, Song H, Yu D. Overexpression of the GmNAC2gene, an NAC transcription factor, reduces abiotic stress tolerance in tobacco. Plant Mol Biol Rep, 2013, 31: 435-442.
doi: 10.1007/s11105-012-0514-7
[14] Wang X, Basnayake B M, Zhang H, Li G, Li W, Virk N, Mengiste T, Song F. The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. Mol Plant Microbe Interact, 2009, 22: 1227-1238.
doi: 10.1094/MPMI-22-10-1227
[15] Wu Y, Deng Z, Lai J, Zhang Y, Yang C, Yin B, Zhao Q, Zhang L, Li Y, Yang C, Xie Q. Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res, 2009, 19: 1279-1290.
doi: 10.1038/cr.2009.108
[16] Lu P L, Chen N Z, An R, Su Z, Qi B S, Ren F, Chen J, Wang X C. A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol, 2007, 63: 289-305.
doi: 10.1007/s11103-006-9089-8
[17] Jensen M K, Hagedorn P H, De Torres-Zabala M, Grant M R, Rung J H, Collinge D B, Lyngkjaer M F. Transcriptional regulation by an NAC (NAM-ATAF1, 2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J, 2008, 56: 867-880.
doi: 10.1111/j.1365-313X.2008.03646.x
[18] Nogueira F T S, Schlögl P S, Camargo S R, Fernandez J H, De Rosa V E, Pompermayer P, Arruda P. SsNAC23, a member of the NAC domain protein family, is associated with cold, herbivory and water stress in sugarcane. Plant Sci, 2005, 169: 93-106.
doi: 10.1016/j.plantsci.2005.03.008
[19] Carrillo-Bermejo E A, Gamboa-Tuz S D, Pereira-Santana A, Keb-Llanes M A, Castaño E, Figueroa-Yañez L J, Rodriguez-Zapata L C. The SoNAP gene from sugarcane (Saccharum officinarum) encodes a senescence-associated NAC transcription factor involved in response to osmotic and salt stress. J Plant Res, 2020, 133: 897-909.
doi: 10.1007/s10265-020-01230-y pmid: 33094397
[20] Peng X, Zhao Y, Li X, Wu M, Chai W, Sheng L, Wang Y, Dong Q, Jiang H, Cheng B. Genomewide identification, classification and analysis of NAC type gene family in maize. J Genet, 2015, 94: 377-390.
pmid: 26440076
[21] Kadier Y, Zu Y Y, Dai Q M, Song G, Lin S W, Sun Q P, Pan J B, Lu M. Genome-wide identification, classification and expression analysis of NAC family of genes in sorghum [Sorghum bicolor (L.) Moench]. Plant Growth Regul, 2017, 83: 301-312.
doi: 10.1007/s10725-017-0295-y
[22] 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
[23] Feng M, Yu Q, Chen Y, Fu Z, Xu L, Guo J. ScMT10, a metallothionein-like gene from sugarcane, enhances freezing tolerance in Nicotiana tabacum transgenic plants. Environ Exp Bot, 2022, 194: 104750.
doi: 10.1016/j.envexpbot.2021.104750
[24] Liu F, Huang N, Wang L, Ling H, Sun T, Ahmad W, Muhammad K, Guo J, Xu L, Gao S, Que Y, Su Y. A novel l-ascorbate peroxidase 6 gene, ScAPX6, plays an important role in the regulation of response to biotic and abiotic stresses in sugarcane. Front Plant Sci, 2018, 8: 2262-2262.
doi: 10.3389/fpls.2017.02262
[25] 苏亚春, 李聪娜, 苏炜华, 尤垂淮, 岑光莉, 张畅, 任永娟, 阙友雄. 甘蔗割手密种类甜蛋白家族鉴定及栽培种同源基因功能分析. 作物学报, 2021, 47: 1275-1296.
doi: 10.3724/SP.J.1006.2021.04192
Su Y C, Li C N, Su W H, You C H, Cen G L, Zhang C, Ren Y J, Que Y X. Identification of thaumatin-like protein family in Saccharum spontaneum and functional analysis of its homologous gene in sugarcane cultivar. Acta Agron Sin, 2021, 47: 1275-1296. (in Chinese with English abstract)
[26] Xue B, Guo J, Que Y, Fu Z, Wu L, Xu L. Selection of suitable endogenous reference genes for relative copy number detection in sugarcane. Int J Mol Sci, 2014, 15: 8846-8862.
doi: 10.3390/ijms15058846 pmid: 24857916
[27] Livak K J, Schmittgen T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 2001, 25: 402-408.
doi: 10.1006/meth.2001.1262 pmid: 11846609
[28] 黄宁, 惠乾龙, 方振名, 李姗姗, 凌辉, 阙友雄, 袁照年. 甘蔗β-胡萝卜素异构酶基因家族的鉴定、定位和表达分析. 作物学报, 2021, 47: 882-893.
doi: 10.3724/SP.J.1006.2021.04128
Huang N, Hui Q, Fang Z M, Li S S, Ling H, Que Y X, Yuan Z N. Identification, localization and expression analysis of beta-carotene isomerase gene family in sugarcane. Acta Agron Sin, 2021, 47: 882-893. (in Chinese with English abstract)
doi: 10.3724/SP.J.1006.2021.04128
[29] Yang X, Wang X, Ji L, Yi Z, Fu C, Ran J, Hu R, Zhou G. Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis. Plant Cell Rep, 2015, 34: 943-958.
doi: 10.1007/s00299-015-1756-2
[30] Lu M, Ying S, Zhang D F, Shi Y S, Song Y C, Wang T Y, Li Y. A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep, 2012, 31: 1701-1711.
doi: 10.1007/s00299-012-1284-2
[31] Ohnishi T, Sugahara S, Yamada T, Kikuchi K, Yoshiba Y, Hirano H Y, Tsutsumi N. OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genetic syst, 2005, 80: 135-139.
doi: 10.1266/ggs.80.135
[32] Jannoo N, Grivet L, Chantret N, Garsmeur O, Glaszmann J C, Arruda P, D’Hont A. Orthologous comparison in a gene-rich region among grasses reveals stability in the sugarcane polyploid genome. Plant J, 2007, 50: 574-585.
pmid: 17425713
[33] Hufford M B, Seetharam A S, Woodhouse M R, Chougule K M, Dawe R K. De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science, 2021, 373: 655-662.
doi: 10.1126/science.abg5289
[34] Zhang J, Zhang X, Tang H, Zhang Q, Hua X, Ma X, Zhu F, Jones T, Zhu X, Bowers J, Wai C M, Zheng C, Shi Y, Chen S, Xu X, Yue J, Nelson D R, Huang L, Li Z, Xu H, Zhou D, Wang Y, Hu W, Lin J, Deng Y, Pandey N, Mancini M, Zerpa D, Nguyen J K, Wang L, Yu L, Xin Y, Ge L, Arro J, Han J O, Chakrabarty S, Pushko M, Zhang W, Ma Y, Ma P, Lv M, Chen F, Zheng G, Xu J, Yang Z, Deng F, Chen X, Liao Z, Zhang X, Lin Z, Lin H, Yan H, Kuang Z, Zhong W, Liang P, Wang G, Yuan Y, Shi J, Hou J, Lin J, Jin J, Cao P, Shen Q, Jiang Q, Zhou P, Ma Y, Zhang X, Xu R, Liu J, Zhou Y, Jia H, Ma Q, Qi R, Zhang Z, Fang J, Fang H, Song J, Wang M, Dong G, Wang G, Chen Z, Ma T, Liu H, Dhungana S R, Huss S E, Yang X, Sharma A, Trujillo J H, Martinez M C, Hudson M, Riascos J J, Schuler M, Chen L-Q, Braun D M, Li L, Yu Q, Wang J, Wang K, Schatz M C, Heckerman D, Van Sluys M-A, Souza G M, Moore P H, Sankoff D, VanBuren R, Paterson A H, Nagai C, Ming R. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet, 2018, 50: 1565-1573.
doi: 10.1038/s41588-018-0237-2
[35] Gong L, Zhang H, Liu X, Gan X, Nie F, Yang W, Zhang L, Chen Y, Song Y, Zhang H. Ectopic expression of HaNAC1, an ATAF transcription factor from Haloxylon ammodendron, improves growth and drought tolerance in transgenic Arabidopsis. Plant Physiol Biochem, 2020, 151: 535-544.
doi: 10.1016/j.plaphy.2020.04.008
[36] D'Hont A, Grivet L, Feldmann P, Glaszmann J C, Rao S, Berding N. Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics. Mol Gen Genet, 1996, 250: 405-413.
[37] 张欢, 杨乃科, 商丽丽, 高晓茹, 刘庆昌, 翟红, 高少培, 何绍贞. 甘薯抗旱相关基因IbNAC72的克隆与功能分析. 作物学报, 2020, 46: 1649-1658.
doi: 10.3724/SP.J.1006.2020.04051
Zhang H, Yagn N K, Shang L L, Gao X R, Liu Q C, Zhai H, Gao S P, He S Z. Cloning and functional analysis of a drought tolerance-related gene IbNAC72 in sweet potato. Acta Agron Sin, 2020, 46: 1649-1658. (in Chinese with English abstract)
[38] Hong Y, Zhang H, Huang L, Li D, Song F. Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in rice. Front Plant Sci, 2016, 7: 4.
doi: 10.3389/fpls.2016.00004 pmid: 26834774
[39] Liu W, Zhao B G, Chao Q, Wang B, Zhang Q, Zhang C, Li S, Jin F, Yang D, Li X. Function analysis of ZmNAC33, a positive regulator in drought stress response in Arabidopsis. Plant Physiol Biochem, 2019, 145: 174-183.
doi: 10.1016/j.plaphy.2019.10.038
[40] Vlot A C, Dempsey D M A, Klessig D F. Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol, 2009, 47: 177-206.
doi: 10.1146/annurev.phyto.050908.135202 pmid: 19400653
[41] 龙亚芹, 王万东, 王美存, 陈于福, 解德宏, 陈华蕊, 俞艳春, 尼章光. 水杨酸(SA)诱导植物对病虫害产生抗性及作用机制研究. 热带农业科学, 2009, 29(12): 46-50.
Long Y Q, Wang W D, Wang M C, Chen Y F, Xie D H, Chen H R, Yu Y C, Ni Z G. Salicylic acid induced resistance of plants against insects and diseases and its interaction mechanism. Chin J Trop Agric, 2009, 29(12): 46-50. (in Chinese with English abstract)
[42] 蒋旭, 崔会婷, 王珍, 张铁军, 龙瑞才, 杨青川, 康俊梅. 紫花苜蓿MsNST的克隆及对木质素与纤维素合成的功能分析. 中国农业科学, 2020, 53: 3818-3832.
Jiang X, Cui H T, Wang Z, Zhang T J, Long R C, Yang Q C, Kang J M. Cloning and function analysis of MsNST in lignin and cellulose biosynthesis pathway from alfalfa. Sci Agric Sin, 2020, 53: 3818-3832. (in Chinese with English abstract)
[43] Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics, 2010, 284: 173-183.
doi: 10.1007/s00438-010-0557-0
[44] Bang S W, Choi S, Jin X, Jung S E, Choi J W, Seo J S. Transcriptional activation of rice CINNAMOYL-CoA REDUCTASE 10 by OsNAC5, contributes to drought tolerance by modulating lignin accumulation in roots. Plant Biotechnol J, 2022, 20: 736-747
doi: 10.1111/pbi.13752
[45] Jensen M K, Lindemose S, Masi F D, Reimer J J, Nielsen M, Perera V, Workman C T, Turck F, Grant M R, Mundy J, Petersen M, Skriver K. ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Bio, 2013, 3: 321-327.
doi: 10.1016/j.fob.2013.07.006
[46] 张艳馥, 沙伟. 转录因子概述. 生物学教学, 2009, 34(10): 7-8.
Zhang F X, Sha W. Overview of transcription factors. Biol Teach, 2009, 34(10): 7-8. (in Chinese with English abstract)
[47] Zhong R, Richardson E A, Ye Z H. The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell, 2007, 19: 2776-2792.
doi: 10.1105/tpc.107.053678
[48] Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T. VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell, 2010, 22: 1249-1263.
doi: 10.1105/tpc.108.064048
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