|TaNF-YB11, a gene of NF-Y transcription factor family in Triticum aestivum, confers drought tolerance on plants via modulating osmolyte accumulation and reactive oxygen species homeostasis
|ZHAO Ying-jia, ZHANG Yan-yang, BAI Xin-yang, LIN Rui-ze, SHI Gui-qing, DU Ping-ping, XIAO Kai
|State Key Laboratory of North China Crop Improvement and Regulation, Hebei Agricultural University/College of Agronomy, Hebei Agricultural University, Baoding 071001, P.R.China
摘要 转录因子（TFs）调控多种逆境防御相关的生理过程和植物逆境响应。本研究中，作者鉴定了小麦NF-YB转录因子家族基因TaNF-YB11介导植物抵御干旱逆境能力的特征。TaNF-YB11含有NF-YB家族特有的保守结构域，该基因编码蛋白经内质网分选后靶向细胞核内。酵母双杂交分析表明，TaNF-YB11分别与NF-YA家族成员TaNF-YA2和NF-YC家族成员TaNF-YC3在蛋白水平上相互作用。这些结果表明，上述TF蛋白通过组建异源三聚体对下游基因进行转录调控。在27 h干旱条件下，根和叶中TaNF-YB11转录本数量较正常生长对照增多。此外，干旱上调的TaNF-YB11表达水平随正常恢复处理进程逐渐下调，表明该基因参与了植物对干旱逆境的响应过程。TaNF-YB11具有赋予植株抵御抗旱逆境的能力; 干旱处理下，过表达TaNF-YB11株系植株表型和生物量均高于野生型对照，这主要与该基因促进气孔关闭、增强渗透物质积累能力和改善细胞活性氧(ROS)稳态有关。调控脯氨酸生物合成P5CS家族基因TaP5CS2在TaNF-YB11株系中呈上调表达模式，干旱胁迫下下调表达TaP5CS2株系脯氨酸积累量减少。与此类似，编码超氧化物歧化酶(SOD) TaSOD2和过氧化氢酶(CAT)基因TaCAT3在过表达TaNF-YB11株系中上调表达，上述细胞保护酶基因通过调节SOD和CAT活性在改善干旱处理下细胞ROS稳态中发挥重要作用。RNA-seq分析结果显示，与“细胞过程”、“环境信息处理”、“遗传信息加工”、“代谢”和“机体系统”相关的众多基因受到TaNF-YB11转录调节。本研究结果表明，TaNF-YB11通过在转录组水平上对干旱逆境响应相关的不同生物学过程基因进行调控，增强植株抵御干旱逆境的能力。综上，TaNF-YB11在介导植株抵御干旱逆境中发挥重要作用，该基因可作为小麦抗旱分子育种的重要基因资源。
Transcription factors (TFs) regulate diverse stress defensive-associated physiological processes and plant stress responses. We characterized TaNF-YB11, a gene of the NF-YB TF family in Triticum aestivum, in mediating plant drought tolerance. TaNF-YB11 harbors the conserved domains specified by its NF-YB partners and targets the nucleus after the endoplasmic reticulum (ER) assortment. Yeast two-hybrid assay indicated the interactions of TaNF-YB11 with TaNF-YA2 and TaNF-YC3, two proteins encoded by genes in the NF-YA and NF-YC families, respectively. These results suggested that the heterotrimer established among them further regulated downstream genes at the transcriptional level. The transcripts of TaNF-YB11 were promoted in roots and leaves under a 27-h drought regime. Moreover, its upregulated expression levels under drought were gradually restored following a recovery treatment, suggesting its involvement in plant drought response. TaNF-YB11 conferred improved drought tolerance on plants; the lines overexpressing target gene displayed improved phenotype and biomass compared with wild type (WT) under drought treatments due to enhancement of stomata closing, osmolyte accumulation, and cellular reactive oxygen species (ROS) homeostasis. Knockdown expression of TaP5CS2, a P5CS family gene modulating proline biosynthesis that showed upregulated expression in drought-challenged TaNF-YB11 lines, alleviated proline accumulation of plants treated by drought. Likewise, TaSOD2 and TaCAT3, two genes encoding superoxide dismutase (SOD) and catalase (CAT) that were upregulated underlying TaNF-YB11 regulation, played critical roles in ROS homeostasis via regulating SOD and CAT activities. RNA-seq analysis revealed that numerous genes associated with processes of ‘cellular processes’, ‘environmental information processing’, ‘genetic information processing’, ‘metabolism’, and ‘organismal systems’ modified transcription under drought underlying control of TaNF-YB11. These results suggested that the TaNF-YB11-mediated drought response is possibly accomplished through the target gene in modifying gene transcription at the global level, which modulates complicated biological processes related to drought response. TaNF-YB11 is essential in plant drought adaptation and a valuable target for molecular breeding of drought-tolerant cultivars in T. aestivum.
Received: 19 April 2021
Accepted: 08 July 2021
|Fund: This work was supported by the National Natural Science Foundation of China (31872869), the State Key Laboratory of North China Crop Improvement and Regulation (NCCIR2022ZZ-7), the National Key R&D Program of China (SQ2022YFD1200002), the Science and Technology Planning Project of Hebei Province, China (216Z6401G), and the Postgraduate Innovation Funding Project of Hebei Province, China (CXZZSS2021071).
|About author: Correspondence XIAO Kai, E-mail: email@example.com
Cite this article:
ZHAO Ying-jia, ZHANG Yan-yang, BAI Xin-yang, LIN Rui-ze, SHI Gui-qing, DU Ping-ping, XIAO Kai.
TaNF-YB11, a gene of NF-Y transcription factor family in Triticum aestivum, confers drought tolerance on plants via modulating osmolyte accumulation and reactive oxygen species homeostasis. Journal of Integrative Agriculture, 21(11): 3114-3130.
| Ábrahám E, Hourton-Cabassa C, Erdei L, Szabados L. 2010. Methods for determination of proline in plants. In: Sunkar R, ed., Plant Stress Tolerance: Methods and Protocols. Methods in Molecular Biology. Humana Press, New York, NY. pp. 317–331.
Ajithkumar I P, Panneerselvam R. 2014. ROS scavenging system, osmotic maintenance, pigment and growth status of Panicum sumatrense Roth. under drought stress. Cell Biochemistry and Biophysics, 68, 587–595.
Baldoni E, Genga A, Cominelli E. 2015. Plant MYB transcription factors: Their role in drought response mechanisms. International Journal of Molecular Sciences, 16, 15811–15851.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society (B), 57, 289–300.
Bolger A M, Lohse M, Usadel B. 2014. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.
Boyle E I, Weng S, Gollub J, Jin H, Botstein D, Cherry J M, Sherlock G. 2004. GO: TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics, 20, 3710–3715.
DaCosta M, Wang Z, Huang B. 2004. Physiological adaptation of kentucky bluegrass to localized soil drying. Crop Science, 44, 1307–1314.
Dolfini D, Gatta R, Mantovani R. 2012. NF-Y and the transcriptional activation of CCAAT promoters. Critical Review in Biochemistry and Molecular Biology, 47, 29–49.
DuBois M, Gilles K A, Hamilton J K, Rebers P A, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350–356.
Fahad S, Bajwa A A, Nazir U, Anjum S A, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan M Z, Alharby H, Wu C, Wang D, Huang J. 2017. Crop production under drought and heat stress: Plant responses and mnagement options. Frontiers in Plant Science, 8, 1147.
Frontini M, Imbriano C, Manni I, Mantovani R. 2004. Cell cycle regulation of NF-YC nuclear localization. Cell Cycle, 3, 217–222.
Fu Y, Ma H, Chen S, Gu T, Gong J. 2018. Control of proline accumulation under drought via a novel pathway comprising the histone methylase CAU1 and the transcription factor ANAC055. Journal of Experimental Botany, 69, 579–588.
Gong X, Liu M, Zhang L, Liu W, Wang C. 2013. Sucrose transporter gene atsuc4 responds to drought stress by regulating the sucrose distribution and metabolism in Arabidopsis thaliana. Advanced Materials Research, 12, 2971–2975.
Guo C, Zhao X, Liu X, Zhang L, Gu J, Li X, Lu W, Xiao K. 2013. Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta, 237, 1163–1178.
Gusmaroli G, Tonelli C, Mantovani R. 2002. Regulation of the CCAAT-Binding NF-Y subunits in Arabidopsis thaliana. Gene, 264, 173–185.
Han X, Tang S, An Y, Zheng D, Xia X, Yin W. 2013. Overexpression of the poplar NF-YB7 transcription factorconfers drought tolerance and improves water-use efficiency in Arabidopsis. Journal of Experimental Botany, 64, 4589–4601.
Hao L, Liu Xu Y, Zhang X, Sun B, Liu C, Zhang D, Tang H, Li C, Li Y, Shi Y, Xie X, Song Y, Wang T, Li Y. 2020. Genome-wide identification and comparative analysis of drought related genes in roots of two maize inbred lines with contrasting drought tolerance by RNA sequencing. Journal of Integrative Agriculture, 19, 449–464.
He F, Sheng M, Tang M. 2017. Effects of Rhizophagus irregularison photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Frontiers in Plant Science, 8, 183.
He G, Xu J, Wang Y, Liu J, Li P, Chen M, Ma Y, Xu Z. 2016. Drought-responsive WRKY transcription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis. BMC Plant Biology, 16, 116.
Huang X S, Liu J H, Chen X J. 2010. Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biology, 10, 230.
Imadi S R, Kazi A G, Ahanger M A, Gucel S, Ahmad P. 2015. Plant transcriptomics and responses to environmental stress: an overview. Journal of Genetics, 94, 525–537.
Koffler B E, Luschin-Ebengreuth N, Stabentheiner E, Müller M, Zechmann B. 2014. Compartment specific response of antioxidants to droughtstress in Arabidopsis. Plant Science, 227, 133–144.
Kreps J A, Wu Y J, Chang H S, Zhu T, Wang X, Harper J F. 2002. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology, 130, 2129–2141.
Li P, Yang X, Wang H, Pan T, Yang J, Wang Y, Xu Y, Yang Z, Xu C. 2021. Metabolic responses to combined water deficit and salt stress in maize primary roots. Journal of Integrative Agriculture, 20, 109–119.
Li X, Lü X, Wang X, Peng Q, Zhang M, Ren M. 2020. Biotic and abiotic stress-responsive genes are stimulated to resist drought stress in purple wheat. Journal of Integrative Agriculture, 19, 33–50.
Liu J X, Howell S H. 2010. bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell, 22, 782–796.
Maheshwari P, Kummari D, Palakolanu S R, Nagasai T U, Nagaraju M, Rajasheker G, Jawahar G, Jalaja N, Rathnagiri P, Kavi P B. 2019. Genome-wide identification and expression profile analysis of nuclear factor Y family genes in Sorghum bicolor L. (Moench). PLoS ONE, 14, e0222203.
Mantovani R. 1999. The molecular biology of the CCAAT-binding factor NF-Y. Gene, 239, 15–27.
Metzker M L. 2010. Applications of next-generation sequencing technologies: The next generation. Nature Reviews Genetics, 11, 31–46.
Monroe J G, Powell T, Price N, Mullen J L, Howard A, Evans K, Lovell J T, McKay J K. 2018. Drought adaptation in Arabidopsis thaliana by extensive genetic loss-of-function. eLife, 7, e41038.
Nardini M, Gnesutta N, Donati G, Gatta R, Forni C, Fossati A. 2013. Sequence-specific transcription factor NF-Y displays histone-like DNA binding and H2B-like ubiquitination. Cell, 152, 132–143.
Parre E, Ghars M A, Leprince A S, Thiery L, Lefebvre D, Bordenave M, Richard L, Mazars C, Abdelly C, Savoure A. 2007. Calcium signaling via phospholipase C is essential for proline accumulation upon ionic but not nonionic hyperosmotic stresses in Arabidopsis. Plant Physiology, 144, 503–512.
Petroni K, Kumimoto R W, Gnesutta N, Calvenzani V, Fornari M, Tonelli C. 2012. The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell, 24, 4777–4792.
Reynolds M P, Mujeer-Kazi A, Sawkins M. 2015. Prospects for utilising plant-adaptive mechanisms to improve wheat and other crops in drought- and salinity-prone environments. Annals of Applied Biology, 146, 239–259.
Robinson M D, McCarthy D J, Smyth G K. 2010. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139–140.
Sato H, Suzuki T, Takahashi F, Shinozaki K, Yamaguchi-Shinozaki K. 2019. NF-YB2 and NF-YB3 have functionally diverged and differentially induce drought and heat stress-specific genes. Plant Physiology, 180, 1677–1690.
Savouré A, Hua X J, Bertauche N, Van Montagu M, Verbruggen N. 1997. Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana. Molecular and General Genetics, 254, 104–109.
Savouré A, Jaoua S, Hua X J, Ardiles W, Van Montagu M, Verbruggen N. 1995. Isolation, characterization, and chromosomal location of a gene encoding the Δ1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Letters, 372, 13–19.
Siefers N, Dang K K, Kumimoto R W, Bynum W E T, Tayrose G, Holt B F. 2009. Tissue-specific expression patterns of Arabidopsis NF-Y transcription factors suggest potential for extensive combinatorial complexity. Plant Physiology, 149, 625–641.
Sofo A, Scopa A, Nuzzaci M, Vitti A. 2015. Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences, 16, 13561–13578.
Strizhov N, Abrahám E, Okrész L, Blickling S, Zilberstein A, Schell J, Koncz C, Szabados L. 1997. Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant Journal, 12, 557–569.
Su Z, Ma X, Guo H, Sukiran N L, Guo B, Assmann S M, Ma H. 2013. Flower development under drought stress: morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis. Plant Cell, 25, 3785–3807.
Sun Z, Ding C, Li X, Xiao K. 2012. Molecular characterization and expression analysis of TaZFP15, a C2H2-type zinc finger transcription factor gene in wheat (Triticum aestivum L.). Journal of Integrative Agriculture, 11, 31–42.
Székely G, Ábrahám E, Cséplő Á, Rigó G, Zsigmond L, Csiszár J,Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L. 2008. Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant Journal, 53, 11–28.
Tan W, Zhang D, Zhou H, Zheng T, Yin Y, Lin H. 2018. Transcription factor HAT1 is a substrate of SnRK2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought. PLoS Genetics, 14, e1007336.
Tian C, Li S, Fan C, Li Y, Zhang J, Sun J, Chen Y, Su X, Lu M, Liang C, Hu Z. 2016. Effects of drought and salt-stresses on gene expression in Caragana korshinskii seedlings revealed by RNA-seq. BMC Genomics, 17, 200.
Vanaja M, Yadav S K, Archana G, Lakshmi N J, Venkateswarlu B. 2011. Response of C4 (maize) and C3 (sunflower) crop plants to drought stress and enhanced carbon dioxide concentration. Plant Soil and Environment, 57, 207–215.
Verslues P E, Kim Y S, Zhu J K, Altered A B A. 2007. Proline and hydrogen peroxide in an Arabidopsis glutamate: Glyoxylate aminotransferase mutant. Plant Molecular Biology, 64, 205–217.
Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S. 2010. Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. Journal of Proteome Research, 9, 6561–6577.
Wang Z, Bao Y, Pei T, Wu T, Du X, He M, Wang Y, Liu Q, Yang H, Jiang J, Zhang H, Li J, Zhao T, Xu X. 2020. Silencing the SLB3 transcription factor gene decreases drought stress tolerance in tomato. Journal of Integrative Agriculture, 19, 2699–2708.
Wu J, Zhang J, Li X, Xu J J, Wang L. 2016. Identification and characterization of a PutCu/Zn-SOD gene from Puccinellia tenuiflora (Turcz.) Scribn. et Merr. Plant Growth Regulation, 79, 55–64.
Yin M, Wang Y, Zhang L, Li J, Quan W, Yang L, Wang Q, Chan Z. 2017. The Arabidopsis Cys2/His2 zinc finger transcription factor ZAT18 is a positive regulator of plant tolerance to drought stress. Journal of Experimental Botany, 68, 2991–3005.
Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchi-Shinozaki K, Wada K, Harada Y, Shinozaki K. 1995. Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant Journal, 7, 751–760.
Zhang B, Su L, Hu B, Li L. 2018. Expression of AhDREB1, an AP2/ERF transcription factor gene from peanut, is affected by histone acetylation and increases abscisic acid sensitivity and tolerance to osmotic stress in Arabidopsis. International Journal of Molecular Sciences, 19, 1441.
Zhang S, Li Y, Song G, Gao J, Zhang R, Li W, Chen M, Li G. 2020. Heterologous expression of the ThIPK2 gene enhances drought resistance of common wheat. Journal of Integrative Agriculture, 19, 941–952.
Zhang X, Liu X, Zhang D, Tang H, Sun B, Li C, Hao L, Liu C, Li Y, Shi Y, Xie X, Song Y, Wang T, Li Y. 2017. Genome-wide identification of gene expression in contrasting maize inbred lines under field drought conditions reveals the significance of transcription factors in drought tolerance. PLoS ONE, 12, e0179477.
Zhao C, Haigh A M, Holford P, Chen Z. 2018. Roles of chloroplast retrograde Signals and ion transport in plant drought tolerance. International Journal of Molecular Sciences, 19, 963.
Zhao H, Wu D, Kong F, Lin K, Zhang H, Li G. 2016. The Arabidopsis thaliana nuclear factor Y transcription factors. Frontiers in Plant Science, 7, 2045.
Zhong S, Joung J G, Zheng Y, Chen Y R, Liu B, Shao Y, Xiang J Z, Fei Z, Giovannoni J J. 2011. High-throughput Illumina strand-specific RNA sequencing library preparation. Cold Spring Harbor Protocol, 8, 940–949.
|No Suggested Reading articles found!