Genome and Transcriptome-Wide Analysis of OsWRKY and OsNAC Gene Families in Oryza sativa and Their Response to White-Backed Planthopper Infestation
Abstract
:1. Introduction
2. Results
2.1. Phylogenetic Analysis and Classification of OsWRKY and OsNAC Genes
2.2. Phylogenetic Comparison of OsWRKY and OsNAC Proteins in Arabidopsis and Rice
2.3. Orthology Relationships of OsWRKY and OsNAC Genes in Arabidopsis and Rice
2.4. Chromosomal Location and Gene Duplication
2.5. Insights into Exon–Intron Arrangements
2.6. Analysis of Conserved Motifs
2.7. Protein Interaction Networks and Functional Annotations
2.8. Gene Ontology Analysis of Rice OsWRKY and OsNAC Genes
2.9. Differential Gene Expression Analysis of OsWRKY and OsNAC Genes during WBPH Stress
3. Discussion
4. Materials and Methods
4.1. Plant Material, WBPH Infestation and RNA Extraction
4.2. Data Resources
4.3. OsWRKY and OsNAC Family Identification in O Sativa
4.4. Multiple Sequence Alignment and Phylogenetic Analysis
4.5. Chromosomal Location and Gene Duplication Analysis
4.6. Exon–Intron Organization, Identification and Analysis of Conserved Motifs
4.7. Prediction of Protein–Protein Interaction Network
4.8. Gene Ontology-Based Functional Annotation Analysis
4.9. Expression Analysis of Rice OsWRKY and OsNAC Genes in Response to WBPH Stress
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Suzuki, N.; Rivero, R.M.; Shulaev, V.; Blumwald, E.; Mittler, R. Abiotic and biotic stress combinations. New Phytol. 2014, 203, 32–43. [Google Scholar] [CrossRef] [PubMed]
- Khan, I.; Zhang, Y.; Akbar, F.; Khan, J. Abiotic Stress Tolerance in Cereals through Genome Editing. In Omics Approach to Manage Abiotic Stress in Cereals; Springer: Berlin/Heidelberg, Germany, 2022; pp. 295–319. [Google Scholar]
- Gull, A.; Lone, A.A.; Wani, N.U.I. Biotic and Abiotic Stresses in Plants. In Abiotic and Biotic Stress in Plants; IntechOpen: London, UK, 2019; pp. 1–19. [Google Scholar]
- Jang, Y.-H.; Yun, S.; Park, J.-R.; Kim, E.-G.; Yun, B.-J.; Kim, K.-M. Biological Efficacy of Cochlioquinone-9, a Natural Plant Defense Compound for White-Backed Planthopper Control in Rice. Biology 2021, 10, 1273. [Google Scholar] [CrossRef] [PubMed]
- Jan, R.; Khan, M.A.; Asaf, S.; Lee, I.-J.; Kim, K.-M. Overexpression of OsF3H modulates WBPH stress by alteration of phenylpropanoid pathway at a transcriptomic and metabolomic level in Oryza sativa. Sci. Rep. 2020, 10, 14685. [Google Scholar] [CrossRef] [PubMed]
- Jan, R.; Khan, M.A.; Asaf, S.; Lee, I.-J.; Kim, K.-M. Over-Expression of Chorismate Mutase Enhances the Accumulation of Salicylic Acid, Lignin, and Antioxidants in Response to the White-Backed Planthopper in Rice Plants. Antioxidants 2021, 10, 1680. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.; Liu, J.; Triplett, L.; Leach, J.E.; Wang, G.-L. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu. Rev. Phytopathol. 2014, 52, 213–241. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khan, I.; Khan, S.; Zhang, Y.; Zhou, J.; Akhoundian, M.; Jan, S.A. CRISPR-Cas technology based genome editing for modification of salinity stress tolerance responses in rice (Oryza sativa L.). Mol. Biol. Rep. 2021, 48, 3605–3615. [Google Scholar] [CrossRef]
- Khan, I.; Khan, S.; Zhang, Y.; Zhou, J. Genome-wide analysis and functional characterization of the Dof transcription factor family in rice (Oryza sativa L.). Planta 2021, 253, 101. [Google Scholar] [CrossRef]
- Abdullah-Zawawi, M.-R.; Ahmad-Nizammuddin, N.-F.; Govender, N.; Harun, S.; Mohd-Assaad, N.; Mohamed-Hussein, Z.-A. Comparative genome-wide analysis of WRKY, MADS-box and MYB transcription factor families in Arabidopsis and rice. Sci. Rep. 2021, 11, 19678. [Google Scholar] [CrossRef]
- Franco-Zorrilla, J.M.; López-Vidriero, I.; Carrasco, J.L.; Godoy, M.; Vera, P.; Solano, R. DNA-binding specificities of plant transcription factors and their potential to define target genes. Proc. Natl. Acad. Sci. USA 2014, 111, 2367–2372. [Google Scholar] [CrossRef] [Green Version]
- Zhang, L.; Zhang, J.; Nie, Q. DIRECT-NET: An efficient method to discover cis-regulatory elements and construct regulatory networks from single-cell multiomics data. Sci. Adv. 2022, 8, eabl7393. [Google Scholar] [CrossRef]
- Mitsuda, N.; Ohme-Takagi, M. Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol. 2009, 50, 1232–1248. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mishra, P.; Tripathi, A.; Kashyap, S.P.; Aamir, M.; Tiwari, K.N.; Singh, V.; Tiwari, S.K. In silico mining of WRKY TFs through Solanum melongena L. and Solanum incanum L. transcriptomes and identification of SiWRKY53 as a source of resistance to bacterial wilt. Plant Gene 2021, 26, 100278. [Google Scholar] [CrossRef]
- de Souza, M.M.; Zerlotini, A.; Geistlinger, L.; Tizioto, P.C.; Taylor, J.F.; Rocha, M.I.; Diniz, W.J.; Coutinho, L.L.; Regitano, L.C. A comprehensive manually-curated compendium of bovine transcription factors. Sci. Rep. 2018, 8, 13747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, M.; Ma, Z.; Sun, W.; Huang, L.; Wu, Q.; Tang, Z.; Bu, T.; Li, C.; Chen, H. Genome-wide analysis of the NAC transcription factor family in Tartary buckwheat (Fagopyrum tataricum). BMC Genom. 2019, 20, 113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peng, X.; Wang, Y.; He, R.; Zhao, M.; Shen, S. Global transcriptomics identification and analysis of transcriptional factors in different tissues of the paper mulberry. BMC Plant Biol. 2014, 14, 194. [Google Scholar] [CrossRef] [Green Version]
- Joshi, R.; Wani, S.H.; Singh, B.; Bohra, A.; Dar, Z.A.; Lone, A.A.; Pareek, A.; Singla-Pareek, S.L. Transcription factors and plants response to drought stress: Current understanding and future directions. Front. Plant Sci. 2016, 7, 1029. [Google Scholar] [CrossRef] [Green Version]
- Srivastava, R.; Kumar, S.; Kobayashi, Y.; Kusunoki, K.; Tripathi, P.; Kobayashi, Y.; Koyama, H.; Sahoo, L. Comparative genome-wide analysis of WRKY transcription factors in two Asian legume crops: Adzuki bean and Mung bean. Sci. Rep. 2018, 8, 16971. [Google Scholar] [CrossRef] [Green Version]
- Ramamoorthy, R.; Jiang, S.-Y.; Kumar, N.; Venkatesh, P.N.; Ramachandran, S. A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol. 2008, 49, 865–879. [Google Scholar] [CrossRef]
- Rushton, P.J.; Somssich, I.E.; Ringler, P.; Shen, Q.J. WRKY transcription factors. Trends Plant Sci. 2010, 15, 247–258. [Google Scholar] [CrossRef]
- Silva Monteiro de Almeida, D.; Oliveira Jordão do Amaral, D.; Del-Bem, L.-E.; Bronze dos Santos, E.; Santana Silva, R.J.; Peres Gramacho, K.; Vincentz, M.; Micheli, F. Genome-wide identification and characterization of cacao WRKY transcription factors and analysis of their expression in response to witches’ broom disease. PLoS ONE 2017, 12, e0187346. [Google Scholar] [CrossRef]
- Zhu, X.; Liu, S.; Meng, C.; Qin, L.; Kong, L.; Xia, G. WRKY transcription factors in wheat and their induction by biotic and abiotic stress. Plant Mol. Biol. Rep. 2013, 31, 1053–1067. [Google Scholar] [CrossRef]
- Puranik, S.; Sahu, P.P.; Mandal, S.N.; Parida, S.K.; Prasad, M. Comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in foxtail millet (Setaria italica L.). PLoS ONE 2013, 8, e64594. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guerin, C.; Roche, J.; Allard, V.; Ravel, C.; Mouzeyar, S.; Bouzidi, M.F. Genome-wide analysis, expansion and expression of the NAC family under drought and heat stresses in bread wheat (T. aestivum L.). PLoS ONE 2019, 14, e0213390. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trishla, V.S.; Kirti, P.B. Structure-function relationship of Gossypium hirsutum NAC transcription factor, GhNAC4 with regard to ABA and abiotic stress responses. Plant Sci. 2021, 302, 110718. [Google Scholar] [CrossRef]
- Park, J.; Kim, Y.-S.; Kim, S.-G.; Jung, J.-H.; Woo, J.-C.; Park, C.-M. Integration of auxin and salt signals by the NAC transcription factor NTM2 during seed germination in Arabidopsis. Plant Physiol. 2011, 156, 537–549. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, R.; Qi, G.; Kong, Y.; Kong, D.; Gao, Q.; Zhou, G. Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol. 2010, 10, 145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamaguchi, M.; Kubo, M.; Fukuda, H.; Demura, T. Vascular-related NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J. 2008, 55, 652–664. [Google Scholar] [CrossRef]
- Puranik, S.; Sahu, P.P.; Srivastava, P.S.; Prasad, M. NAC proteins: Regulation and role in stress tolerance. Trends Plant Sci. 2012, 17, 369–381. [Google Scholar] [CrossRef] [PubMed]
- Jackson, S.A. Rice: The first crop genome. Rice 2016, 9, 14. [Google Scholar] [CrossRef] [Green Version]
- Lata, C.; Yadav, A.; Prasad, M. Role of Plant Transcription Factors in Abiotic Stress Tolerance. In Abiotic Stress Response in Plants; IntechOpen: London, UK, 2011; Volume 10, pp. 269–296. [Google Scholar]
- Seo, E.; Choi, D. Functional studies of transcription factors involved in plant defenses in the genomics era. Brief. Funct. Genom. 2015, 14, 260–267. [Google Scholar] [CrossRef]
- Li, Y.; Liao, S.; Mei, P.; Pan, Y.; Zhang, Y.; Zheng, X.; Xie, Y.; Miao, Y. OsWRKY93 dually functions between leaf senescence and in response to biotic stress in rice. Fronti. Plant Sci. 2021, 12, 643011. [Google Scholar] [CrossRef] [PubMed]
- Peng, Y.; Bartley, L.E.; Chen, X.; Dardick, C.; Chern, M.; Ruan, R.; Canlas, P.E.; Ronald, P.C. OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol. Plant 2008, 1, 446–458. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, X.; Wang, H.; Liu, J.; Han, S.; Lin, M.; Guo, Z.; Chen, X. OsWRKY62 and OsWRKY76 Interact with Importin α1s for Negative Regulation of Defensive Responses in Rice Nucleus. Rice 2022, 15, 12. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Li, X.; Yan, S.; Yu, T.; Yang, J.; Dong, J.; Zhang, S.; Zhao, J.; Yang, T.; Mao, X. OsWRKY67 positively regulates blast and bacteria blight resistance by direct activation of PR genes in rice. BMC Plant Biol. 2018, 18, 257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nuruzzaman, M.; Sharoni, A.M.; Kikuchi, S. Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front. Microbiol. 2013, 4, 248. [Google Scholar] [CrossRef] [Green Version]
- Nuruzzaman, M.; Sharoni, A.M.; Satoh, K.; Karim, M.R.; Harikrishna, J.A.; Shimizu, T.; Sasaya, T.; Omura, T.; Haque, M.A.; Hasan, S.M. NAC transcription factor family genes are differentially expressed in rice during infections with Rice dwarf virus, Rice black-streaked dwarf virus, Rice grassy stunt virus, Rice ragged stunt virus, and Rice transitory yellowing virus. Front. Plant Sci. 2015, 6, 676. [Google Scholar] [CrossRef] [Green Version]
- Jimmy, J.L.; Babu, S. Variations in the structure and evolution of rice WRKY genes in indica and japonica genotypes and their co-expression network in mediating disease resistance. Evol. Bioinform. 2019, 15, 1176934319857720. [Google Scholar] [CrossRef] [Green Version]
- Berri, S.; Abbruscato, P.; Faivre-Rampant, O.; Brasileiro, A.; Fumasoni, I.; Satoh, K.; Kikuchi, S.; Mizzi, L.; Morandini, P.; Pè, M.E. Characterization of WRKYco-regulatory networks in rice and Arabidopsis. BMC Plant Biol. 2009, 9, 120. [Google Scholar] [CrossRef] [Green Version]
- Cannon, S.B.; Mitra, A.; Baumgarten, A.; Young, N.D.; May, G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004, 4, 10. [Google Scholar] [CrossRef] [Green Version]
- Gribskov, M. Identification of sequence patterns, motifs and domains. Encycl. Bioinform. Comput. Biol. 2018, 1, 332–340. [Google Scholar]
- Singh, B.; Mishra, S.; Bisht, D.S.; Joshi, R. Growing rice with less water: Improving productivity by decreasing water demand. In Rice Improvement; Springer: Cham, Switzerland, 2021; pp. 147–170. [Google Scholar]
- Xie, J.-N.; Guo, J.-J.; Jin, D.-C.; Wang, X.-J. Genetic diversity of sogatella furcifera (Hemiptera: Delphacidae) in China detected by inter-simple sequence repeats. J. Insect Sci. 2014, 14, 233. [Google Scholar] [CrossRef]
- Li, F.; Hua, H.; Han, Y.; Hou, M. Plant-mediated horizontal transmission of Asaia between white-backed planthoppers, Sogatella furcifera. Front. Microbiol. 2020, 11, 593485. [Google Scholar] [CrossRef] [PubMed]
- Li, F.; Hua, H.; Ali, A.; Hou, M. Characterization of a bacterial symbiont Asaia sp. in the white-backed planthopper, Sogatella furcifera, and its effects on host fitness. Front. Microbiol. 2019, 10, 2179. [Google Scholar] [CrossRef]
- Tan, G.; Weng, Q.; Ren, X.; Huang, Z.; Zhu, L.; He, G. Two whitebacked planthopper resistance genes in rice share the same loci with those for brown planthopper resistance. Heredity 2004, 92, 212–217. [Google Scholar] [CrossRef] [PubMed]
- Roux, F.; Voisin, D.; Badet, T.; Balagué, C.; Barlet, X.; Huard-Chauveau, C.; Roby, D.; Raffaele, S. Resistance to phytopathogens e tutti quanti: Placing plant quantitative disease resistance on the map. Mol. Plant Pathol. 2014, 15, 427. [Google Scholar] [CrossRef] [PubMed]
- Kissoudis, C.; Sunarti, S.; Van De Wiel, C.; Visser, R.G.; van der Linden, C.G.; Bai, Y. Responses to combined abiotic and biotic stress in tomato are governed by stress intensity and resistance mechanism. J. Exp. Bot. 2016, 67, 5119–5132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Phukan, U.J.; Jeena, G.S.; Shukla, R.K. WRKY transcription factors: Molecular regulation and stress responses in plants. Front. Plant Sci. 2016, 7, 760. [Google Scholar] [CrossRef] [Green Version]
- Li, M.R.; Ding, N.; Lu, T.; Zhao, J.; Wang, Z.H.; Jiang, P.; Liu, S.T.; Wang, X.F.; Liu, B.; Li, L.F. Evolutionary Contribution of Duplicated Genes to Genome Evolution in the Ginseng Species Complex. Genome Biol. Evol. 2021, 13, evab051. [Google Scholar] [CrossRef] [PubMed]
- Huang, S.; Hu, L.; Zhang, S.; Zhang, M.; Jiang, W.; Wu, T.; Du, X. Rice OsWRKY50 Mediates ABA-Dependent Seed Germination and Seedling Growth, and ABA-Independent Salt Stress Tolerance. Int. J. Mol. Sci. 2021, 22, 8625. [Google Scholar] [CrossRef]
- Peng, X.; Wang, H.; Jang, J.-C.; Xiao, T.; He, H.; Jiang, D.; Tang, X. OsWRKY80-OsWRKY4 module as a positive regulatory circuit in rice resistance against Rhizoctonia solani. Rice 2016, 9, 63. [Google Scholar] [CrossRef] [Green Version]
- Jeyasri, R.; Muthuramalingam, P.; Satish, L.; Adarshan, S.; Lakshmi, M.A.; Pandian, S.K.; Chen, J.-T.; Ahmar, S.; Wang, X.; Mora-Poblete, F. The role of OsWRKY genes in rice when faced with single and multiple abiotic stresses. Agronomy 2021, 11, 1301. [Google Scholar] [CrossRef]
- Wu, X.; Shiroto, Y.; Kishitani, S.; Ito, Y.; Toriyama, K. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep. 2009, 28, 21–30. [Google Scholar] [CrossRef] [PubMed]
- Qiu, Y.; Yu, D. Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ. Exp. Bot. 2009, 65, 35–47. [Google Scholar] [CrossRef]
- Jin, J.; Tian, F.; Yang, D.-C.; Meng, Y.-Q.; Kong, L.; Luo, J.; Gao, G. PlantTFDB 4.0: Toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 2017, 45, gkw982. [Google Scholar] [CrossRef] [Green Version]
- Goodstein, D.M.; Shu, S.; Howson, R.; Neupane, R.; Hayes, R.D.; Fazo, J.; Mitros, T.; Dirks, W.; Hellsten, U.; Putnam, N. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res. 2012, 40, D1178–D1186. [Google Scholar] [CrossRef]
- Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef]
- Rambaut, A. FigTree version 1.4.0. Available online: http://tree.bio.ed.ac.uk/software/figtree (accessed on October 2016).
- Rambaut, A.; Drummond, A. Molecular Evolution, Phylogenetics and Epidemiology. FigTree v1. 2007. Available online: http://tree.bio.ed.ac.uk/ (accessed on October 2016).
- Wei, F.; Coe, E.; Nelson, W.; Bharti, A.K.; Engler, F.; Butler, E.; Kim, H.; Goicoechea, J.L.; Chen, M.; Lee, S. Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet. 2007, 3, e123. [Google Scholar] [CrossRef] [Green Version]
- Lee, T.-H.; Tang, H.; Wang, X.; Paterson, A.H. PGDD: A database of gene and genome duplication in plants. Nucleic Acids Res. 2012, 41, D1152–D1158. [Google Scholar] [CrossRef]
- Du, Z.; Zhou, X.; Ling, Y.; Zhang, Z.; Su, Z. agriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010, 38, W64–W70. [Google Scholar] [CrossRef] [Green Version]
- Alexa, A.; Rahnenführer, J.; Lengauer, T. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 2006, 22, 1600–1607. [Google Scholar] [CrossRef] [Green Version]
- Liao, J.-L.; Zhou, H.-W.; Peng, Q.; Zhong, P.-A.; Zhang, H.-Y.; He, C.; Huang, Y.-J. Transcriptome changes in rice (Oryza sativa L.) in response to high night temperature stress at the early milky stage. BMC Genom. 2015, 16, 18. [Google Scholar] [CrossRef] [PubMed]
- Sirén, J.; Välimäki, N.; Mäkinen, V. HISAT2-fast and sensitive alignment against general human population. IEEE/ACM Trans. Comput. Biol. Bioinform. 2014, 11, 375–388. [Google Scholar] [CrossRef] [PubMed]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef] [PubMed]
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Khan, I.; Jan, R.; Asaf, S.; Khan, A.L.; Bilal, S.; Kim, K.-M.; Al-Harrasi, A. Genome and Transcriptome-Wide Analysis of OsWRKY and OsNAC Gene Families in Oryza sativa and Their Response to White-Backed Planthopper Infestation. Int. J. Mol. Sci. 2022, 23, 15396. https://doi.org/10.3390/ijms232315396
Khan I, Jan R, Asaf S, Khan AL, Bilal S, Kim K-M, Al-Harrasi A. Genome and Transcriptome-Wide Analysis of OsWRKY and OsNAC Gene Families in Oryza sativa and Their Response to White-Backed Planthopper Infestation. International Journal of Molecular Sciences. 2022; 23(23):15396. https://doi.org/10.3390/ijms232315396
Chicago/Turabian StyleKhan, Ibrahim, Rahmatullah Jan, Sajjad Asaf, Abdul Latif Khan, Saqib Bilal, Kyung-Min Kim, and Ahmed Al-Harrasi. 2022. "Genome and Transcriptome-Wide Analysis of OsWRKY and OsNAC Gene Families in Oryza sativa and Their Response to White-Backed Planthopper Infestation" International Journal of Molecular Sciences 23, no. 23: 15396. https://doi.org/10.3390/ijms232315396