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Research Articles

Vol. 10 No. 3 (2023)

Transcriptome-wide identification and expression analysis of the NAC gene family in lowland bamboo [Oxytenanthera abyssinica (A.Rich) Munro] under abiotic stresses

DOI
https://doi.org/10.14719/pst.2280
Submitted
7 December 2022
Published
12-05-2023 — Updated on 01-07-2023
Versions

Abstract

NAC (NAM, no apical meristem, ATAF and CUC) is one of the largest gene families of the plant-specific transcription factors (TF). NAC TFs have immense involvement in plant growth and developmental processes and have particular importance in enhancing plant resistance to multiple abiotic stresses. NAC members have unique structural makeup and a range of biological activities. Despite their enormous roles in plants, comprehensive study on identification, characterization and expression profiling of NACs under abiotic stress is lacking in Lowland bamboo [Oxytenanthera abyssinica (A.Rich) Munro]. Thus, this study aimed to identify NAC members, characterize their protein properties, construct their phylogenetic relationships and more importantly, establish their expression profiling under abiotic stress. From this abiotic stress-induced transcriptome, 220 lowland bamboo TFs with intact and complete NAC DNA binding domains (PF01849) were identified. Following their identification, analysis of functional annotation, protein characterization, phylogenetic relationships and expression profiling were conducted. The analysis presented up-regulation of 142 unigenes in response to abiotic stress, the association of 26 unigenes directly to stress response and the involvement of 92 unigenes in genetic information processing and 29 in environmental information processing according to KEGG analysis. These results suggest the most likely involvement of NACs in lowland bamboo stress response and adaptation. As a species best survived in a moisture-stressed environment, this study has provided valuable information that could shed light on further functional analysis research efforts aiming to exploit NACs in developing stress-resilient bamboo and related plants.

References

  1. Basak M, Dutta S, Biswas S, Chakraborty S, Sarka A, Rahaman T, Dey S, Biswas P, Das M. Genomic insights into growth and development of bamboos: what have we learned and what more to discover? Trees. 2021. https://doi.org/10.1007/s00468-021-02197-6.
  2. Qiao G, Yang H, Han X, Liu M, Jiang J, Jiang Y. Enhanced cold stress tolerance of transgenic Dendrocalamus latiflorus Munro (Ma bamboo) plants expressing a bacterial CodA gene. In Vit Cellu and Develop Biolo – Plant. 2014. https://doi.org/10.1007/s11627-013-9591-z.
  3. Tao G, Fu Y, Zhou M. “Advances in studies on molecular mechanisms of the rapid growth of bamboo species,” J of Agric Biotechnol. 2018;26: 871– 887.
  4. Guo ZH, Ma PF, Yang GQ, Hu JY, Liu YL, Xia EH, Zhong MC, Zhao L, Sun GL, XuY X, Zhao YJ, Zhang YC, Zhang YX, Zhang XM, Zhou MY, Guo Y, Guo C, Liu JX, Ye XY, Chen YM, Yang Y, Han B, Lin, CS, Lu Y, Li DZ. Genome sequences provide insights into the reticulate origin and unique traits of woody bamboo. Mol Plant. 2019a; 12:1353–1365. https://doi.org/10.1016/j.molp.2019.05.009
  5. Inada T, Hall JB. Oxytenanthera abyssinica (A. Rich). Munro. Record from Protabase. 2008.
  6. 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 Biolo.2010; 10:145. https://doi.org/10.1186/1471-2229-10-145
  7. Ahuja I, de Vos RC, Bones AM, Hall RD. Plant molecular stress responses face climate change. Trends Plant Sci. 2010;15: 664–674. https://doi.org/10.1016/j.tplants.2010.08.002
  8. Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R. TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot. 2012;63: 2933–2946. https://doi.org/10.1093/jxb/err462
  9. Tran L-SP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. The Plant Cell. 2004; 16:2481-2498. https://doi.org/10.1105/tpc.104.022699
  10. Agarwal PK, Agarwal P, Reddy MK, Sopory S K. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep. 2006; 25: 1263–1274. https://doi.org/10.1007/s00299-006-0204-8
  11. Olsen AN, Ernst HA, Leggio LL, Skriver K. NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci. 2005;10: 79–87. https://doi.org/10.1016/j.tplants.2004.12.010
  12. Puranik S, Sahu PP, Srivastava PS, Prasad M. NAC proteins: regulation and role in stress tolerance. Trends Plant Sci. 2012;17: 369–381. https://doi.org/10.1016/j.tplants.2012.02.004
  13. Huang J, Ren R, Rong Y, Tang B, Deng J, Chen Q, Shi T. Identification, expression, and functional study of seven NAC transcription factor genes involved in stress response in Tartary Buckwheat (Fagopyrum tataricum (L.) Gaertn.). Agronomy. 2022; 12: 849. https://doi.org/10.3390/
  14. Chen X, Wang Y, Lv B, Li J, Luo L, Lu S, Zhang X, Ma H, Ming F. The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway. Plant Cell Physiol. 2014; 55: 604–619. https://doi.org/10.1093/pcp/pct204.
  15. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell. 1997; 9:841–857. PMID: 9212461. https://doi.org/10.1105/tpc.9.6.841
  16. 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; 10:239–24. https://doi.org/10.1093/dnares/10.6.239
  17. Li B, Hu SL, Cao Y, Gang X. Bioinformatics analysis of NAC gene family in moso bamboo. Genomics and Appli Biolo. 2015; 34(8):1769–1777. https://doi.org/10.13417/j.gab.034.001769.
  18. Tran LSP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress1 promoter. Plant Cell. 2004; 16: 2481–2498. https://doi.org/10.1105/tpc.104.022699
  19. Yang R, Deng C, Ouyang B, Ye Z. Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato. Mol Biol Repo. 2011; 38:857-863. https://doi.org/10.1007/s11033-010-0177-0
  20. Puranik S, Sahu PP, Mandal SN, B VS, Parida SK. The comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in foxtail millet (Setaria italica L.). PLoS ONE 8. e6459. 2013. https://doi.org/10.1371/journal.pone.0064594
  21. Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS. Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.) DNA Res.2013;20:403- 423. https://doi.org/10.1093/dnares/dst019
  22. Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S. Genome-wide analysis of NAC transcription factor family in rice. Gene.2010; 465:30-44. https://doi.org/10.1016/j.gene.2010.06.008
  23. Liu T, Song X, Duan W, Huang Z, Liu G, Li Y, Hou X. Genome-wide analysis and expression patterns of NAC transcription factor family under different developmental stages and abiotic stresses in Chinese cabbage. Plant Mol Biol Repo .2014; 32:1041-1056. https://doi.org/10.1007/s11105-014-0712-6
  24. Wei S, Gao L, Zhang Y, Zhang F, Yang X, Huang D. Genome-wide investigation of the NAC transcription factor family in melon (Cucumis melo L.) and their expression analysis under salt stress. Plant Cell Rep. 2016; 35:1827-1839. https://doi.org/10.1007/s00299-016-1997-8
  25. Li W, Zeng Y, Fangliu Yin F, Wei R, Xiaofei M X. Genome?wide identification and comprehensive analysis of the NAC transcription factor family in sunflower during salt and drought stress. Sci Rep. 2021; 11:19865. https://doi.org/10.1038/s41598-021-98107-4.
  26. Andrews S. FastQC: A quality control tool for high throughput sequence data.2010.
  27. Joshi NA, Fass JN. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ fles 201h1t.tp://www.citeulike.org /user/mvermaat/article/13260426.2011.
  28. Grabherr MG, Haas BJ, Yassour M. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7): 644-52. https://doi.org/10.1038/nbt.1883
  29. Fu L, Niu B, Zhu Z, Wu S, Li W.CD-HIT: Accelerated for clustering the next-generation sequencing data. Bioinfo.2012; 28:3150-2. https://doi.org/10.1093/bioinformatics/bts565
  30. Adem M, Zhao K, Beyene D, Feyissa T, Jiang T. De novo assembly and transcriptome profiling of Ethiopian lowland bamboo [Oxytenanthera abyssinica (A.Rich) Munro] under drought and salt stresses. Open Biotechnol J. 2019;13: 6–17. https://doi.org/10.2174/1874070701913010006.
  31. Zheng Y, Jia C, Sun H. iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein Kinases. Mol Plant.2016; 9:1667-1670. https://doi.org/10.1016/j.molp.2016.09.014
  32. Yu C, Cheng C, Su W, Chang Kc, Huang S, Hwang J, Lu Ch. CELLO2GO: A Web Server for Protein Sub-Cellular Localization Prediction with Functional Gene Ontology Annotation. Plos ONE. 2014;9(6): E99368. https://doi.org/10.1371/journal.pone.0099368
  33. Kanehisa M, Sato Y, Morishima K. Blast KOALA and Ghost KOALA: KEGG tools for functional characterization of genome and metagenome sequences. Databases.2015. https://doi.org/10.1016/j.jmb.2015.11.006
  34. Tamura K, Stecher G, and Kumar S. MEGA 11: Molecular Evolutionary Genetics Analysis. Version 11. Mol Bio and Evo.2021; 38(7):3022–3027.https://doi.org/10.1093/molbev/msab120.
  35. Fan C, Ma J, Guo Q, Li X, Wang H, Lu M. Selection of Reference Genes for Quantitative Real-Time PCR in Bamboo (Phyllostachys edulis). PLoS ONE.2013; 8(2): e56573. https://doi.org/10.1371/journal.pone.0056573
  36. Suchithra B, Devaraj VR, Babu RN. Genome-Wide Analysis of NAC Transcription Factors and their Expression Pattern During High Temperature and Drought Stress in Groundnut. African Crop Sci J. 2018; 26:327 – 348. https://doi.org/10.4314/acsj.v26i3.1
  37. Muller M, Seifert S, LuÈbbe T, Leuschner C, Finkeldey R. De novo transcriptome assembly and analysis of differential gene expression in response to drought in European beech. PLoS ONE. 2017. 12, e0184167. https://doi.org/ 10.1371/journal.pone.0184167.
  38. Marques DN, dos Reis SP, de Souza CRB. Plant NAC transcription factors responsive to abiotic stresses. Plant Gene 2017; 11:170–179. https://doi.org/10.1016/j.plgene.2017.06.003
  39. Hou D, Zhongyu Z, Qiutao H, Ling L, Naresh V, Juan Z, Wei Z, Aimin W, Xinchun L PeSNAC-1 a NAC transcription factor from moso bamboo (Phyllostachys edulis) confers tolerance to salinity and drought stress in transgenic rice. Tree Physiol. 2020; 40(12):1792-1806. https://doi.org/10.1093/treephys/tpaa099.
  40. Xie L, CaiM, Li X, Zheng H, Xie Y, Cheng Z, Bai Y, Li J, Mu S, Gao J. Overexpression of PheNAC3 from moso bamboo promotes leaf senescence and enhances abiotic stress tolerance in Arabidopsis. PeerJ 8:e8716. 2020. https://doi.org/10.7717/peerj.8716.
  41. Tariq R, Hussain A, Tariq A, Hayder M,Khalid B, Khan I, H, Pär K. Ingvarsson Genome-wide analyses of the mung bean NAC gene family reveals orthologs, co-expression networking and expression profiling under abiotic and biotic stresses. BMC Plant Biol. 2022; 22:343. https://doi.org/10.1186/s12870-022-03716-4.
  42. Li P, Peng Z, Xu P, Tang G, Ma C,Zhu J, Shan L and Wan S. Genome-wide identification of NAC transcription factors and their functional prediction of abiotic stress response in Peanut. Front. Genet. 2021. 12:630292. https:// doi.org/10.3389/fgene.2021.630292.
  43. Zhao S, Jiang T, Zhang Y, Zhang K, Feng K, Wu P, Li L. Identification of the NAC Transcription factors and their function in ABA and salinity response in Nelumbo nucifera. Int J Mol Sci. 2022; 23(20):12394. https://doi.org/10.3390/ijms232012394.
  44. Nie G, Yang Z, He J, Liu A, Chen J, Wang S, Wang X, Feng G, Li D, Peng Y, Huang L, Zhang X. Genome-wide investigation of the NAC transcription factor family in Miscanthus sinensis and expression analysis under various abiotic stresses. Front. Plant Sci. 2021; 12:766550. https://doi.org/10.3389/fpls.2021.766550.
  45. Wang Z, Ni L, Liu D, Fu Z, Hua J, Lu Z, Liu L, Yin Y, Li H, Gu C.Genome-wide identification and characterization of NAC family in Hibiscus hamabo Sieb. et Zucc. under various abiotic Stresses. Int. J. Mol. Sci. 2022. 23; 3055. https://doi.org/10.3390/ijms23063055.
  46. Yan H, Ma G, Teixeira da Silva JA, Qiu L, Xu J, Zhou H, Wei M, Xiong J, Li M, Zhou S, Wu J, Tang X. Genome-wide identification and analysis of NAC transcription factor family in two diploid wild relatives of cultivated sweet Potato uncovers potential NAC Genes related to drought tolerance. Front. Genet.2021. 12:744220. https:// doi.org/10.3389/fgene.2021.744220.
  47. Xu Y, Li P, Ma F, Huang D, Xing W, Wu B, Sun P, Xu B, Song S. Characterization of the NAC transcription Factor in Passion Fruit (Passiflora edulis) and functional identification of PeNAC-19 in Cold Stress. Plants 2023, 12;1393. https:// doi.org/10.3390/plants12061393.
  48. Wang GL, An YH, Zhou CL, Hu ZZ, Ren XQ, Xiong AS. Transcriptome-wide identification of NAC (no apical meristem/Arabidopsis transcription activation factor/cup-shaped cotyledon) transcription factors potentially involved in salt stress response in garlic. PeerJ. 2022. https://doi.org/10:e14602 DOI 10.7717/peerj.14602.
  49. Huang X, Qiu X, Wang Y, Abubakar AS, Chen P, Chen J, Chen K, Yu C, Wang X, Gao G, Zhu A. Genome-wide investigation of the NAC transcription factor family in Apocynum venetum revealed their synergistic roles in abiotic stress response and Trehalose Metabolism. Int J Mol Sci. 2023. 26;24(5):4578. https://doi.org/10.3390/ijms24054578.
  50. Chen Y, Li X, Xie X, Liu L, Fu J, Wang Q, Maize transcription factor ZmNAC2 enhances osmotic stress tolerance in transgenic Arabidopsis, J of Plant Physio.2023. 282: 153948, ISSN 0176-1617. https://doi.org/10.1016/j.jplph.2023.153948.

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