Identification and evolutionary characterization of salt-responsive transcription factors in the succulent halophyte Suaeda fruticosa


Autoři: Joann Diray-Arce aff001;  Alisa Knowles aff001;  Anton Suvorov aff002;  Jacob O’Brien aff001;  Collin Hansen aff001;  Seth M. Bybee aff002;  Bilquees Gul aff003;  M. Ajmal Khan aff003;  Brent L. Nielsen aff001
Působiště autorů: Department of Microbiology and Molecular Biology, Brigham Young University, Provo, Utah, United States of America aff001;  Department of Biology, Brigham Young University, Provo, Utah, United States of America aff002;  Institute of Sustainable Halophyte Utilization, University of Karachi, Karachi, Pakistan aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222940

Souhrn

Transcription factors are key regulatory elements that affect gene expression in response to specific signals, including environmental stresses such as salinity. Halophytes are specialized plants that have the ability to complete their life cycle in saline environments. In this study we have identified and characterized the evolutionary relationships of putative transcription factors (TF) in an obligate succulent halophyte, Suaeda fruticosa, that are involved in conferring salt tolerance. Using RNA-seq data we have analyzed the expression patterns of certain TF families, predicted protein-protein interactions, and analyzed evolutionary trajectories to elucidate their possible roles in salt tolerance. We have detected the top differentially expressed (DE) transcription factor families (MYB, CAMTA, MADS-box and bZIP) that show the most pronounced response to salinity. The majority of DE genes in the four aforementioned TF families cluster together on TF phylogenetic trees, which suggests common evolutionary origins and trajectories. This research represents the first comprehensive TF study of a leaf succulent halophyte including their evolutionary relationships with TFs in other halophyte and salt-senstive plants. These findings provide a foundation for understanding the function of salt-responsive transcription factors in salt tolerance and associated gene regulation in plants.

Klíčová slova:

DNA transcription – Gene expression – Multiple alignment calculation – Phylogenetic analysis – Plant resistance to abiotic stress – Sequence alignment – Transcription factors – Quinoa


Zdroje

1. Flowers T, Colmer T. Salinity tolerance in halophytes. New Phytol. 2008;179:945–63. doi: 10.1111/j.1469-8137.2008.02531.x 18565144

2. Zhu J. Plant salt tolerance. Trends Plant Sci. 2001;6:66–71. 11173290

3. Glenn EP, Brown JJ, Blumwald E. Salt Tolerance and Crop Potential of Halophytes. Critical Reviews in Plant Sciences. 1999;18:227–55. doi: 10.1080/07352689991309207

4. Jiang Y, Zeng B, Zhao H, Zhang M, Xie S, Lai J. Genome-wide transcription factor gene prediction and their expressional tissue-specificities in maize. J Integr Plant Biol. 2012;54(9):616–30. Epub 2012/08/07. doi: 10.1111/j.1744-7909.2012.01149.x 22862992.

5. Long Y, Scheres B, Blilou I. The logic of communication: roles for mobile transcription factors in plants. J Exp Bot. 2015;66(4):1133–44. Epub 2015/01/31. doi: 10.1093/jxb/eru548 25635110.

6. Golldack D, Luking I, Yang O. Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep. 2011;30(8):1383–91. Epub 2011/04/09. doi: 10.1007/s00299-011-1068-0 21476089.

7. You J, Chan Z. ROS Regulation During Abiotic Stress Responses in Crop Plants. Frontiers in plant science. 2015;6:1092. Epub 2015/12/24. doi: 10.3389/fpls.2015.01092 26697045; PubMed Central PMCID: PMC4672674.

8. Diray-Arce J, Gul B, Khan MA, Nielsen B. 10—Halophyte Transcriptomics: Understanding Mechanisms of Salinity Tolerance. Halophytes for Food Security in Dry Lands. San Diego: Academic Press; 2016. p. 157–75.

9. Ghanekar R, Srinivasasainagendra V, Page G. Cross-Chip Probe Matching Tool: A Web-Based Tool for Linking Microarray Probes within and across Plant Species. Int J Plant Genomics. 2008;7. doi: 10.1155/2008/451327 18949054

10. Hameed A, Hussain T, Gulzar S, Aziz I, Gul B, Khan MA. Salt tolerance of a cash crop halophyte Suaeda fruticosa: biochemical responses to salt and exogenous chemical treatments. Acta Physiologiae Plantarum. 2012;34:2331–40. doi: 10.1007/s11738-012-1035-6

11. Diray-Arce J, Clement M, Gul B, Ajmal Khan M, Nielsen BL. Transcriptome Assembly, Profiling and Differential Gene Expression Analysis of the halophyte Suaeda fruticosa Provides Insights into Salt Tolerance. BMC Genomics. 2015;16(353). doi: 10.1186/s12864-015-1553-x 25943316

12. Jin J, Zhang H, Kong L, Gao G, Luo J. PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Research. 2014;42(D1):D1182–D7. doi: 10.1093/nar/gkt1016 24174544

13. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28(23):3150–2. Epub 2012/10/13. doi: 10.1093/bioinformatics/bts565 23060610; PubMed Central PMCID: PMC3516142.

14. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. doi: 10.1093/bioinformatics/btp616 19910308

15. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39(Web Server issue):W29–37. Epub 2011/05/20. doi: 10.1093/nar/gkr367 21593126; PubMed Central PMCID: PMC3125773.

16. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43(Database issue):D447–52. Epub 2014/10/30. doi: 10.1093/nar/gku1003 25352553; PubMed Central PMCID: PMC4383874.

17. Mirarab S, Nguyen N, Guo S, Wang LS, Kim J, Warnow T. PASTA: Ultra-Large Multiple Sequence Alignment for Nucleotide and Amino-Acid Sequences. J Comput Biol. 2015;22(5):377–86. Epub 2014/12/31. doi: 10.1089/cmb.2014.0156 25549288; PubMed Central PMCID: PMC4424971.

18. Haddad F, Baldwin KM. Reverse transcription of the ribonucleic acid: the first step in RT-PCR assay. Methods Mol Biol. 2010;630:261–70. Epub 2010/03/20. doi: 10.1007/978-1-60761-629-0_17 20301003.

19. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science. 2008;319(5859):64–9. Epub 2007/12/15. doi: 10.1126/science.1150646 18079367.

20. Rahman H, Yang J, Xu YP, Munyampundu JP, Cai XZ. Phylogeny of Plant CAMTAs and Role of AtCAMTAs in Nonhost Resistance to Xanthomonas oryzae pv. oryzae. Front Plant Sci. 2016;7:177. Epub 2016/03/15. doi: 10.3389/fpls.2016.00177 26973658; PubMed Central PMCID: PMC4770041.

21. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practival and powerful approach to multiple testing. J Royal Statistical Soc Series. 1995;57:289–300.

22. Lai LB, Nadeau JA, Lucas J, Lee EK, Nakagawa T, Zhao L, et al. The Arabidopsis R2R3 MYB proteins FOUR LIPS and MYB88 restrict divisions late in the stomatal cell lineage. Plant Cell. 2005;17(10):2754–67. Epub 2005/09/13. doi: 10.1105/tpc.105.034116 16155180; PubMed Central PMCID: PMC1242270.

23. Xie Z, Li D, Wang L, Sack FD, Grotewold E. Role of the stomatal development regulators FLP/MYB88 in abiotic stress responses. The Plant journal: for cell and molecular biology. 2010;64(5):731–9. Epub 2010/11/26. doi: 10.1111/j.1365-313X.2010.04364.x 21105921.

24. Anwer M, Boikoglu E, Herrero E, Hallstein M, Davis A, Velikkakam JG, et al. Natural variation reveals that intracellular distribution of ELF3 protein is associated with function in the circadian clock. Elife. 2014;3. doi: 10.7554/eLife.02206.001

25. Boxall SF, Foster JM, Bohnert HJ, Cushman JC, Nimmo HG, Hartwell J. Conservation and divergence of circadian clock operation in a stress-inducible Crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiol. 2005;137(3):969–82. Epub 2005/03/01. doi: 10.1104/pp.104.054577 15734916; PubMed Central PMCID: PMC1065398.

26. Finkelstein RR, Gibson SI. ABA and sugar interactions regulating development: cross-talk or voices in a crowd? Curr Opin Plant Biol. 2002;5(1):26–32. Epub 2002/01/15. 11788304.

27. Wang W, Tang W, Ma T, Niu D, Jin JB, Wang H, et al. A pair of light signaling factors FHY3 and FAR1 regulates plant immunity by modulating chlorophyll biosynthesis. J Integr Plant Biol. 2016;58(1):91–103. Epub 2015/05/20. doi: 10.1111/jipb.12369 25989254; PubMed Central PMCID: PMC4736690.

28. Babitha KC, Vemanna RS, Nataraja KN, Udayakumar M. Overexpression of EcbHLH57 Transcription Factor from Eleusine coracana L. in Tobacco Confers Tolerance to Salt, Oxidative and Drought Stress. PLoS One. 2015;10(9):e0137098. Epub 2015/09/15. doi: 10.1371/journal.pone.0137098 26366726; PubMed Central PMCID: PMC4569372.

29. Toda Y, Yoshida M, Hattori T, Takeda S. RICE SALT SENSITIVE3 binding to bHLH and JAZ factors mediates control of cell wall plasticity in the root apex. Plant Signal Behav. 2013;8(11):e26256. Epub 2013/08/31. doi: 10.4161/psb.26256 23989667; PubMed Central PMCID: PMC4091359.

30. Zou J, Liu A, Chen X, Zhou X, Gao G, Wang W, et al. Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol. 2009;166(8):851–61. Epub 2009/01/13. doi: 10.1016/j.jplph.2008.11.007 19135278.

31. Garg R, Verma M, Agrawal S, Shankar R, Majee M, Jain M. Deep transcriptome sequencing of wild halophyte rice, Porteresia coarctata, provides novel insights into the salinity and submergence tolerance factors. DNA Res. 2014;21(1):69–84. Epub 2013/10/10. doi: 10.1093/dnares/dst042 24104396; PubMed Central PMCID: PMC3925395.

32. Sharma R, Mishra M, Gupta B, Parsania C, Singla-Pareek SL, Pareek A. De Novo Assembly and Characterization of Stress Transcriptome in a Salinity-Tolerant Variety CS52 of Brassica juncea. PLoS One. 2015;10(5):e0126783. Epub 2015/05/15. doi: 10.1371/journal.pone.0126783 25970274; PubMed Central PMCID: PMC4429966.

33. Zhou X, Hua D, Chen Z, Zhou Z, Gong Z. Elongator mediates ABA responses, oxidative stress resistance and anthocyanin biosynthesis in Arabidopsis. Plant J. 2009;60(1):79–90. Epub 2009/06/09. doi: 10.1111/j.1365-313X.2009.03931.x 19500300.

34. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell. 2003;15(1):63–78. Epub 2003/01/02. doi: 10.1105/tpc.006130 12509522; PubMed Central PMCID: PMC143451.

35. Feller A, Machemer K, Braun EL, Grotewold E. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant Journal. 2011;66(1):94–116. doi: 10.1111/j.1365-313X.2010.04459.x WOS:000288862500008. 21443626

36. Roy S. Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant Signal Behav. 2016;11(1):e1117723. Epub 2015/12/05. doi: 10.1080/15592324.2015.1117723 26636625; PubMed Central PMCID: PMC4871670.

37. Yang A, Dai X, Zhang WH. A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot. 2012;63(7):2541–56. Epub 2012/02/04. doi: 10.1093/jxb/err431 22301384; PubMed Central PMCID: PMC3346221.

38. Ganesan G, Sankararamasubramanian HM, Harikrishnan M, Ganpudi A, Parida A. A MYB transcription factor from the grey mangrove is induced by stress and confers NaCl tolerance in tobacco. J Exp Bot. 2012;63(12):4549–61. Epub 2012/08/21. doi: 10.1093/jxb/ers135 22904269.

39. Kofuji R, Sumikawa N, Yamasaki M, Kondo K, Ueda K, Ito M, et al. Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Mol Biol Evol. 2003;20(12):1963–77. Epub 2003/09/02. doi: 10.1093/molbev/msg216 12949148.

40. Smaczniak C, Immink RG, Angenent GC, Kaufmann K. Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development. 2012;139(17):3081–98. Epub 2012/08/09. doi: 10.1242/dev.074674 22872082.

41. Zhu Q, Zhang JT, Gao XS, Tong JH, Xiao LT, Li WB, et al. The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene. 2010;457(1–2):1–12. doi: 10.1016/j.gene.2010.02.011 WOS:000278261400001. 20193749

42. Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, et al. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell. 2003;15(7):1538–51. Epub 2003/07/03. doi: 10.1105/tpc.011544 12837945; PubMed Central PMCID: PMC165399.

43. Saha G, Park JI, Jung HJ, Ahmed NU, Kayum MA, Chung MY, et al. Genome-wide identification and characterization of MADS-box family genes related to organ development and stress resistance in Brassica rapa. BMC Genomics. 2015;16:178. Epub 2015/04/17. doi: 10.1186/s12864-015-1349-z 25881193; PubMed Central PMCID: PMC4422603.

44. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, et al. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics. 2007;8:242. Epub 2007/07/21. doi: 10.1186/1471-2164-8-242 17640358; PubMed Central PMCID: PMC1947970.

45. Lee S, Woo YM, Ryu SI, Shin YD, Kim WT, Park KY, et al. Further characterization of a rice AGL12 group MADS-box gene, OsMADS26. Plant Physiol. 2008;147(1):156–68. Epub 2008/03/21. doi: 10.1104/pp.107.114256 18354041; PubMed Central PMCID: PMC2330315.

46. Liang C, Meng Z, Meng Z, Malik W, Yan R, Lwin KM, et al. GhABF2, a bZIP transcription factor, confers drought and salinity tolerance in cotton (Gossypium hirsutum L.). Scientific reports. 2016;6:35040. Epub 2016/10/08. doi: 10.1038/srep35040 27713524; PubMed Central PMCID: PMC5054369.

47. Shen H, Cao K, Wang X. AtbZIP16 and AtbZIP68, two new members of GBFs, can interact with other G group bZIPs in Arabidopsis thaliana. BMB Rep. 2008;41(2):132–8. Epub 2008/03/05. doi: 10.5483/bmbrep.2008.41.2.132 18315949.

48. Ji X, Liu G, Liu Y, Zheng L, Nie X, Wang Y. The bZIP protein from Tamarix hispida, ThbZIP1, is ACGT elements binding factor that enhances abiotic stress signaling in transgenic Arabidopsis. BMC Plant Biol. 2013;13:151. Epub 2013/10/08. doi: 10.1186/1471-2229-13-151 24093718; PubMed Central PMCID: PMC3852707.

49. Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya, Tsai YC, et al. A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta. 2010;231(6):1459–73. Epub 2010/04/02. doi: 10.1007/s00425-010-1147-4 20358223.

50. Shaikhali J, Noren L, de Dios Barajas-Lopez J, Srivastava V, Konig J, Sauer UH, et al. Redox-mediated mechanisms regulate DNA binding activity of the G-group of basic region leucine zipper (bZIP) transcription factors in Arabidopsis. J Biol Chem. 2012;287(33):27510–25. Epub 2012/06/22. doi: 10.1074/jbc.M112.361394 22718771; PubMed Central PMCID: PMC3431687.

51. Correa LGG, Riano-Pachon DM, Schrago CG, dos Santos RV, Mueller-Roeber B, Vincentz M. The Role of bZIP Transcription Factors in Green Plant Evolution: Adaptive Features Emerging from Four Founder Genes. Plos One. 2008;3(8). ARTN e2944 doi: 10.1371/journal.pone.0002944 WOS:000264412600030. 18698409

52. Onai K, Ishiura M. PHYTOCLOCK1 encoding a novel GARP protein essential for the Arabidopsis circadian clock. Genes Cell. 2005;10:963–72.

53. Yang T, Peng H, Whitaker BD, Conway WS. Characterization of a calcium/calmodulin-regulated SR/CAMTA gene family during tomato fruit development and ripening. BMC Plant Biol. 2012;12:19. Epub 2012/02/15. doi: 10.1186/1471-2229-12-19 22330838; PubMed Central PMCID: PMC3292969.

54. Benn G, Wang CQ, Hicks DR, Stein J, Guthrie C, Dehesh K. A key general stress response motif is regulated non-uniformly by CAMTA transcription doi: 10.1111/tpj.12620 factors. The Plant journal: for cell and molecular biology. 2014;80(1):82–92. Epub 2014/07/22. 25039701; PubMed Central PMCID: PMC4172554.

55. Jin H, Dong D, Yang Q, Zhu D. Salt-Responsive Transcriptome Profiling of Suaeda glauca via RNA Sequencing. PLoS One. 2016;11(3):e0150504. Epub 2016/03/02. doi: 10.1371/journal.pone.0150504 26930632; PubMed Central PMCID: PMC4773115.

56. Mishra A, Tanna B. Halophytes: Potential Resources for Salt Stress Tolerance Genes and Promoters. Front Plant Sci. 2017;8:829. Epub 2017/06/03. doi: 10.3389/fpls.2017.00829 28572812; PubMed Central PMCID: PMC5435751.


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden