Genome-wide identification and expression profile analysis of nuclear factor Y family genes in Sorghum bicolor L. (Moench)

English version

Autoři: P. Maheshwari ^aff001; Divya Kummari ^aff002; Sudhakar Reddy Palakolanu ^aff002; U. Nagasai Tejaswi ^aff003; M. Nagaraju ^aff001; G. Rajasheker ^aff001; G. Jawahar ^aff001; N. Jalaja ^aff003; P. Rathnagiri ^aff005; P. B. Kavi Kishor ^aff001
Působiště autorů: Department of Genetics, Osmania University, Hyderabad, India ^aff001; International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Hyderabad, India ^aff002; Department of Biotechnology, Vignan’s Foundation for Science, Technology and Research, Vadlamudi, Guntur, Andhra Pradesh, India ^aff003; Department of Biochemistry, ICMR-National Institute of Nutrition, Hyderabad, India ^aff004; Genomix CARL Pvt. Ltd. Rayalapuram Road, Pulivendula, Kadapa, Andhra Pradesh, India ^aff005; Genomix Molecular Diagnostics Pvt Ltd., Kukatpally, Hyderabad, India ^aff006; Genomix Biotech Inc., Atlanta, GA, United States of America ^aff007
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222203

Souhrn

Members of the plant Heme Activator Protein (HAP) or NUCLEAR FACTOR Y (NF-Y) are trimeric transcription factor complexes composed of the NF-YA, NF-YB and NF-YC subfamilies. They bind to the CCAAT box in the promoter regions of the target genes and regulate gene expressions. Plant NF-Ys were reported to be involved in adaptation to several abiotic stresses as well as in development. In silico analysis of Sorghum bicolor genome resulted in the identification of a total of 42 NF-Y genes, among which 8 code for the SbNF-YA, 19 for SbNF-YB and 15 for the SbNF-YC subunits. Analysis was also performed to characterize gene structures, chromosomal distribution, duplication status, protein subcellular localizations, conserved motifs, ancestral protein sequences, miRNAs and phylogenetic tree construction. Phylogenetic relationships and ortholog predictions displayed that sorghum has additional NF-YB genes with unknown functions in comparison with Arabidopsis. Analysis of promoters revealed that they harbour many stress-related cis-elements like ABRE and HSE, but surprisingly, DRE and MYB elements were not detected in any of the subfamilies. SbNF-YA1, 2, and 6 were found upregulated under 200 mM salt and 200 mM mannitol stresses. While NF-YA7 appeared associated with high temperature (40°C) stress, NF-YA8 was triggered by both cold (4°C) and high temperature stresses. Among NF-YB genes, 7, 12, 15, and 16 were induced under multiple stress conditions such as salt, mannitol, ABA, cold and high temperatures. Likewise, NF-YC 6, 11, 12, 14, and 15 were enhanced significantly in a tissue specific manner under multiple abiotic stress conditions. Majority of the mannitol (drought)-inducible genes were also induced by salt, high temperature stresses and ABA. Few of the high temperature stress-induced genes are also induced by cold stress (NF-YA2, 4, 6, 8, NF-YB2, 7, 10, 11, 12, 14, 16, 17, NF-YC4, 6, 12, and 13) thus suggesting a cross talk among them. This work paves the way for investigating the roles of diverse sorghum NF-Y proteins during abiotic stress responses and provides an insight into the evolution of diverse NF-Y members.

Klíčová slova:

Biology and life sciences – Genetics – Gene expression – Genomics – Biochemistry – Nucleic acids – Plant science – Organisms – Eukaryota – Plants – Grasses – Computational biology – Physical sciences – Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Plant and algal models – Proteins – DNA-binding proteins – Plant pathology – Database and informatics methods – Bioinformatics – Sequence analysis – Gene regulation – RNA – Non-coding RNA – Sequence motif analysis – Transcription factors – Regulatory proteins – Physics – Classical mechanics – Ecology and environmental sciences – Plant ecology – Plant-environment interactions – Ecology – Plant physiology – Plant defenses – Plant resistance to abiotic stress – Natural antisense transcripts – MicroRNAs – Genome complexity – Brassica – Introns – Mechanical stress – Arabidopsis thaliana – Sorghum – Thermal stresses

Zdroje

1. Kim IS, Sinha S, De Crombrugghe B, Maity SN. Determination of functional domains in the C subunit of the CCAAT-binding factor (CBF) necessary for formation of a CBF-DNA complex: CBF-B interacts simultaneously with both the CBF-A and CBF-C subunits to form a heterotrimeric CBF molecule. Molecular and Cellular Biology. 1996;16(8): 4003–13. doi: 10.1128/mcb.16.8.4003 8754798

2. Romier C, Cocchiarella F, Mantovani R, Moras D. The NF-YB/NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y. Journal of Biological Chemistry. 2003; 278(2): 1336–45. doi: 10.1074/jbc.M209635200 12401788

3. Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, et al. The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. The Plant Cell. 2012; 24(12): 4777–92. doi: 10.1105/tpc.112.105734 23275578

4. Laloum T, De Mita S, Gamas P, Baudin M, Niebel A. CCAAT-box binding transcription factors in plants: Y so many?. Trends in Plant Science. 2013; 18(3): 157–66. doi: 10.1016/j.tplants.2012.07.004 22939172

5. Frontini M, Imbriano C, Manni I, Mantovani R. Cell-cycle regulation of NF-YC nuclear localization. Cell Cycle. 2004; 3(2): 205–10. doi: 10.4161/cc.3.2.654

6. Mantovani R. The molecular biology of the CCAAT-binding factor NF-Y. Gene. 1999; 239(1): 15–27. doi: 10.1016/s0378-1119(99)00368-6 10571030

7. Hackenberg D, Wu Y, Voigt A, Adams R, Schramm P, Grimm B. Studies on differential nuclear translocation mechanism and assembly of the three subunits of the Arabidopsis thaliana transcription factor NF-Y. Molecular Plant. 2012; 5(4): 876–88. doi: 10.1093/mp/ssr107 22199235

8. Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, et al. LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. The Plant Cell. 2003; 15(1): 5–18. doi: 10.1105/tpc.006973 12509518

9. Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI, Lapik YR, et al. The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis. Plant Physiology. 2007; 143(4): 1590–600. doi: 10.1104/pp.106.089904 17322342

10. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, et al. Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National Academy of Sciences. 2007; 104(42): 16450–5.

11. Li L, Yu Y, Wei J, Huang G, Zhang D, Liu Y, et al. Homologous HAP5 subunit from Picea wilsonii improved tolerance to salt and decreased sensitivity to ABA in transformed Arabidopsis. Planta. 2013; 238(2): 345–56. doi: 10.1007/s00425-013-1894-0 23703145

12. Yan DH, Xia X, Yin W. NF-YB family genes identified in a poplar genome-wide analysis and expressed in Populus euphratica are responsive to drought stress. Plant Molecular Biology Reporter. 2013; 31(2): 363–70.

13. Siefers N, Dang KK, Kumimoto RW, Bynum WE, Tayrose G, Holt BF. Tissue-specific expression patterns of Arabidopsis NF-Y transcription factors suggest potential for extensive combinatorial complexity. Plant Physiology. 2009; 149(2): 625–41 doi: 10.1104/pp.108.130591 19019982

14. Ballif J, Endo S, Kotani M, MacAdam J, Wu Y. Over-expression of HAP3b enhances primary root elongation in Arabidopsis. Plant Physiology and Biochemistry. 2011; 49(6): 579–83. doi: 10.1016/j.plaphy.2011.01.013 21316979

15. Stephenson TJ, McIntyre CL, Collet C, Xue GP. TaNF-YB3 is involved in the regulation of photosynthesis genes in Triticum aestivum. Functional & Integrative Genomics. 2011; 11(2): 327–40.

16. Sun X, Ling S, Lu Z, Ouyang YD, Liu S, Yao J. OsNF-YB1, a rice endosperm-specific gene, is essential for cell proliferation in endosperm development. Gene. 2014; 551(2): 214–21. doi: 10.1016/j.gene.2014.08.059 25178525

17. Huang M, Hu Y, Liu X, Li Y, Hou X. Arabidopsis LEAFY COTYLEDON1 mediates postembryonic development via interacting with PHYTOCHROME-INTERACTING FACTOR4. The Plant Cell. 2015; 27(11): 3099–111. doi: 10.1105/tpc.15.00750 26566918

18. Soyano T, Kouchi H, Hirota A, Hayashi M. Nodule inception directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genetics. 2013; 9(3): e1003352. doi: 10.1371/journal.pgen.1003352 23555278

19. Ni Z, Hu Z, Jiang Q, Zhang H. GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Molecular Biology. 2013; 82(1–2): 113–29. doi: 10.1007/s11103-013-0040-5 23483290

20. Alam MM, Tanaka T, Nakamura H, Ichikawa H, Kobayashi K, Yaeno T, et al. Overexpression of a rice heme activator protein gene (Os HAP 2E) confers resistance to pathogens, salinity and drought, and increases photosynthesis and tiller number. Plant Biotechnology Journal. 2015; 13(1): 85–96. doi: 10.1111/pbi.12239 25168932

21. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, et al. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post transcriptionally to promote drought resistance. The Plant Cell. 2008; 20(8): 2238–51. doi: 10.1105/tpc.108.059444 18682547

22. Han X, Tang S, An Y, Zheng DC, Xia XL, Yin WL. Overexpression of the poplar NF-YB7 transcription factor confers drought tolerance and improves water-use efficiency in Arabidopsis. Journal of Experimental Botany. 2013; 64(14): 4589–601. doi: 10.1093/jxb/ert262 24006421

23. Chen M, Zhao Y, Zhuo C, Lu S, Guo Z. Overexpression of a NF‐YC transcription factor from Bermuda grass confers tolerance to drought and salinity in transgenic rice. Plant Biotechnology Journal. 2015; 13(4): 482–91. doi: 10.1111/pbi.12270 25283804

24. Zhang F, Han M, Lv Q, Bao F, He Y. Identification and expression profile analysis of NUCLEAR FACTOR-Y families in Physcomitrella patens. Frontiers in Plant Science. 2015; 6: 642. doi: 10.3389/fpls.2015.00642 26347760

25. Stephenson TJ, McIntyre CL, Collet C, Xue GP. Genome-wide identification and expression analysis of the NF-Y family of transcription factors in Triticum aestivum. Plant Molecular Biology. 2007; 65(1–2): 77–92. doi: 10.1007/s11103-007-9200-9 17598077

26. Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N. Identification, characterization and interaction of HAP family genes in rice. Molecular Genetics and Genomics. 2008; 279(3): 279–89. doi: 10.1007/s00438-007-0312-3 18193457

27. Yang W, Lu Z, Xiong Y, Yao J. Genome-wide identification and co-expression network analysis of the OsNF-Y gene family in rice. The Crop Journal. 2017; 5(1): 21–31.

28. Zhao H, Wu D, Kong F, Lin K, Zhang H, Li G. The Arabidopsis thaliana nuclear factor Y transcription factors. Frontiers in Plant Science. 2017; 7:2045. doi: 10.3389/fpls.2016.02045 28119722

29. Cao S, Kumimoto RW, Siriwardana CL, Risinger JR, Holt BF III. Identification and characterization of NF-Y transcription factor families in the monocot model plant Brachypodium distachyon. PloS ONE. 2011; 6(6): e21805. doi: 10.1371/journal.pone.0021805 21738795

30. Liang M, Yin X, Lin Z, Zheng Q, Liu G, Zhao G. Identification and characterization of NF-Y transcription factor families in Canola (Brassica napus L.). Planta. 2014; 239(1): 107–26. doi: 10.1007/s00425-013-1964-3 24097262

31. Feng ZJ, He GH, Zheng WJ, Lu PP, Chen M, Gong YM, et al. Foxtail millet NF-Y families: genome-wide survey and evolution analyses identified two functional genes important in abiotic stresses. Frontiers in Plant Science. 2015; 6: 1142. doi: 10.3389/fpls.2015.01142 26734043

32. Quach TN, Nguyen HT, Valliyodan B, Joshi T, Xu D, Nguyen HT. Genome-wide expression analysis of soybean NF-Y genes reveals potential function in development and drought response. Molecular Genetics and Genomics. 2015; 290(3): 1095–115. doi: 10.1007/s00438-014-0978-2 25542200

33. Yang J, Wan XL, Guo C, Zhang JW, Bao MZ. Identification and expression analysis of nuclear factor Y families in Prunus mume under different abiotic stresses. Biologia Plantarum. 2016; 60(3): 419–26.

34. Wang Y, Xu W, Chen Z, Han B, Haque ME, Liu A. Gene structure, expression pattern and interaction of Nuclear Factor-Y family in castor bean (Ricinus communis). Planta. 2018; 247(3): 559–72. doi: 10.1007/s00425-017-2809-2 29119268

35. Pereira SL, Martins CP, Sousa AO, Camillo LR, Araujo CP, Alcantara GM, et al. Genome-wide characterization and expression analysis of citrus NUCLEAR FACTOR-Y (NF-Y) transcription factors identified a novel NF-YA gene involved in drought-stress response and tolerance. PloS ONE. 2018; 13(6): e0199187. doi: 10.1371/journal.pone.0199187 29906271

36. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, et al. The Sorghum bicolor genome and the diversification of grasses. Nature. 2009; 457(7229): 551. doi: 10.1038/nature07723 19189423

37. Tuberosa R, Salvi S, Sanguineti MC, Landi P, Maccaferri M, Conti S. Mapping QTLs regulating morpho‐physiological traits and yield: Case studies, shortcomings and perspectives in drought‐stressed maize. Annals of Botany. 2002; 89(7): 941–63.

38. Mace ES, Tai S, Gilding EK, Li Y, Prentis PJ, Bian L, et al. Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum. Nature Communications. 2013; 4: 2320. doi: 10.1038/ncomms3320 23982223

39. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, et al. SMART 4.0: towards genomic data integration. Nucleic Acids Research. 2004; 32 (suppl_1): D142–4.

40. Guo AY, Zhu QH, Chen X, Luo JC. GSDS: a gene structure display server. Yi chuan = Hereditas. 2007; 29(8): 1023–6. 17681935

41. Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research. 2006; 34(suppl_2): W369–73.

42. Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the ExPASy server. InThe proteomics protocols handbook 2005 (pp. 571–607). Humana press.

43. Blom N, Sicheritz‐Pontén T, Gupta R, Gammeltoft S, Brunak S. Prediction of post‐translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics. 2004; 4(6): 1633–49. doi: 10.1002/pmic.200300771 15174133

44. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, et al. WoLF PSORT: protein localization predictor. Nucleic Acids Research. 2007; 35(suppl_2): W585–7.

45. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research. 2002; 30(1): 325–7. doi: 10.1093/nar/30.1.325 11752327

46. Dai X, Zhao PX. psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research. 2011; 39(suppl_2): W155–9.

47. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution. 2013; 30(12): 2725–9. doi: 10.1093/molbev/mst197 24132122

48. Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH. Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Molecular Biology and Evolution. 2002; 19(3): 256–62. doi: 10.1093/oxfordjournals.molbev.a004079 11861885

49. Yang S, Zhang X, Yue JX, Tian D, Chen JQ. Recent duplications dominate NBS-encoding gene expansion in two woody species. Molecular Genetics and Genomics. 2008; 280(3): 187–98. doi: 10.1007/s00438-008-0355-0 18563445

50. Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research. 2006; 34(suppl_2): W609–12. doi: 10.1093/nar/gkl315 16845082

51. 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 Research. 2014; 43(D1): D447–52.

52. Sudhakar Reddy P, Srinivas Reddy D, Sivasakthi K, Bhatnagar-Mathur P, Vadez V, Sharma KK. Evaluation of sorghum [Sorghum bicolor (L.)] reference genes in various tissues and under abiotic stress conditions for quantitative real-time PCR data normalization. Frontiers in Plant Science. 2016; 7: 529. doi: 10.3389/fpls.2016.00529 27200008

53. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C T method. Nature Protocols. 2008; 3(6): 1101. 18546601

54. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, et al. The draft genome of sweet orange (Citrus sinensis). Nature genetics. 2013; 45(1): 59. doi: 10.1038/ng.2472 23179022

55. Malviya N, Jaiswal P, Yadhav D. Genome-wide characterization of Nuclear Factor Y (NF-Y) gene family of sorghum [Sorghum bicolor (L.) Moench]: a bioinformatics approach. Physiology and Molecular Biology of Plants. 2016; 22(1): 33–49. doi: 10.1007/s12298-016-0349-z 27186017

56. 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. 2013; 42(D1): D1182–7.

57. Koralewski TE, Krutovsky KV. Evolution of exon-intron structure and alternative splicing. PLoS ONE. 2011; 6(3): e18055. doi: 10.1371/journal.pone.0018055 21464961

58. Combier JP, Frugier F, De Billy F, Boualem A, El-Yahyaoui F, Moreau S, et al. MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes & Development. 2006; 20(22): 3084–8.

59. Li T, Zhang H, Liu Z, Deng H, Sharma S, Wei X, et al. A group of nuclear factor Y transcription factors are sub-functionalized during endosperm development in monocots. Journal of experimental botany. 2018; 69(10): 2495–510. doi: 10.1093/jxb/ery087 29514259

60. Chu H, Nguyen K, Watanabe Y, Le D, Pham T, Mochida K, et al. Identification, Structural Characterization and Gene Expression Analysis of Members of the Nuclear Factor-Y Family in Chickpea (Cicer arietinum L.) under Dehydration and Abscisic Acid Treatments. International journal of molecular sciences. 2018; 19(11): 3290.

61. Li S, Li K, Ju Z, Cao D, Fu D, Zhu H, et al. Genome-wide analysis of tomato NF-Y factors and their role in fruit ripening. BMC Genomics. 2016; 17(1): 36.

62. Roy SW, Gilbert W. The evolution of spliceosomal introns: patterns, puzzles and progress. Nature Reviews Genetics. 2006; 7(3): 211. doi: 10.1038/nrg1807 16485020

63. Fedorova L, Fedorov A. Introns in gene evolution. InOrigin and evolution of new gene functions. Springer, Dordrecht. 2003; 123–131.

64. Le Hir H, Nott A, Moore MJ. How introns influence and enhance eukaryotic gene expression. Trends in Biochemical Sciences. 2003; 28(4): 215–20. doi: 10.1016/S0968-0004(03)00052-5 12713906

65. Testa A, Donati G, Yan P, Romani F, Huang TH, Vigano MA, et al. Chromatin immunoprecipitation (ChIP) on chip experiments uncover a widespread distribution of NF-Y binding CCAAT sites outside of core promoters. Journal of Biological Chemistry. 2005; 280(14): 13606–15. doi: 10.1074/jbc.M414039200 15647281

66. Hahn ST, Pinkham JE, Wei R, Miller RE, Guarente LE. The HAP3 regulatory locus of Saccharomyces cerevisiae encodes divergent overlapping transcripts. Molecular and Cellular Biology. 1988; 8(2): 655–63. doi: 10.1128/mcb.8.2.655 2832732

67. Xing Y, Fikes JD, Guarente L. Mutations in yeast HAP2/HAP3 define a hybrid CCAAT box binding domain. The EMBO Journal. 1993; 12(12): 4647–55. 8223474

68. Steidl S, Tuncher A, Goda H, Guder C, Papadopoulou N, Kobayashi T, et al. A single subunit of a heterotrimeric CCAAT-binding complex carries a nuclear localization signal: piggy back transport of the pre-assembled complex to the nucleus. Journal of Molecular Biology. 2004; 342(2): 515–24. doi: 10.1016/j.jmb.2004.07.011 15327951

69. Liu JX, Howell SH. bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. The Plant Cell. 2010; 22(3): 782–96. doi: 10.1105/tpc.109.072173 20207753

70. Caras IW, Weddell GN, Davitz MA, Nussenzweig V, Martin DW. Signal for attachment of a phospholipid membrane anchor in decay accelerating factor. Science. 1987; 238(4831): 1280–3. doi: 10.1126/science.2446389 2446389

71. Kong H, Landherr LL, Frohlich MW, Leebens‐Mack J, Ma H, DePamphilis CW. Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. The Plant Journal. 2007; 50(5): 873–85. doi: 10.1111/j.1365-313X.2007.03097.x 17470057

72. Nekrutenko A, Baker RJ. Sub genome-specific markers in allopolyploid cotton Gossypium hirsutum: implications for evolutionary analysis of polyploids. Gene. 2003; 306: 99–103. doi: 10.1016/s0378-1119(03)00427-x 12657471

73. Washida H, Wu CY, Suzuki A, Yamanouchi U, Akihama T, Harada K, et al. Identification of cis-regulatory elements required for endosperm expression of the rice storage protein glutelin gene GluB-1. Plant Molecular Biology. 1999; 40(1): 1–2. doi: 10.1023/a:1026459229671 10394940

74. Fang Y, Xie K, Xiong L. Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. Journal of Experimental Botany. 2014; 65(8): 2119–35. doi: 10.1093/jxb/eru072 24604734

75. Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Baurle I. Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. The Plant Cell. 2014; 26(4): 1792–807. doi: 10.1105/tpc.114.123851 24769482

76. Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, et al. Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Molecular Biology. 2009; 10(1): 29.

77. Han X, Tang S, An Y, Zheng DC, Xia XL, Yin WL. Overexpression of the poplar NF-YB7 transcription factor confers drought tolaerance and improves water-use efficiency in Arabidopsis. Ournal of Experimental Botany 2013; 64: 4589–4601.

78. Sorin C, Declerck M, Christ A, Blein T, Ma L, Lelandais‐Briere C, et al. A miR169 isoform regulates specific NF‐YA targets and root architecture in Arabidopsis. New Phytologist. 2014; 202(4): 1197–211. doi: 10.1111/nph.12735 24533947

79. Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, et al. Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnology Letters. 2011; 33(2): 403–9. doi: 10.1007/s10529-010-0436-0 20960221

80. Batistic O, Kudla J. Plant calcineurin B-like proteins and their interacting protein kinases. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 2009; 1793(6): 985–92.

81. Shi Y. Serine/threonine phosphatases: mechanism through structure. Cell. 2009; 139(3): 468–84. doi: 10.1016/j.cell.2009.10.006 19879837

82. Feng ZJ, He GH, Zheng WJ, Lu PP, Chen M, Gong YM, et al. Foxtail millet NF-Y families: genome-wide survey and evolution analyses identified two functional genes important in abiotic stresses. Frontiers in Plant Science. 2015; 6: 1142. doi: 10.3389/fpls.2015.01142 26734043

83. Xu L, Lin Z, Tao Q, Liang M, Zhao G, Yin X, et al. Multiple NUCLEAR FACTOR Y transcription factors respond to abiotic stress in Brassica napus L. PloS ONE. 2014; 9(10): e111354. doi: 10.1371/journal.pone.0111354 25356551

84. Zhang T, Zhang D, Liu Y, Luo C, Zhou Y, Zhang L. Overexpression of a NF-YB3 transcription factor from Picea wilsonii confers tolerance to salinity and drought stress in transformed Arabidopsis thaliana. Plant Physiology and Biochemistry. 2015; 94: 153–16 doi: 10.1016/j.plaphy.2015.05.001 26093308

85. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, et al. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. The PlantJournal. 2002; 31(3): 279–92.

86. Van Ha C, Esfahani MN, Watanabe Y, Tran UT, Sulieman S, Mochida K, et al. Genome-wide identification and expression analysis of the CaNAC family members in chickpea during development, dehydration and ABA treatments. PLoS One. 2014; 9(12):e114107. doi: 10.1371/journal.pone.0114107 25479253

87. Barbosa EG, Leite JP, Marin SR, Marinho JP, Carvalho JD, Fuganti-Pagliarini R, et al. Overexpression of the ABA-dependent AREB1 transcription factor from Arabidopsis thaliana improves soybean tolerance to water deficit. Plant molecular biology reporter. 2013; 31(3): 719–30.

88. Yan H, Jia H, Chen X, Hao L, An H, Guo X. The cotton WRKY transcription factor GhWRKY17 functions in drought and salt stress in transgenic Nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant and Cell Physiology. 2014; 55(12):2060–76. doi: 10.1093/pcp/pcu133 25261532

89. Yang X, Yang YN, Xue LJ, Zou MJ, Liu JY, Chen F, et al. Rice ABI5-Like1 regulates abscisic acid and auxin responses by affecting the expression of ABRE-containing genes. Plant physiology. 2011; 156(3):1397–409. doi: 10.1104/pp.111.173427 21546455

90. Kim JS, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T, et al. An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant and Cell Physiology. 2011; 52(12): 2136–46. doi: 10.1093/pcp/pcr143 22025559

91. Zhang H, Zhu H, Pan Y, Yu Y, Luan S, Li L. A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Molecular plant. 2014; 7(10): 1522–32. doi: 10.1093/mp/ssu063 24851876

92. Lan Thi Hoang X, Du Nhi NH, Binh Anh Thu N, Phuong Thao N, Phan Tran LS. Transcription factors and their roles in signal transduction in plants under abiotic stresses. Current genomics. 2017; 18(6):483–97. doi: 10.2174/1389202918666170227150057 29204078

93. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, et al. Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National Academy of Science, USA. 2007; 104: 16450–16455.

94. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, et al. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell. 2008; 20: 2238–2251. doi: 10.1105/tpc.108.059444 18682547

95. Chen M, Zhao Y, Zhuo C, Lu S, Guo Z. Overexpression of a NF-YC transcription factor from bermudagrass confers tolerance to drought and salinity in transgenic rice. Plant Biotechnology Journal. 2015, 13: 482–491. doi: 10.1111/pbi.12270 25283804

Genome-wide identification and expression profile analysis of nuclear factor Y family genes in Sorghum bicolor L. (Moench)

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PLOS One

Získaná hemofilie - Povědomí o nemoci a její diagnostika

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