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Systematic analysis of NAC transcription factors’ gene family and identification of post-flowering drought stress responsive members in sorghum

  • Sepideh Sanjari
  • Reza Shirzadian-Khorramabad
  • Zahra-Sadat ShobbarEmail author
  • Maryam Shahbazi
Original Article

Abstract

Key message

SbNAC genes (131) encoding 183 proteins were identified from the sorghum genome and characterized. The expression patterns of SbSNACs were evaluated at three sampling time points under post-flowering drought stress.

Abstract

NAC proteins are specific transcription factors in plants, playing vital roles in development and response to various environmental stresses. Despite the fact that Sorghum bicolor is well-known for its drought-tolerance, it suffers from grain yield loss due to pre and post-flowering drought stress. In the present study, 131 SbNAC genes encoding 183 proteins were identified from the sorghum genome. The phylogenetic trees were constructed based on the NAC domains of sorghum, and also based on sorghum with Arabidopsis and 8 known NAC domains of other plants, which classified the family into 15 and 19 subfamilies, respectively. Based on the obtained results, 13 SbNAC proteins joined the SNAC subfamily, and these proteins are expected to be involved in response to abiotic stresses. Promoter analysis revealed that all SbNAC genes comprise different stress-associated cis-elements in their promoters. UTRs analysis indicated that 101 SbNAC transcripts had upstream open reading frames, while 39 of the transcripts had internal ribosome entry sites in their 5′UTR. Moreover, 298 miRNA target sites were predicted to exist in the UTRs of SbNAC transcripts. The expression patterns of SbSNACs were evaluated in three genotypes at three sampling time points under post-flowering drought stress. Based on the results, it could be suggested that some gene members are involved in response to drought stress at the post-flowering stage since they act as positive or negative transcriptional regulators. Following further functional analyses, some of these genes might be perceived to be promising candidates for breeding programs to enhance drought tolerance in crops.

Keywords

NAC Drought Sorghum bicolor (L.) Moench Phylogenetic tree Gene expression 

Notes

Acknowledgements

This study was supported by Agricultural Biotechnology Research Institute of Iran (Project Number: 3-03-0305-93122), Education and Extension Organization (AREEO). University of Guilan and the Ministry of Science, Research and Technology are also acknowledged for supporting the project. The authors are grateful for the kind cooperation of Dr. Azim Khazaei and Mr. Mojtaba Jowkar (to plant culture in the field), Dr. Behzad Sorkhi (to provide real-time PCR facility) and Mr. Mohammad Jedari (to create the artworks).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

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References

  1. Afifi A, May S, Clark V (2003) Computer-aided multivariate analysis. CRC Press, LondonGoogle Scholar
  2. Aida M, Ishida T, Fukaki H et al (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857.  https://doi.org/10.1105/tpc.9.6.841 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bailey TL, Boden M, Buske FA et al (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208.  https://doi.org/10.1093/nar/gkp335 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297.  https://doi.org/10.1016/S0092-8674(04)00045-5 CrossRefPubMedGoogle Scholar
  5. Bashirullah A, Cooperstock RL, Lipshitz HD (2001) Spatial and temporal control of RNA stability. Proc Natl Acad Sci USA 98:7025–7028.  https://doi.org/10.1073/pnas.111145698 CrossRefPubMedGoogle Scholar
  6. Benson DA, Boguski MS, Lipman DJ, Ostell J (1997) GenBank. Nucleic Acids Res 25:1–6.  https://doi.org/10.1093/nar/25.1.1 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Blum A (2004) Sorghum physiology. In: Nguyen HT, Blum A (eds) Physiology and biotechnology integration for plant breeding. CRC Press, Boca Raton, pp 141–223Google Scholar
  8. Casa AM, Mitchell SE, Hamblin MT et al (2005) Diversity and selection in sorghum: Simultaneous analyses using simple sequence repeats. Theor Appl Genet 111:23–30.  https://doi.org/10.1007/s00122-005-1952-5 CrossRefPubMedGoogle Scholar
  9. Cenci A, Guignon V, Roux N, Rouard M (2014) Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots. Plant Mol Biol 85:63–80.  https://doi.org/10.1007/s11103-013-0169-2 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chen X, Wang Y, Lv B et al (2014) The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway. Plant Cell Physiol 55:604–619.  https://doi.org/10.1093/pcp/pct204 CrossRefPubMedGoogle Scholar
  11. Collinge M, Boller T (2001) Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol 46:521–529.  https://doi.org/10.1023/A:1010639225091 CrossRefPubMedGoogle Scholar
  12. Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159.  https://doi.org/10.1093/nar/gkr319 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dean C, Schmidt R (1995) Plant genomes: a current molecular description. Annu Rev Plant Physiol Plant Mol Biol 46:395–418.  https://doi.org/10.1146/annurev.pp.46.060195.002143 CrossRefGoogle Scholar
  14. Duval M, Hsieh T-F, Kim S-Y, Thomas TL (2002) Molecular characterization of AtNAM: a member of theArabidopsis NAC domain superfamily. Plant Mol Biol 50:237–248CrossRefPubMedGoogle Scholar
  15. Fang Y, You J, Xie K et al (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genom 280:547–563.  https://doi.org/10.1007/s00438-008-0386-6 CrossRefGoogle Scholar
  16. Finn RD, Coggill P, Eberhardt RY et al (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285.  https://doi.org/10.1093/nar/gkv1344 CrossRefPubMedGoogle Scholar
  17. Finn RD, Attwood TK, Babbitt PC et al (2017) InterPro in 2017—beyond protein family and domain annotations. Nucleic Acids Res 45:D190–D199.  https://doi.org/10.1093/nar/gkw1107 CrossRefPubMedGoogle Scholar
  18. Fujita M, Fujita Y, Maruyama K et al (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876.  https://doi.org/10.1111/j.1365-313X.2004.02171.x CrossRefPubMedGoogle Scholar
  19. Goodstein DM, Shu S, Howson R et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:1178–1186.  https://doi.org/10.1093/nar/gkr944 CrossRefGoogle Scholar
  20. Gray NK, Wickens M (1998) Control of translation initiation in animals. Annu Rev Cell Dev Biol 14:399–458.  https://doi.org/10.1146/annurev.cellbio.14.1.399 CrossRefPubMedGoogle Scholar
  21. Grillo G, Turi A, Licciulli F et al (2010) UTRdb and UTRsite (RELEASE 2010): a collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acids Res 38:D75–D80.  https://doi.org/10.1093/nar/gkp902 CrossRefPubMedGoogle Scholar
  22. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612.  https://doi.org/10.1111/j.1365-313X.2006.02723.x CrossRefPubMedGoogle Scholar
  23. Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549.  https://doi.org/10.1111/j.1365-3040.2003.01158.x CrossRefGoogle Scholar
  24. Ha Van C, Nasr Esfahani M, Watanabe Y et al (2014) Genome-wide identification and expression analysis of the CaNAC family members in chickpea during development, dehydration and ABA treatments. PLoS One 9:e114107.  https://doi.org/10.1371/journal.pone.0114107 CrossRefGoogle Scholar
  25. He X-J, Mu R-L, Cao W-H et al (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916.  https://doi.org/10.1111/j.1365-313X.2005.02575.x CrossRefPubMedGoogle Scholar
  26. He L, Shi X, Wang Y et al (2017) Arabidopsis ANAC069 binds to C[A/G]CG[T/G] sequences to negatively regulate salt and osmotic stress tolerance. Plant Mol Biol 93:369–387.  https://doi.org/10.1007/s11103-016-0567-3 CrossRefPubMedGoogle Scholar
  27. Hofmann N (2013) Endoplasmic reticulum–localized transcription factors and mitochondrial retrograde regulation. Plant Cell 25:10–1105Google Scholar
  28. Hu H, Dai M, Yao J et al (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992.  https://doi.org/10.1073/pnas.0604882103 CrossRefPubMedGoogle Scholar
  29. Hu R, Qi G, Kong Y et al (2010) Comprehensive analysis of NAC domain transcription factor gene family in populus trichocarpa. BMC Plant Biol 10:145.  https://doi.org/10.1186/1471-2229-10-145 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hu B, Jin J, Guo A-Y et al (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297.  https://doi.org/10.1093/bioinformatics/btu817 CrossRefPubMedGoogle Scholar
  31. Ibraheem O, Botha CEJ, Bradley G (2010) In silico analysis of cis-acting regulatory elements in 5′ regulatory regions of sucrose transporter gene families in rice (Oryza sativa Japonica) and Arabidopsis thaliana. Comput Biol Chem 34:268–283.  https://doi.org/10.1016/j.compbiolchem.2010.09.003 CrossRefPubMedGoogle Scholar
  32. Jansen R-P (2001) mRNA localization: message on the move. Nat Rev Mol Cell Biol 2:247–256.  https://doi.org/10.1038/35067016 CrossRefPubMedGoogle Scholar
  33. Jensen MK, Hagedorn PH, de Torres-Zabala M et al (2008) Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J 56:867–880.  https://doi.org/10.1111/j.1365-313X.2008.03646.x CrossRefPubMedGoogle Scholar
  34. Jeong JS, Kim YS, Baek KH et al (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197.  https://doi.org/10.1104/pp.110.154773 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Jeong JS, Kim YS, Redillas MCFR et al (2013) OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol J 11:101–114.  https://doi.org/10.1111/pbi.12011 CrossRefPubMedGoogle Scholar
  36. Jin J, Tian F, Yang DC et al (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045.  https://doi.org/10.1093/nar/gkw982 CrossRefPubMedGoogle Scholar
  37. John I, Hackett R, Cooper W et al (1997) Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Mol Biol 33:641–651.  https://doi.org/10.1023/A:1005746831643 CrossRefPubMedGoogle Scholar
  38. Kadier Y, Zu Y, Dai Q et al (2017) Genome-wide identification, classification and expression analysis of NAC family of genes in sorghum [Sorghum bicolor (L.) Moench]. Plant Growth Regul 83:301–312.  https://doi.org/10.1007/s10725-017-0295-y CrossRefGoogle Scholar
  39. Kato H, Motomura T, Komeda Y et al (2010) Overexpression of the NAC transcription factor family gene ANAC036 results in a dwarf phenotype in Arabidopsis thaliana. J Plant Physiol 167:571–577.  https://doi.org/10.1016/j.jplph.2009.11.004 CrossRefPubMedGoogle Scholar
  40. Kebede H, Subudhi PK, Rosenow DT, Nguyen HT (2001) Quantitative trait loci influencing drought tolerance in grain sorghum (Sorghum bicolor L. Moench). TAG Theor Appl Genet 103:266–276.  https://doi.org/10.1007/s001220100541 CrossRefGoogle Scholar
  41. Kharrazi M, Rad M (2002) Evaluation of sorghum genotypes under drought stress conditions using some stress tolerance indices. Afr J Biotechnol 10(61):13086–13089Google Scholar
  42. Kikuchi K, Ueguchi-Tanaka M, Yoshida KT et al (2000) Molecular analysis of the NAC gene family in rice. MGG Mol Gen Genet 262:1047–1051.  https://doi.org/10.1007/PL00008647 CrossRefPubMedGoogle Scholar
  43. Kim Y-S, Kim S-G, Park J-E et al (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144.  https://doi.org/10.1105/tpc.106.043018 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kim HS, Park BO, Yoo JH et al (2007) Identification of a calmodulin-binding NAC protein as a transcriptional repressor in Arabidopsis. J Biol Chem 282:36292–36302.  https://doi.org/10.1074/jbc.M705217200 CrossRefPubMedGoogle Scholar
  45. Ko J-H, Yang SH, Park AH et al (2007) ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana. Plant J 50:1035–1048.  https://doi.org/10.1111/j.1365-313X.2007.03109.x CrossRefPubMedGoogle Scholar
  46. Kubo M, Udagawa M, Nishikubo N et al (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860.  https://doi.org/10.1101/gad.1331305 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kumar S, Nei M, Dudley J, Tamura K (2006) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. October 88:559–566.  https://doi.org/10.1093/bib/bbn017.MEGA CrossRefGoogle Scholar
  48. Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948.  https://doi.org/10.1093/bioinformatics/btm404 CrossRefGoogle Scholar
  49. Le DT, Nishiyama R, Watanabe Y et al (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18:263–276.  https://doi.org/10.1093/dnares/dsr015 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lee S, Seo PJ, Lee HJ, Park CM (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70:831–844.  https://doi.org/10.1111/j.1365-313X.2012.04932.x CrossRefPubMedGoogle Scholar
  51. Lescot M, Déhais P, Thijs G et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327.  https://doi.org/10.1093/nar/30.1.325 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43:D257–D260.  https://doi.org/10.1093/nar/gku949 CrossRefPubMedGoogle Scholar
  53. Li JQ, Zhang J, Wang XC, Chen J (2010) A membrane-tethered transcription factor ANAC089 negatively regulates floral initiation in Arabidopsis thaliana. Sci China Life Sci 53:1299–1306.  https://doi.org/10.1007/s11427-010-4085-2 CrossRefPubMedGoogle Scholar
  54. Li P, Wind JJ, Shi X et al (2011) Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci 108:3436–3441.  https://doi.org/10.1073/pnas.1018665108 CrossRefPubMedGoogle Scholar
  55. Lu PL, Chen NZ, An R et al (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305.  https://doi.org/10.1007/s11103-006-9089-8 CrossRefPubMedGoogle Scholar
  56. Lu M, Ying S, Zhang D-F et al (2012) A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep 31:1701–1711.  https://doi.org/10.1007/s00299-012-1284-2 CrossRefPubMedGoogle Scholar
  57. Lu M, Zhang D-F, Shi Y-S et al (2013) Expression of SbSNAC1, a NAC transcription factor from sorghum, confers drought tolerance to transgenic Arabidopsis. Plant Cell Tissue Organ Cult 115:443–455.  https://doi.org/10.1007/s11240-013-0375-2 CrossRefGoogle Scholar
  58. Ludlow MM, Muchow RC (1990) A critical evaluation of traits for improving crop yields in water-limited environments. Adv Agron 43:107–153CrossRefGoogle Scholar
  59. Makita Y, Shimada S, Kawashima M et al (2015) MOROKOSHI: transcriptome database in sorghum bicolor. Plant Cell Physiol 56:e6.  https://doi.org/10.1093/pcp/pcu187 CrossRefPubMedGoogle Scholar
  60. Mao C, Ding W, Wu Y et al (2007) Overexpression of a NAC-domain protein promotes shoot branching in rice. New Phytol 176:288–298.  https://doi.org/10.1111/j.1469-8137.2007.02177.x CrossRefPubMedGoogle Scholar
  61. Mao X, Zhang H, Qian X et al (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946.  https://doi.org/10.1093/jxb/err462 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Mao X, Chen S, Li A et al (2014) Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS One.  https://doi.org/10.1371/journal.pone.0084359 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Martínez-Salas E, Piñeiro D, Fernández N (2012) Alternative mechanisms to initiate translation in eukaryotic mRNAs. Comp Funct Genomics 2012:391546CrossRefPubMedPubMedCentralGoogle Scholar
  64. Menz MA, Klein RR, Unruh NC et al (2004) Genetic diversity of public inbreds of sorghum determined by mapped AFLP and SSR markers. Crop Sci 44:1236.  https://doi.org/10.2135/cropsci2004.1236 CrossRefGoogle Scholar
  65. Mignone F, Gissi C, Liuni S, Pesole G (2002) Untranslated regions of mRNAs. Genome Biol 3(3):reviews0004-1CrossRefGoogle Scholar
  66. Morishita T, Kojima Y, Maruta T et al (2009) Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant Cell Physiol 50:2210–2222.  https://doi.org/10.1093/pcp/pcp159 CrossRefPubMedGoogle Scholar
  67. Mostafa M, Shahbazi M, Khazaei A (2011) Effect of post-flowering water stress on yield and physiological characters of grain sorghum genotypes. Iran J Plant Physiol 2(1):341–344Google Scholar
  68. Mullet JE, Klein RR, Klein PE (2002) Sorghum bicolor—an important species for comparative grass genomics and a source of beneficial genes for agriculture. Curr Opin Plant Biol 5:118–121.  https://doi.org/10.1016/S1369-5266(02)00232-7 CrossRefPubMedGoogle Scholar
  69. Nakashima K, Takasaki H, Mizoi J et al (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta Gene Regul Mech 1819:97–103.  https://doi.org/10.1016/j.bbagrm.2011.10.005 CrossRefGoogle Scholar
  70. Ning YQ, Ma ZY, Huang HW et al (2015) Two novel NAC transcription factors regulate gene expression and flowering time by associating with the histone demethylase JMJ14. Nucleic Acids Res 43:1469–1484.  https://doi.org/10.1093/nar/gku1382 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Nuruzzaman M, Manimekalai R, Sharoni AM et al (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44.  https://doi.org/10.1016/J.GENE.2010.06.008 CrossRefPubMedGoogle Scholar
  72. Ohbayashi I, Lin C, Shinohara N, Matsumura Y (2017) Evidence for a role of ANAC082 as a ribosomal stress response mediator leading to growth defects and developmental alterations in Arabidopsis. Plant Cell.  https://doi.org/10.1105/tpc.17.00255 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87.  https://doi.org/10.1016/J.TPLANTS.2004.12.010 CrossRefPubMedGoogle Scholar
  74. Ooka H, Satoh K, Doi K et al (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247CrossRefPubMedGoogle Scholar
  75. Ozretić P, Bisio A, Inga A, Levanat S (2012) The growing relevance of cap-independent translation initiation in cancer-related genes. Period Biol 114(4):471–478Google Scholar
  76. Pesole G, Mignone F, Gissi C et al (2001) Structural and functional features of eukaryotic mRNA untranslated regions. Gene 276:73–81.  https://doi.org/10.1016/S0378-1119(01)00674-6 CrossRefPubMedGoogle Scholar
  77. Podzimska-Sroka D, O’Shea C, Gregersen P, Skriver K (2015) NAC transcription factors in senescence: from molecular structure to function in crops. Plants 4:412–448.  https://doi.org/10.3390/plants4030412 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Rachmat A, Nugroho S, Sukma D, Aswidinnoor H (2014) Overexpression of OsNAC6 transcription factor from Indonesia rice cultivar enhances drought and salt tolerance. Emir J Food Agric 26:519–527.  https://doi.org/10.9755/ejfa.v26i6.17672 CrossRefGoogle Scholar
  79. Reinhart BJ, Weinstein EG, Rhoades MW et al (2002) MicroRNAs in plants. Genes Dev 16:1616–1626.  https://doi.org/10.1101/gad.1004402 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Ren T (2000) HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:1917–1926.  https://doi.org/10.1105/tpc.12.10.1917 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Ricachenevsky FK, Menguer PK, Sperotto RA (2013) kNACking on heaven’s door: how important are NAC transcription factors for leaf senescence and Fe/Zn remobilization to seeds? Front Plant Sci.  https://doi.org/10.3389/fpls.2013.00226 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Riechmann JL, Heard J, Martin G et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110.  https://doi.org/10.1126/science.290.5499.2105 CrossRefPubMedGoogle Scholar
  83. Rooney WL, Blumenthal J, Bean B, Mullet JE (2007) Designing sorghum as a dedicated bioenergy feedstock. Biofuels Bioprod Biorefining 1:147–157.  https://doi.org/10.1002/bbb.15 CrossRefGoogle Scholar
  84. Rosenow D, Ejeta G, Clark L, Gilbert M et al (1997) Breeding for pre- and post-flowering drought stress resistance in sorghum. In: Proceedings of the international conference on genetic improvement of sorghum and pearl millet. INSORMIL, Lincoln, pp 400–411Google Scholar
  85. Rushton P, Bokowiec M, Han S et al (2008) Tobacco transcription factors: novel insights into transcriptional regulation in the Solanaceae. Plant physiol 147(1):280–295CrossRefPubMedPubMedCentralGoogle Scholar
  86. Rychlik W (2007) OLIGO 7 primer analysis software. In: PCR primer design. Humana Press, New York, pp 35–59CrossRefGoogle Scholar
  87. Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM Is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103.  https://doi.org/10.1016/S0092-8674(00)80902-2 CrossRefPubMedGoogle Scholar
  88. Saga H, Ogawa T, Kai K et al (2012) Identification and characterization of ANAC042, a transcription factor family gene involved in the regulation of camalexin biosynthesis in Arabidopsis. Mol Plant-Microbe Interact 25:684–696.  https://doi.org/10.1094/MPMI-09-11-0244 CrossRefPubMedGoogle Scholar
  89. Sakuraba Y, Kim Y-S, Han S-H et al (2015) The Arabidopsis transcription factor NAC016 promotes drought stress responses by repressing AREB1 transcription through a trifurcate feed-forward regulatory loop involving NAP. Plant Cell 27:1771–1787.  https://doi.org/10.1105/tpc.15.00222 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Sanchez AC, Subudhi PK, Rosenow DT, Nguyen HT (2002) Mapping QTLs associated with drought resistance in sorghum (Sorghum bicolor L. Moench). Plant Mol Biol 48:713–726.  https://doi.org/10.1023/A:1014894130270 CrossRefPubMedGoogle Scholar
  91. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108.  https://doi.org/10.1038/nprot.2008.73 CrossRefGoogle Scholar
  92. Seo PJ, Kim MJ, Park JY et al (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661–671.  https://doi.org/10.1111/j.1365-313X.2009.04091.x CrossRefPubMedGoogle Scholar
  93. Shang H, Li W, Zou C, Yuan Y (2013) Analyses of the NAC transcription factor gene family in Gossypium raimondii Ulbr.: chromosomal location, structure, phylogeny, and expression patterns. J Integr Plant Biol 55:663–676.  https://doi.org/10.1111/jipb.12085 CrossRefPubMedGoogle Scholar
  94. Shiriga K, Sharma R, Kumar K et al (2014) Genome-wide identification and expression pattern of drought-responsive members of the NAC family in maize. Meta Gene 2:407–417.  https://doi.org/10.1016/J.MGENE.2014.05.001 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Singh A, Sharma V, Pal A (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). Dna &#8230Google Scholar
  96. Souer E, van Houwelingen A, Kloos D et al (1996) The No apical meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85:159–170.  https://doi.org/10.1016/S0092-8674(00)81093-4 CrossRefPubMedGoogle Scholar
  97. Sperotto RA, Ricachenevsky FK, Duarte GL et al (2009) Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230:985–1002.  https://doi.org/10.1007/s00425-009-1000-9 CrossRefPubMedGoogle Scholar
  98. Subudhi PK, Rosenow DT, Nguyen HT (2000) Quantitative trait loci for the stay green trait in sorghum (Sorghum bicolor L. Moench): consistency across genetic backgrounds and environments. TAG Theor Appl Genet 101:733–741.  https://doi.org/10.1007/s001220051538 CrossRefGoogle Scholar
  99. Sudhakar Reddy P, Srinivas Reddy D, Sivasakthi K et al (2016) Evaluation of sorghum [Sorghum bicolor (L.)] reference genes in various tissues and under abiotic stress conditions for quantitative real-time PCR data normalization. Front Plant Sci 7:1–14.  https://doi.org/10.3389/fpls.2016.00529 CrossRefGoogle Scholar
  100. Tang Y, Liu M, Gao S et al (2012) Molecular characterization of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol Plant 144:210–224.  https://doi.org/10.1111/j.1399-3054.2011.01539.x CrossRefPubMedGoogle Scholar
  101. Tran LP, Nakashima K, Sakuma Y et al (2004) 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. Plant Cell 16:2481–2498.  https://doi.org/10.1105/tpc.104.022699.Shinozaki CrossRefPubMedPubMedCentralGoogle Scholar
  102. Tuinstra MR, Grote EM, Goldsbrough PB, Ejeta G (1997) Genetic analysis of post-flowering drought tolerance and components of grain development in Sorghum bicolor (L.) Moench. Mol Breed 3:439–448.  https://doi.org/10.1023/A:1009673126345 CrossRefGoogle Scholar
  103. Uauy C, Distelfeld A, Fahima T et al (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301.  https://doi.org/10.1126/science.1133649 CrossRefPubMedPubMedCentralGoogle Scholar
  104. Voorrips RE (2002) Computer note MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedPubMedCentralGoogle Scholar
  105. Walulu RS, Rosenow DT, Wester DB, Nguyen HT (1994) Inheritance of the stay green trait in sorghum. Crop Sci 34:970.  https://doi.org/10.2135/cropsci1994.0011183X003400040026x CrossRefGoogle Scholar
  106. Waters BM, Uauy C, Dubcovsky J, Grusak MA (2009) Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. J Exp Bot 60:4263–4274.  https://doi.org/10.1093/jxb/erp257 CrossRefPubMedGoogle Scholar
  107. Willemsen V, Bauch M, Bennett T et al (2008) The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 15:913–922.  https://doi.org/10.1016/j.devcel.2008.09.019 CrossRefPubMedGoogle Scholar
  108. Wu X-Y, Hu W-J, Luo H et al (2016) Transcriptome profiling of developmental leaf senescence in sorghum (Sorghum bicolor). Plant Mol Biol 92:555–580.  https://doi.org/10.1007/s11103-016-0532-1 CrossRefPubMedGoogle Scholar
  109. Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036.  https://doi.org/10.1101/gad.852200 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Xu W, Subudhi PK, Crasta OR et al (2000) Molecular mapping of QTLs conferring stay-green in grain sorghum (Sorghum bicolor L. Moench). Genome 43:461–469.  https://doi.org/10.1139/g00-003 CrossRefPubMedGoogle Scholar
  111. Xu B, Sathitsuksanoh N, Tang Y et al (2012) Overexpression of AtLOV1 in switchgrass alters plant architecture, lignin content, and flowering time. PLoS One.  https://doi.org/10.1371/journal.pone.0047399 CrossRefPubMedPubMedCentralGoogle Scholar
  112. Xue G-P, Way HM, Richardson T et al (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant 4:697–712.  https://doi.org/10.1093/MP/SSR013 CrossRefPubMedGoogle Scholar
  113. Yilmaz A, Nishiyama MY, Fuentes BG et al (2009) GRASSIUS: a platform for comparative regulatory genomics across the grasses. Plant Physiol 149:171–180.  https://doi.org/10.1104/pp.108.128579 CrossRefPubMedPubMedCentralGoogle Scholar
  114. You J, Zhang L, Song B et al (2015) Systematic analysis and identification of stress-responsive genes of the NAC gene family in Brachypodium distachyon. PLoS One 10:e0122027.  https://doi.org/10.1371/journal.pone.0122027 CrossRefPubMedPubMedCentralGoogle Scholar
  115. Zhang L, Zheng Y, Jagadeeswaran G et al (2011) Identification and temporal expression analysis of conserved and novel microRNAs in Sorghum. Genomics 98:460–468.  https://doi.org/10.1016/J.YGENO.2011.08.005 CrossRefPubMedGoogle Scholar
  116. Zhang S, Zhou B, Kang Y et al (2015) C-terminal domains of histone demethylase JMJ14 interact with a pair of NAC transcription factors to mediate specific chromatin association. Cell Discov 1:15003.  https://doi.org/10.1038/celldisc.2015.3 CrossRefPubMedPubMedCentralGoogle Scholar
  117. Zhao C, Avci U, Grant EH et al (2008) XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J 53:425–436.  https://doi.org/10.1111/j.1365-313X.2007.03350.x CrossRefPubMedGoogle Scholar
  118. Zhao J, Liu J-S, Meng F-N et al (2016) ANAC005 is a membrane-associated transcription factor and regulates vascular development in Arabidopsis. J Integr Plant Biol 58:442–451.  https://doi.org/10.1111/jipb.12379 CrossRefPubMedGoogle Scholar
  119. Zhong R, Demura T, Ye Z-H (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell Online 18:3158–3170.  https://doi.org/10.1105/tpc.106.047399 CrossRefGoogle Scholar
  120. Zhong R, Lee C, Zhou J et al (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Online 20:2763–2782.  https://doi.org/10.1105/tpc.108.061325 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Agricultural Biotechnology, Faculty of Agricultural SciencesUniversity of GuilanRashtIran
  2. 2.Department of Systems BiologyAgricultural Biotechnology Research Institute of Iran, Education and Extension Organization (AREEO)KarajIran
  3. 3.Department of Molecular PhysiologyAgricultural Biotechnology Research Institute of Iran, Education and Extension Organization (AREEO)KarajIran

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