NAC transcription factors in senescence: from molecular structure to function in crops

Plants

Volumn 4, Issue 3, 2015, Pages 412-448

  Podzimska Sroka, Dagmara ^a   O’Shea, Charlotte ^b   Gregersen, Per L ^a   Skriver, Karen ^b  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Abiotic stress; Crop breeding; Domain structure; Gene regulatory network; NAC transcription factor; Senescence

Indexed keywords

EID: 84949549378     PISSN: None     EISSN: 22237747     Source Type: Journal    
DOI: 10.3390/plants4030412     Document Type: Review

References (171)

1. Feller, U.; Fisher, A. Nitrogen metabolism in senescing leaves. Crit. Rev. Plant Sci. 1994, 1, 241–273.
2. Thomas, H. Aging in the plant and animal kingdoms? The role of cell death. Rev. Clin. Gerontol. 1994, 4, 5–20.
3. Buchanan-Wollaston, V. The molelcular biology of leaf senescence. J. Exp. Biol. 1997, 48, 181–199.
4. Buchanan-Wollaston, V.; Earl, S.; Harrison, E.; Mathas, E.; Navabpour, S.; Page, T.; Pink, D. The molecular analysis of leaf senescence—A genomics approach. Plant Biotechnol. J. 2003, 1, 3–22.
5. Hopkins, M.; Taylor, C.; Liu, Z.; Ma, F.; McNamara, L.; Wang, T.W.; Thompson, J.E. Regulation and execution of molecular disassembly and catabolism during senescence. New Phytol. 2007, 175, 201–214.
6. Lim, P.O.; Woo, H.R.; Nam, H.G. Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Sci. 2003, 8, 272–278.
7. Guiboileau, A.; Sormani, R.; Meyer, C.; Masclaux-Daubresse, C. Senescence and death of plant organs: Nutrient recycling and developmental regulation. C. R. Biol. 2010, 333, 382–391.
8. Gregersen, P.L. Senescence and nutrient remobilization in crop plants. In The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops; Hawkesford, M.J., Barraclough, P., Eds.; Wiley-Blackwell: Oxford, UK, 2011; pp. 83–102.
9. Fisher, A. The complex regulation of senescence. Crit. Rev. Plant Sci. 2012, 31, 124–147.
10. Gregersen, P.L.; Culetic, A.; Boschian, L.; Krupinska, K. Plant senescence and crop productivity. Plant Mol. Biol. 2013, 82, 603–622.
11. Lim, P.O.; Kim, H.J.; Nam, H.G. Leaf senescence. Annu. Rev. Plant Biol. 2007, 58, 115–136.
12. Woo, H.R.; Kim, H.J.; Nam, H.G.; Lim, P.O. Plant leaf senescence and death—Regulation by multiple layers of control and implications for aging in general. J. Cell Sci. 2013, 126, 4823–4833.
13. Ghanem, M.E.; Albacete, A.; Martinez-Andujar, C.; Acosta, M.; Romero-Aranda, R.; Dodd, I.C.; Lutts, S.; Perez-Alfocea, F. Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J. Exp. Bot. 2008, 59, 3039–3050.
14. Gepstein, S.; Glick, B.R. Strategies to ameliorate abiotic stress-induced plant senescence. Plant Mol. Biol. 2013, 82, 623–633.
15. Khanna-Chopra, R. Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma 2012, 249, 469–481.
16. Lers, A. Evironmental regulation of senescence. In Senescence Processes in Plants; Gan, S., Ed.; Blackwell Publishing Ltd: Oxford, UK, 2007; pp. 108–144.
17. Thomas, H.; Stoddart, J.L. Leaf senescence. Annu. Rev. Plant Physiol. 1980, 31, 83–111.
18. Jibran, R.; Hunter, A.; Dijkwel, P. Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Biol. 2013, 82, 547–561.
19. Gosti, F.; Beaudoin, N.; Serizet, C.; Webb, A.A.; Vartanian, N.; Giraudat, J. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 1999, 11, 1897–1910.
20. Even-Chen, Z.; Itai, C. The role of abscisic acid in senescence of detached tobacco leaves. Physiol. Plant 2015, 34, 97–100.
21. Gepstein, S.; Thimann, K.V. Changes in the abscisic acid content of oat leaves during senescence. Proc. Natl. Acad. Sci. USA 1980, 77, 2050–2053.
22. Philosoph-Hadas, S.; Hadas, E.; Aharoni, N. Characterization and use in ELISA of new monoclonal antibody for quantitation of abscisic acid in senescing rice leaves. Plant Growth Regul. 1993, 12, 71–78.
23. He, P.; Osaki, M.; Takebe, M.; Shinano, T.; Wasaki, J. Endogenous hormones and expression of senescence-related genes in different senescent types of maize. J. Exp. Bot. 2005, 56, 1117–1128.
24. Zhao, H.; Qiu, K.; Ren, G.; Zhu, Y.; Kuai, B. A pleiotropic phenotype is associated with altered endogenous hormone balance in the developmentally stunted mutant (dsm1). J. Plant. Biol. 2010, 53, 79–87.
25. Buchanan-Wollaston, V.; Page, T.; Harrison, E.; Breeze, E.; Lim, P.O.; Nam, H.G.; Lin, J.F.; Wu, S.H.; Swidzinski, J.; Ishizaki, K.; et al. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 2005, 42, 567–585.
26. Allu, A.D.; Soja, A.M.; Wu, A.; Szymanski, J.; Balazadeh, S. Salt stress and senescence: Identification of cross-talk regulatory components. J. Exp. Bot. 2014, 65, 3993–4008.
27. Breeze, E.; Harrison, E.; McHattie, S.; Hughes, L.; Hickman, R.; Hill, C.; Kiddle, S.; Kim, Y.S.; Penfold, C.A.; Jenkins, D.; et al. High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 2011, 23, 873–894.
28. Liang, C.; Wang, Y.; Zhu, Y.; Tang, J.; Hu, B.; Liu, L.; Ou, S.; Wu, H.; Sun, X.; Chu, J.; Chu, C. OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc. Natl. Acad. Sci. USA 2014, 111, 10013–10018.
29. Guo, Y.; Gan, S. Leaf senescence: Signals, execution, and regulation. Curr. Top. Dev. Biol. 2005, 71, 83–112.
30. Kim, J.; Chang, C.; Tucker, M.L. To grow old: Regulatory role of ethylene and jasmonic acid in senescence. Plant Sci. 2015, 6, 1–7.
31. Jing, H.C.; Schippers, J.H.; Hille, J.; Dijkwel, P.P. Ethylene-induced leaf senescence depends on age-related changes and OLD genes in Arabidopsis. J. Exp. Bot. 2005, 56, 2915–2923.
32. Grbić, V.; Bleecker, A.B. Ethylene regualtes the timing of leaf senescence in Arabidopsis. Plant J. 1995, 8, 595–602.
33. Oh, S.A.; Park, J.H.; Lee, G.I.; Paek, K.H.; Park, S.K.; Nam, H.G. Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J. 1997, 12, 527–535.
34. Jing, H.C.; Sturre, M.J.; Hille, J.; Dijkwel, P.P. Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J. 2002, 32, 51–63.
35. Schippers, J.H.M.; Jing, H.-C.; Hille, J.; Dijkwel, P.P. Developmental and hormonal control of leaf senescence. In Senescence Processes in Plants; Gan, S.; Ed.; Blackwell Publishing Ltd: Oxford, UK, 2007; pp. 145–170.
36. Noodén, L.D.; Singh, S.; Letham, D.S. Correlation of xylem sap cytokinin levels with monocarpic senescence in soybean. Plant Physiol. 1990, 93, 33–39.
37. Gan, S.; Amasino, R.M. Making Sense of Senescence (Molecular Genetic Regulation and Manipulation of Leaf Senescence). Plant Physiol. 1997, 113, 313–319.
38. Ori, N.; Juarez, M.T.; Jackson, D.; Yamaguchi, J.; Banowetz, G.M.; Hake, S. Leaf senescence is delayed in tobacco plants expressing the maize homeobox gene knotted1 under the control of a senescence-activated promoter. Plant Cell 1999, 11, 1073–1080.
39. Masferrer, A.; Arro, M.; Manzano, D.; Schaller, H.; Fernandez-Busquets, X.; Moncalean, P.; Fernandez, B.; Cunillera, N.; Boronat, A.; Ferrer, A. Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels. Plant J. 2002, 30, 123–132.
40. Guo, Y.; Cai, Z.; Gan, S. Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ. 2004, 276, 521–549.
41. Lin, J.F.; Wu, S.H. Molecular events in senescing Arabidopsis leaves. Plant J. 2004, 39, 612–628.
42. Van der Graaff, E.; Schwacke, R.; Schneider, A.; Desimone, M.; Flugge, U.I.; Kunze, R. Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 2006, 141, 776–792.
43. Balazadeh, S.; Riano-Pachon, D.M.; Mueller-Roeber, B. Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol. Stuttg. 2008, 10, S63–S75.
44. Gregersen, P.L.; Holm, P.B. Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotechnol. J. 2007, 5, 192–206.
45. Christiansen, M.W.; Gregersen, P.L. Members of the barley NAC transcription factor gene family show differential co-regulation with senescence-associated genes during senescence of flag leaves. J. Exp. Bot. 2014, 65, 4009–4022.
46. Thomas, H.; Smart, C.M. Crops that stay green. Ann. Appl. Biol. 1993, 123, 193–219.
47. Thomas, H.; Howarth, C.J. Five ways to stay green. J. Exp. Bot. 2000, 51, 329–337.
48. Jukanti, A.K.; Heidlebaugh, N.M.; Parrott, D.L.; Fischer, I.A.; McInnerney, K.; Fischer, A.M. Comparative transcriptome profiling of near-isogenic barley (Hordeum vulgare) lines differing in the allelic state of a major grain protein content locus identifies genes with possible roles in leaf senescence and nitrogen reallocation. New Phytol. 2008, 177, 333–349.
49. Parrott, D.L.; Martin, J.M.; Fischer, A.M. Analysis of barley (Hordeum vulgare) leaf senescence and protease gene expression: A family C1A cysteine protease is specifically induced under conditions characterized by high carbohydrate, but low to moderate nitrogen levels. New Phytol. 2010, 187, 313–331.
50. Christiansen, M.W.; Holm, P.B.; Gregersen, P.L. Characterization of barley (Hordeum vulgare L.) NAC transcription factors suggests conserved functions compared to both monocots and dicots. BMC Res. Notes 2011, 4, 302.
51. Hollmann, J.; Gregersen, P.L.; Krupinska, K. Identification of predominant genes involved in regulation and execution of senescence-associated nitrogen remobilization in flag leaves of field grown barley. J. Exp. Bot. 2014, 65, 3963–3973.
52. Shah, S.T.; Pang, C.; Fan, S.; Song, M.; Arain, S.; Yu, S. Isolation and expression profiling of GhNAC transcription factor genes in cotton (Gossypium hirsutum L.) during leaf senescence and in response to stresses. Gene 2013, 531, 220–234.
53. Lin, M.; Pang, C.; Fan, S.; Song, M.; Wei, H.; Yu, S. Global analysis of the Gossypium hirsutum L. Transcriptome during leaf senescence by RNA-Seq. BMC Plant Biol. 2015, 15, 43.
54. Quirino, B.F.; Noh, Y.S.; Himelblau, E.; Amasino, R.M. Molecular aspects of leaf senescence. Trends Plant Sci. 2000, 5, 278–282.
55. Olsen, A.N.; Ernst, H.A.; Leggio, L.L.; Skriver, K. NAC transcription factors: Structurally distinct, functionally diverse. Trends Plant Sci. 2005, 10, 79–87.
56. 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.
57. Nakashima, K.; Takasaki, H.; Mizoi, J.; Shinozaki, K.; Yamaguchi-Shinozaki, K. NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 2012, 1819, 97–103.
58. Guo, Y.; Gan, S. AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 2006, 46, 601–612.
59. Kim, J.H.; Woo, H.R.; Kim, J.; Lim, P.O.; Lee, I.C.; Choi, S.H.; Hwang, D.; Nam, H.G. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 2009, 323, 1053–1057.
60. Balazadeh, S.; Kwasniewski, M.; Caldana, C.; Mehrnia, M.; Zanor, M.I.; Mueller-Roeber, B.; Xue, G.P. ORS1, an H(2)O(2)-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol. Plant 2011, 4, 346–360.
61. Wu, A.; Allu, A.D.; Garapati, P.; Siddiqui, H.; Dortay, H.; Munne-Bosch, S.; Asensi-Fabado, M.A.; Zanor, M.I.; Antonio, C.; Tohge, T.; et al. JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 2012, 24, 482–506.
62. Yang, S.D.; Seo, P.J.; Yoon, H.K.; Park, C.M. The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 2011, 23, 2155–2168.
63. Kim, Y.S.; Sakuraba, Y.; Han, S.H.; Yoo, S.C.; Paek, N.C. Mutation of the Arabidopsis NAC016 transcription factor delays leaf senescence. Plant Cell Physiol. 2013, 54, 1660–1672.
64. Garapati, P.; Xue, G.P.; Munne-Bosch, S.; Balazadeh, S. Transcription Factor ATAF1 in Arabidopsis Promotes Senescence by Direct Regulation of Key Chloroplast Maintenance and Senescence Transcriptional Cascades. Plant Physiol. 2015, in press.
65. Balazadeh, S.; Siddiqui, H.; Allu, A.D.; Matallana-Ramirez, L.P.; Caldana, C.; Mehrnia, M.; Zanor, M.I.; Kohler, B.; Mueller-Roeber, B. A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 2010, 62, 250–264.
66. Hickman, R.; Hill, C.; Penfold, C.A.; Breeze, E.; Bowden, L.; Moore, J.D.; Zhang, P.; Jackson, A.; Cooke, E.; Bewicke-Copley, F.; et al. A local regulatory network around three NAC transcription factors in stress responses and senescence in Arabidopsis leaves. Plant J. 2013, 75, 26–39.
67. Uauy, C.; Distelfeld, A.; Fahima, T.; Blechl, A.; Dubcovsky, J. A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 2006, 314, 1298–1301.
68. Rauf, M.; Arif, M.; Dortay, H.; Matallana-Ramirez, L.P.; Waters, M.T.; Gil, N.H.; Lim, P.O.; Mueller-Roeber, B.; Balazadeh, S. ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. EMBO Rep. 2013, 14, 382–388.
69. Olsen, A.N.; Ernst, H.A.; Leggio, L.L.; Skriver, K. DNA-binding specificity and molecular functions of NAC transcription factros. Plant Sci. 2005, 169, 785–797.
70. Truman, W.; Glazebrook, J. Co-expression analysis identifies putative targets for CBP60g and SARD1 regulation. BMC Plant Biol. 2012, 12, 216.
71. Larkin, M.A.; Blackshields, G.; Brown, N.P.; Chenna, R.; McGettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R.; et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23, 2947–2948.
72. Paradis, E.; Claude, J.; Strimmer, K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 2004, 20, 289–290.
73. Shen, H.; Yin, Y.B.; Chen, F.; Xu, Y.; Dixon, R.A. A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenergy Res. 2009, 2, 217–232.
74. Zhao, C.; Avci, U.; Grant, E.H.; Haigler, C.H.; Beers, E.P. XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J. 2008, 53, 425–436.
75. Liu, L.; Zhou, Y.; Zhou, G.; Ye, R.; Zhao, L.; Li, X.; Lin, Y. Identification of early senescence-associated genes in rice flag leaves. Plant Mol. Biol. 2008, 67, 37–55.
76. Xu, X.; Bai, H.; Liu, C.; Chen, E.; Chen, Q.; Zhuang, J.; Shen, B. Genome-wide analysis of microRNAs and their target genes related to leaf senescence of rice. PLoS ONE 2014, 9, e114313.
77. Meng, C.; Caiping, C.; Tianzhen, Z.; Wangzhen, G. Characterization of six novel NAC genes and their responses to abiotic stresses in Gossypium hirsutum l. Plant Sci. 2009, 176, 352–359.
78. Huang, G.-Q.; Li, W.; Zhou, W.; Zhang, J.-M.; Li, D.-D.; Gong, S.-Y.; Li, X.-B. Seven cotton genes encoding putative NAC domain proteins are preferentially expressed in roots and in respoonse to abiotic stress during root development. Plant Growth Regul. 2013, 71, 101–112.
79. Jensen, M.K.; Kjaersgaard, T.; Nielsen, M.M.; Galberg, P.; Petersen, K.; O’Shea, C.; Skriver, K. The Arabidopsis thaliana NAC transcription factor family: Structure-function relationships and determinants of ANAC019 stress signalling. Biochem. J. 2010, 426, 183–196.
80. Jensen, M.K.; Kjaersgaard, T.; Petersen, K.; Skriver, K. NAC genes: Time-specific regulators of hormonal signaling in Arabidopsis. Plant Signal. Behav. 2010, 5, 907–910.
81. Ernst, H.A.; Olsen, A.N.; Larsen, S.; Lo, L.L. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep. 2004, 5, 297–303.
82. Welner, D.H.; Lindemose, S.; Grossmann, J.G.; Mollegaard, N.E.; Olsen, A.N.; Helgstrand, C.; Skriver, K.; Lo, L.L. DNA binding by the plant-specific NAC transcription factors in crystal and solution: A firm link to WRKY and GCM transcription factors. Biochem. J. 2012, 444, 395–404.
83. Zhu, Q.; Zou, J.; Zhu, M.; Liu, Z.; Feng, P.; Fan, G.; Wang, W.; Liao, H. In silico analysis on structure and DNA binding mode of AtNAC1, a NAC transcription factor from Arabidopsis thaliana. J. Mol. Model. 2014, 20, 2117.
84. Lindemose, S.; Jensen, M.K.; de Velde, J.V.; O’Shea, C.; Heyndrickx, K.S.; Workman, C.T.; Vandepoele, K.; Skriver, K.; Masi, F.D. A DNA-binding-site landscape and regulatory network analysis for NAC transcription factors in Arabidopsis thaliana. Nucleic Acids Res. 2014, 42, 7681–7693.
85. Bu, Q.; Jiang, H.; Li, C.B.; Zhai, Q.; Zhang, J.; Wu, X.; Sun, J.; Xie, Q.; Li, C. Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res. 2008, 18, 756–767.
86. Zhang, K.; Gan, S.S. An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol. 2012, 158, 961–969.
87. Yang, J.; Worley, E.; Udvardi, M. A NAP-AAO3 Regulatory Module Promotes Chlorophyll Degradation via ABA Biosynthesis in Arabidopsis Leaves. Plant Cell 2014, 26, 4862–4874.
88. Jensen, M.K.; Lindemose, S.; de Masi, F.; Reimer, J.J.; Nielsen, M.; Perera, V.; Workman, C.T.; Turck, F.; Grant, M.R.; Mundy, J.; et al. ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Bio. 2013, 3, 321–327.
89. Tran, L.S.; Nakashima, K.; Sakuma, Y.; Simpson, S.D.; 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. Plant Cell 2004, 16, 2481–2498.
90. Lee, S.; Seo, P.J.; Lee, H.J.; Park, C.M. A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J. 2012, 70, 831–844.
91. Jaspers, P.; Blomster, T.; Brosche, M.; Salojarvi, J.; Ahlfors, R.; Vainonen, J.P.; Reddy, R.A.; Immink, R.; Angenent, G.; Turck, F.; et al. Unequally redundant RCD1 and SRO1 mediate stress and developmental responses and interact with transcription factors. Plant J. 2009, 60, 268–279.
92. O’Shea, C.; Kryger, M.; Stender, E.G.; Kragelund, B.B.; Willemoes, M.; Skriver, K. Protein intrinsic disorder in Arabidopsis NAC transcription factors: transcriptional activation by ANAC013 and ANAC046 and their interactions with RCD1. Biochem J 2015, 465, 281–294.
93. Van der Lee, R.; Buljan, M.; Lang, B.; Weatheritt, R.J.; Daughdrill, G.W.; Dunker, A.K.; Gough, J.; Fuxreiter, M.; Gsponer, J.; Jones, D.T.; et al. Classification of Intrinsically Disordered Regions and Proteins. Chem. Rev. 2014, 114, 6589–6631.
94. Dyson, H.J.; Wright, P.E. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 2002, 12, 54–60.
95. Kjaersgaard, T.; Jensen, M.K.; Christiansen, M.W.; Gregersen, P.; Kragelund, B.B.; Skriver, K. Senescence-associated barley NAC (NAM, ATAF1,2, CUC) transcription factor interacts with radical-induced cell death 1 through a disordered regulatory domain. J. Biol. Chem. 2011, 286, 35418–35429.
96. Vacic, V.; Oldfield, C.J.; Mohan, A.; Radivojac, P.; Cortese, M.S.; Uversky, V.N.; Dunker, A.K. Characterization of molecular recognition features, MoRFs, and their binding partners. J. Proteome Res. 2007, 6, 2351–2366.
97. Teotia, S.; Lamb, R.S. The paralogous genes RADICAL-INDUCED CELL DEATH1 and SIMILAR TO RCD ONE1 have partially redundant functions during Arabidopsis development. Plant Physiol. 2009, 151, 180–198.
98. Overmyer, K.; Tuominen, H.; Kettunen, R.; Betz, C.; Langebartels, C.; Sandermann, H., Jr.; Kangasjarvi, J. Ozone-sensitive arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 2000, 12, 1849–1862.
99. Vainonen, J.P.; Jaspers, P.; Wrzaczek, M.; Lamminmaki, A.; Reddy, R.A.; Vaahtera, L.; Brosche, M.; Kangasjarvi, J. RCD1-DREB2A interaction in leaf senescence and stress responses in Arabidopsis thaliana. Biochem. J. 2012, 442, 573–581.
100. Kragelund, B.B.; Jensen, M.K.; Skriver, K. Order by disorder in plant signaling. Trends Plant Sci. 2012, 17, 625–632.
101. Ward, J.J.; McGuffin, L.J.; Bryson, K.; Buxton, B.F.; Jones, D.T. The DISOPRED server for the prediction of protein disorder. Bioinformatics 2004, 20, 2138–2139.
102. Li, T.; Jia, K.P.; Lian, H.L.; Yang, X.; Li, L.; Yang, H.Q. Jasmonic acid enhancement of anthocyanin accumulation is dependent on phytochrome A signaling pathway under far-red light in Arabidopsis. Biochem. Biophys. Res. Commun. 2014, 454, 78–83.
103. Qi, T.; Song, S.; Ren, Q.; Wu, D.; Huang, H.; Chen, Y.; Fan, M.; Peng, W.; Ren, C.; Xie, D. The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate Jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 2011, 23, 1795–1814.
104. Zheng, X.Y.; Spivey, N.W.; Zeng, W.; Liu, P.P.; Fu, Z.Q.; Klessig, D.F.; He, S.Y.; Dong, X. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 2012, 11, 587–596.
105. Fan, W.; Dong, X. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 2002, 14, 1377–1389.
106. He, Z.H.; Cheeseman, I.; He, D.; Kohorn, B.D. A cluster of five cell wall-associated receptor kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis. Plant Mol. Biol. 1999, 39, 1189–1196.
107. Feys, B.J.; Moisan, L.J.; Newman, M.A.; Parker, J.E. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 2001, 20, 5400–5411.
108. Kim, H.J.; Hong, S.H.; Kim, Y.W.; Lee, I.H.; Jun, J.H.; Phee, B.K.; Rupak, T.; Jeong, H.; Lee, Y.; Hong, B.S.; et al. Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. J. Exp. Bot. 2014, 65, 4023–4036.
109. Chao, Q.; Rothenberg, M.; Solano, R.; Roman, G.; Terzaghi, W.; Ecker, J.R. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 1997, 89, 1133–1144.
110. Chang, K.N.; Zhong, S.; Weirauch, M.T.; Hon, G.; Pelizzola, M.; Li, H.; Huang, S.S.; Schmitz, R.J.; Urich, M.A.; Kuo, D.; et al. Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. Elife 2013, 2, e00675.
111. Sharabi-Schwager, M.; Lers, A.; Samach, A.; Guy, C.L.; Porat, R. Overexpression of the CBF2 transcriptional activator in Arabidopsis delays leaf senescence and extends plant longevity. J. Exp. Bot. 2010, 61, 261–273.
112. Zhang, K.; Xia, X.; Zhang, Y.; Gan, S.S. An ABA-regulated and Golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis. Plant J. 2012, 69, 667–678.
113. Alonso, J.M.; Hirayama, T.; Roman, G.; Nourizadeh, S.; Ecker, J.R. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 1999, 284, 2148–2152.
114. Zhou, Y.; Huang, W.; Liu, L.; Chen, T.; Zhou, F.; Lin, Y. Identification and functional characterization of a rice NAC gene involved in the regulation of leaf senescence. BMC Plant Biol. 2013, 13, 132.
115. 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.
116. Distelfeld, A.; Pearce, S.P.; Avni, R.; Scherer, B.; Uauy, C.; Piston, F.; Slade, A.; Zhao, R.; Dubcovsky, J. Divergent functions of orthologous NAC transcription factors in wheat and rice. Plant Mol. Biol. 2012, 78, 515–524.
117. Wu, Y.; Deng, Z.; Lai, J.; Zhang, Y.; Yang, C.; Yin, B.; Zhao, Q.; Zhang, L.; Li, Y.; Yang, C.; et al. Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res. 2009, 19, 1279–1290.
118. Balazadeh, S.; Wu, A.; Mueller-Roeber, B. Salt-triggered expression of the ANAC092-dependent senescence regulon in Arabidopsis thaliana. Plant Signal. Behav. 2010, 5, 733–735.
119. Waters, M.T.; Moylan, E.C.; Langdale, J.A. GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J. 2008, 56, 432–444.
120. Waters, M.T.; Wang, P.; Korkaric, M.; Capper, R.G.; Saunders, N.J.; Langdale, J.A. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 2009, 21, 1109–1128.
121. Kleinow, T.; Himbert, S.; Krenz, H.; Jeske, H.; Koncz, C. NAC domain transcription factor ATAF1 interacts with SNF1-related kinases and silencing of its subfamily causes severe developmental defects in Arabidopsis. Plant Sci. 2009, 177, 360–370.
122. Jossier, M.; Bouly, J.P.; Meimoun, P.; Arjmand, A.; Lessard, P.; Hawley, S.; Grahame, H.D.; Thomas, M. SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J. 2009, 59, 316–328.
123. Jensen, M.K.; Skriver, K. NAC transcription factor gene regulatory and protein-protein interaction networks in plant stress responses and senescence. IUBMB Life 2014, 66, 156–166.
124. Liu, Q.; Kasuga, M.; Sakuma, Y.; Abe, H.; Miura, S.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 1998, 10, 1391–1406.
125. Schramm, F.; Larkindale, J.; Kiehlmann, E.; Ganguli, A.; Englich, G.; von Koskull-Doring, P.; Vierling, E. A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J. 2008, 53, 264–274.
126. Nishizawa-Yokoi, A.; Nosaka, R.; Hayashi, H.; Tainaka, H.; Maruta, T.; Tamoi, M.; Ikeda, M.; Ohme-Takagi, M.; Yoshimura, K.; Yabuta, Y.; et al. HsfA1d and HsfA1e involved in the transcriptional regulation of HsfA2 function as key regulators for the Hsf signaling network in response to environmental stress. Plant Cell Physiol. 2011, 52, 933–945.
127. Yamaguchi, M.; Ohtani, M.; Mitsuda, N.; Kubo, M.; Ohme-Takagi, M.; Fukuda, H.; Demura, T. VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 2010, 22, 1249–1263.
128. Lee, S.; Lee, H.J.; Huh, S.U.; Paek, K.H.; Ha, J.H.; Park, C.M. The Arabidopsis NAC transcription factor NTL4 participates in a positive feedback loop that induces programmed cell death under heat stress conditions. Plant Sci. 2014, 227, 76–83.
129. Shigeoka, S.; Ishikawa, T.; Tamoi, M.; Miyagawa, Y.; Takeda, T.; Yabuta, Y.; Yoshimura, K. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 2002, 53, 1305–1319.
130. Nishizawa, A.; Yabuta, Y.; Yoshida, E.; Maruta, T.; Yoshimura, K.; Shigeoka, S. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 2006, 48, 535–547.
131. Schramm, F.; Ganguli, A.; Kiehlmann, E.; Englich, G.; Walch, D.; von Koskull-Doring, P. The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol. Biol. 2006, 60, 759–772.
132. Yoshida, T.; Sakuma, Y.; Todaka, D.; Maruyama, K.; Qin, F.; Mizoi, J.; Kidokoro, S.; Fujita, Y.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochem. Biophys. Res. Commun. 2008, 368, 515–521.
133. Muller, J.; Boller, T.; Wiemken, A. Trehalose and trehalase in plants: Recent developments. Plant Sci. 1995, 112, 1–9.
134. Verbruggen, N.; Hermans, C. Proline accumulation in plants: A review. Amino Acids 2008, 35, 753–759.
135. Lawes, D.A.; Treharne, K.J. Variation in photosynthetic activity in cereals and its implications in a plant breeding program. I. Variation in seedling leaves and falg leaves. Euphytica 1971, 120, 86–92.
136. Gregersen, P.L.; Holm, P.B.; Krupinska, K. Leaf senescence and nutrient remobilisation in barley and wheat. Plant Bio. Stuttg. 2008, 10, S37–S49.
137. Gong, Y.; Zhang, J.; Gao, J.; Lu, L.; Wang, J. Slow export of photoassimilate from stay-green leaves during late grain’filling stage in hybrid winther wheat (Triticum aestuvum L.). J. Agro Crop Sci. 2005, 191, 292–299.
138. See, D.; Kanazin, V.; Kephart, K.; Blake, T. Mapping genes controlling variation in barley grain protein concentration. Crop Sci. 2002, 42, 680–685.
139. Kade, M.; Barneix, A.J.; Olmos, S.; Dubcovsky, J. Nitrogen uptake and remobilization in tetraploid Langdon durum wheat and a recombinant substitution line with the high grain protein gene Gpc-B1. Plant Breed. 2005, 124, 343–349.
140. Uauy, C.; Brevis, J.C.; Dubcovsky, J. The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. J. Exp. Bot. 2006, 57, 2785–2794.
141. Hagenblad, J.; Asplund, L.; Balfourier, F.; Ravel, C.; Leino, M.W. Strong presence of the high grain protein content allele of NAM-B1 in Fennoscandian wheat. Theor. Appl. Genet. 2012, 125, 1677–1686.
142. Cantu, D.; Pearce, S.P.; Distelfeld, A.; Christiansen, M.W.; Uauy, C.; Akhunov, E.; Fahima, T.; Dubcovsky, J. Effect of the down-regulation of the high Grain Protein Content (GPC) genes on the wheat transcriptome during monocarpic senescence. BMC Genomics 2011, 12, 492.
143. Avni, R.; Zhao, R.; Pearce, S.; Jun, Y.; Uauy, C.; Tabbita, F.; Fahima, T.; Slade, A.; Dubcovsky, J.; Distelfeld, A. Functional characterization of GPC-1 genes in hexaploid wheat. Planta 2014, 239, 313–324.
144. Pearce, S.; Tabbita, F.; Cantu, D.; Buffalo, V.; Avni, R.; Vazquez-Gross, H.; Zhao, R.; Conley, C.J.; Distelfeld, A.; Dubcovksy, J. Regulation of Zn and Fe transporters by the GPC1 gene during early wheat monocarpic senescence. BMC Plant Biol. 2014, 14, 368.
145. Mickelson, S.; See, D.; Meyer, F.D.; Garner, J.P.; Foster, C.R.; Blake, T.K.; Fischer, A.M. Mapping of QTL associated with nitrogen storage and remobilization in barley (Hordeum vulgare L.) leaves. J. Exp. Bot. 2003, 54, 801–812.
146. Yang, L.; Mickelson, S.; See, D.; Blake, T.K.; Fischer, A.M. Genetic analysis of the function of major leaf proteases in barley (Hordeum vulgare L.) nitrogen remobilization. J. Exp. Bot. 2004, 55, 2607–2616.
147. Distelfeld, A.; Korol, A.B.; Dubcovsky, J.; Uauy, C.; Blake, T.; Fahima, T. Colinearity between the barley grain protein content (GPC) QTL on chromosome arm 6HS and the wheat Gpc-B1 region. Mol. Breed. 2008, 22, 25–38.
148. Jamar, C.; Loffet, F.; Frettinger, P.; Ramsay, L.; Fauconnier, M.L.; Du, J.P. NAM-1gene polymorphism and grain protein content in Hordeum. J. Plant Physiol. 2010, 167, 497–501.
149. Cai, S.; Yu, G.; Chen, X.; Huang, Y.; Jiang, X.; Zhang, G.; Jin, X. Grain protein content variation and its association analysis in barley. BMC Plant Biol. 2013, 13, 35.
150. Heidlebaugh, N.M.; Trethewey, B.R.; Jukanti, A.K.; Parrott, D.L.; Martin, J.M.; Fischer, A.M. Effects of a barley (Hordeum vulgare) chromosome 6 grain protein content locus on whole-plant nitrogen reallocation under two different fertilisation regiimes. Funct. Plant Biol. 2008, 35, 619–632.
151. Jukanti, A.K.; Fischer, A.M. A high-grain protein content locus on barley (Hordeum vulgare) chromosome 6 is associated with increased flag leaf proteolysis and nitrogen remobilization. Phys. Plant 2008, 132, 426–439.
152. Distelfeld, A.; Avni, R.; Fischer, A.M. Senescence, nutrient remobilization, and yield in wheat and barley. J. Exp. Bot. 2014, 65, 3783–3798.
153. Lacerenza, J.A.; Parrott, D.L.; Fischer, A.M. A major grain protein content locus on barley (Hordeum vulgare L.) chromosome 6 influences flowering time and sequential leaf senescence. J. Exp. Bot. 2010, 61, 3137–3149.
154. Parrott, D.L.; Downs, E.P.; Fischer, A.M. Control of barley (Hordeum vulgare L.) development and senescence by the interaction between a chromosome six grain protein content locus, day length, and vernalization. J. Exp. Bot. 2012, 63, 1329–1339.
155. Streitner, C.; Danisman, S.; Wehrle, F.; Schoning, J.C.; Alfano, J.R.; Staiger, D. The small glycine-rich RNA binding protein AtGRP7 promotes floral transition in Arabidopsis thaliana. Plant J. 2008, 56, 239–250.
156. Zhao, D.; Derkx, A.P.; Liu, D.C.; Buchner, P.; Hawkesford, M.J. Overexpression of a NAC transcription factor delays leaf senescence and increases grain nitrogen concentration in wheat. Plant Biol. Stuttg. 2015, in press.
157. Fan, K.; Bibi, N.; Gan, S.; Li, F.; Yuan, S.; Ni, M.; Wang, M.; Shen, H.; Wang, X. A novel NAP member GhNAP is involved in leaf senescence in Gossypium hirsutum. J. Exp. Bot. 2015, in press.
158. Dong, H.; Li, W.; Tang, W.; Li, Z.; Zhang, D.; Niu, Y. Yield, quality and leaf senescence of cotton grown at varying planting dates and plant densities in the Yellow River Valley of China. Field Crops Res. 2006, 98, 106–115.
159. Sun, L.; Zhang, H.; Li, D.; Huang, L.; Hong, Y.; Ding, X.S.; Nelson, R.S.; Zhou, X.; Song, F. Functions of rice NAC transcriptional factors, ONAC122 and ONAC131, in defense responses against Magnaporthe grisea. Plant Mol. Biol. 2013, 81, 41–56.
160. Chen, Y.J.; Perera, V.; Christiansen, M.W.; Holme, I.B.; Gregersen, P.L.; Grant, M.R.; Collinge, D.B.; Lyngkjaer, M.F. The barley HvNAC6 transcription factor affects ABA accumulation and promotes basal resistance against powdery mildew. Plant Mol. Biol. 2013, 83, 577–590.
161. Windram, O.; Madhou, P.; McHattie, S.; Hill, C.; Hickman, R.; Cooke, E.; Jenkins, D.J.; Penfold, C.A.; Baxter, L.; Breeze, E.; et al. Arabidopsis defense against Botrytis cinerea: Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 2012, 24, 3530–3557.
162. Balazadeh, S.; Schildhauer, J.; Araujo, W.L.; Munne-Bosch, S.; Fernie, A.R.; Proost, S.; Humbeck, K.; Mueller-Roeber, B. Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: Transcriptomic and metabolomic consequences. J. Exp. Bot. 2014, 65, 3975–3992.
163. McGrann, G.R.; Steed, A.; Burt, C.; Goddard, R.; Lachaux, C.; Bansal, A.; Corbitt, M.; Gorniak, K.; Nicholson, P.; Brown, J.K. Contribution of the drought tolerance-related stress-responsive NAC1 transcription factor to resistance of barley to Ramularia leaf spot. Mol. Plant Pathol. 2015, 16, 201–209.
164. Walters, D.R.; Havis, N.D.; Oxley, S.J.Ramularia collo-cygni: The biology of an emerging pathogen of barley. FEMS Microbiol. Lett. 2008, 279, 1–7.
165. Hu, H.; Dai, M.; Yao, J.; Xiao, B.; Li, X.; Zhang, Q.; Xiong, L. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. USA 2006, 103, 12987–12992.
166. You, J.; Zong, W.; Li, X.; Ning, J.; Hu, H.; Li, X.; Xiao, J.; Xiong, L. The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J. Exp. Bot. 2013, 64, 569–583.
167. 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.
168. Zhong, R.; Lee, C.; Zhou, J.; McCarthy, R.L.; Ye, Z.H. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 2008, 20, 2763–2782.
169. Grant, E.H.; Fujino, T.; Beers, E.P.; Brunner, A.M. Characterization of NAC domain transcription factors implicated in control of vascular cell differentiation in Arabidopsis and Populus. Planta 2010, 232, 337–352.
170. Jervis, J.; Hildreth, S.B.; Sheng, X.; Beers, E.P.; Brunner, A.M.; Helm, R.F. A metabolomic assessment of NAC154 transcription factor overexpression in field grown poplar stem wood. Phytochemistry 2015, 115, 112–120.
171. Couturier, J.; Doidy, J.; Guinet, F.; Wipf, D.; Blaudez, D.; Chalot, M. Glutamine, arginine and the amino acid transporter Pt-CAT11 play important roles during senescence in poplar. Ann. Bot. 2010, 105, 1159–1169.