NtERF32: A non-NIC2 locus AP2/ERF transcription factor required in jasmonate-inducible nicotine biosynthesis in tobacco

Plant Molecular Biology

Volumn 84, Issue 1-2, 2014, Pages 49-66

  Sears, Marta T ^a   Zhang, Hongbo ^a,b   Rushton, Paul J ^a,c   Wu, Martin ^a   Han, Shengcheng ^a,d   Spano, Anthony J ^a   Timko, Michael P ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b SOUTHWEST UNIVERSITY   (China)

^c TEXAS A AND M UNIVERSITY   (United States)

^d BEIJING NORMAL UNIVERSITY   (China)

Author keywords

Ethylene Response Factor (ERF); Jasmonate; NIC2 locus; Nicotiana; Nicotine; Tobacco

Indexed keywords

ALCOHOL DEHYDROGENASE; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; LACTATE MALATE TRANSHYDROGENASE; LACTATE-MALATE TRANSHYDROGENASE; NICOTINE; OXYLIPIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY; PHYSIOLOGY; PROTEIN MOTIF; RNA INTERFERENCE; TOBACCO;

ALCOHOL OXIDOREDUCTASES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL LINE; CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NICOTINE; OXYLIPINS; PHYLOGENY; PLANT PROTEINS; RNA INTERFERENCE; TOBACCO; TRANSCRIPTION FACTORS;

NICOTIANA; NICOTIANA TABACUM;

EID: 84888342819     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-013-0116-2     Document Type: Article

References (94)

1. Baldwin IT (2010) Plant volatiles. Curr Biol 20: R392-R397.
2. Baldwin IT, Preston CA (1999) The eco-physiological complexity of plant responses to insect herbivores. Planta 208: 137-145.
3. Baldwin IT, Schmelz EA, Ohnmeiss TE (1994) Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris spegazzini and comes. J Chem Ecol 20: 2139-2157.
4. Baldwin IT, Schmelz EA, Zhang ZP (1996) Effects of octadecanoid metabolites and inhibitors on induced nicotine accumulation in Nicotiana sylvestris. J Chem Ecol 22: 61-74.
5. Baldwin IT, Zhang ZP, Diab N, Ohnmeiss TE, McCloud ES, Lynds GY, Schmelz EA (1997) Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201: 397-404.
6. Cane KA, Mayer M, Lidgett AJ, Michael AJ, Hamill JD (2005) Molecular analysis of alkaloid metabolism in AABB v. aabb genotype Nicotiana tabacum in response to wounding of aerial tissues and methyl jasmonate treatment of cultured roots. Funct Plant Biol 32: 305-320.
7. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671.
8. Dat J, Vandenabeele S, Vranová E, van Montagu M, Inzé D, van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57: 779-795.
9. Davies PJ (ed) (2010) Plant hormones, 3 biosynthesis, signal transduction, action. Springer, Netherlands.
10. Dawson RF (1942) Accumulation of nicotine in reciprocal grafts of tomato and tobacco. Am J Bot 29: 66-71.
11. De Boer K, Tilleman S, Pauwels L, Vanden Bossche R, De Sutter V, Vanderhaeghen R, Hilson P, Hamill JD, Goossens A (2011) APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. Plant J 66: 1053-1065.
12. De Luca V, St Pierre B (2000) The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci 5: 168-173.
13. De Sutter V, Vanderhaeghen R, Tilleman S, Lammertyn F, Vanhoutte I, Karimi M, Inze D, Goossens A, Hilson P (2005) Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J 44: 1065-1076.
14. DeBoer K, Lye J, Aitken C, Su A, Hamill JD (2009) The A622 gene in Nicotiana glauca (tree tobacco): evidence for a functional role in pyridine alkaloid synthesis. Plant Mol Biol 69: 299-312.
15. DeBoer KD, Dalton HL, Edward FJ, Hamill JD (2011) RNAi-mediated down-regulation of ornithine decarboxylase (ODC) leads to reduced nicotine and increased anatabine levels in transgenic Nicotiana tabacum L. Phytochemistry 72: 344-355.
16. Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in arabidopsis. Ann Bot 92: 329-337.
17. El-Sharkawy I, Sherif S, Mila I, Bouzayen M, Jayasankar S (2009) Molecular characterization of seven genes encoding ethylene-responsive transcriptional factors during plum fruit development and ripening. J Exp Bot 60: 907-922.
18. Facchini PJ (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annu Rev Plant Physiol Plant Mol Biol 52: 29-66.
19. Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase-inhibitors. Plant Cell 4: 129-134.
20. Fernández-Calvo P et al (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23: 701-715.
21. Fischer U, Dröge-Laser W (2004) Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol Plant Microbe Interact 17: 1162-1171.
22. Goossens A et al (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc Natl Acad Sci USA 100: 8595-8600.
23. Halitschke R, Baldwin I (2004) Jasmonates and related compounds in plant-insect interactions. J Plant Growth Regul 23: 238-245.
24. Hashimoto T, Yamada Y (1994) Alkaloid biogenesis-molecular aspects. Annu Rev Plant Physiol Plant Mol Biol 45: 257-285.
25. Hibi N, Fujita T, Hatano M, Hashimoto T, Yamada Y (1992) Putrescine N-methyltransferase in cultured roots of Hyoscyamus albus. Plant Physiol 100: 826-835.
26. Hibi N, Higashiguchi S, Hashimoto T, Yamada Y (1994) Gene expression in tobacco low-nicotine mutants. Plant Cell 6: 723-735.
27. Hildreth SB et al (2011) Tobacco nicotine uptake permease (NUP1) affects alkaloid metabolism. Proc Natl Acad Sci USA 108: 18179-18184.
28. Hou X, Lee LYC, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19: 884-894.
29. Howe GA (2010) Jasmonates. In: Davies PJ (ed) Plant hormones; biosynthesis, signal transduction, action!. Springer, Netherlands, pp 646-680.
30. Imanishi S, Hashizume K, Nakakita M, Kojima H, Matsubayashi Y, Hashimoto T, Sakagami Y, Yamada Y, Nakamura K (1998) Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures. Plant Mol Biol 38: 1101-1111.
31. Jackson DM, Johnson AW, Stephenson MG (2002) Survival and development of Heliothis virescens (Lepidoptera: Noctuidae) larvae on isogenic tobacco lines with different levels of alkaloids. J Econ Entomol 95: 1294-1302.
32. Jefferson RA, Kavanagh TA, Bevan MW (1987) Gus fusions-β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
33. Kajikawa M, Hirai N, Hashimoto T (2009) A PIP-family protein is required for biosynthesis of tobacco alkaloids. Plant Mol Biol 69: 287-298.
34. Kajikawa M, Shoji T, Kato A, Hashimoto T (2011) Vacuole-localized berberine bridge enzyme-like proteins are required for a late step of nicotine biosynthesis in tobacco. Plant Physiol 155: 2010-2022.
35. Katoh K, Misawa K, Kuma KI, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30: 3059-3066.
36. Katsir L, Chung HS, Koo AJK, Howe GA (2008) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11: 428-435.
37. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53: 299-328.
38. Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305: 665-668.
39. Kidd S, Melillo A, Lu R-H, Reed D, Kuno N, Uchida K, Furuya M, Jelesko J (2006) The A and B loci in tobacco regulate a network of stress response genes, few of which are associated with nicotine biosynthesis. Plant Mol Biol 60: 699-716.
40. Legg PD, Collins GB (1971) Inheritance of per cent total alkaloids in Nicotiana tabacum L. II. Genetic effects of two loci in Burley 21 × LA Burley 21 populations. Can J Genet Cytol 13: 287-291.
41. Legg PD, Chaplin JF, Collins GB (1969) Inheritance of percent total alkaloids in Nicotiana tabacum L.; populations derived from crosses of low alkaloid lines with burley and flue-cured varieties. J Hered 60: 213-217.
42. Memelink J, Verpoorte R, Kijne JW (2001) ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6: 212-219.
43. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta Gene Reg Mech 1819: 86-96.
44. Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell-line as the Hela-cell in the cell biology of higher plants. Int Rev Cytol Surv Cell Biol 132: 1-30.
45. Nakano T, Nishiuchi T, Suzuki K, Fujimura T, Shinshi H (2006) Studies on transcriptional regulation of endogenous genes by ERF2 transcription factor in tobacco cells. Plant Cell Physiol 47: 554-558.
46. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA-binding proteins that interact with an ethylene-responsive element. Plant Cell 7: 173-182.
47. Onate-Sanchez L, Anderson JP, Young J, Singh KB (2007) AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiol 143: 400-409.
48. Pauw B, Memelink J (2004) Jasmonate-responsive gene expression. J Plant Growth Regul 23: 200-210.
49. Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23: 3089-3100.
50. Pauwels L et al (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464: 788-791.
51. Penninckx I, Thomma B, Buchala A, Metraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103-2113.
52. Rao MV, Lee HI, Creelman RA, Mullet JE, Davis KR (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12: 1633-1646.
53. Reed DG, Jelesko JG (2004) The A and B loci of Nicotiana tabacum have non-equivalent effects on the mRNA levels of four alkaloid biosynthetic genes. Plant Sci 167: 1123-1130.
54. Reinbothe S, Reinbothe C, Parthier B (1993) Methyl jasmonate-regulated translation of nuclear-encoded chloroplast proteins in barley (Hordeum vulgare L. cv. salome). J Biol Chem 268: 10606-10611.
55. Reinbothe C, Springer A, Samol I, Reinbothe S (2009) Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J 276: 4666-4681.
56. Riechers DE, Timko MP (1999) Structure and expression of the gene family encoding putrescine N-methyltransferase in Nicotiana tabacum: new clues to the evolutionary origin of cultivated tobacco. Plant Mol Biol 41: 387-401.
57. Rushton PJ, Reinstadler A, Lipka V, Lippok B, Somssich IE (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell 14: 749-762.
58. Rushton P, Bokowiec M, Laudeman T, Brannock J, Chen X, Timko M (2008a) TOBFAC: the database of tobacco transcription factors. BMC Bioinformatics 9: 53.
59. Rushton PJ, Bokowiec MT, Han S, Zhang H, Brannock JF, Chen X, Laudeman TW, Timko MP (2008b) Tobacco transcription factors: novel insights into transcriptional regulation in the Solanaceae. Plant Physiol 147: 280-295.
60. Ryan SM, Cane KA, DeBoer KD, Sinclair SJ, Brimblecombe R, Hamill JD (2012) Structure and expression of the quinolinate phosphoribosyltransferase (QPT) gene family in Nicotiana. Plant Sci 188-189: 102-110.
61. Sachan N, Falcone DL (2002) Wound-induced gene expression of putrescine N-methyltransferase in leaves of Nicotiana tabacum. Phytochemistry 61: 797-805.
62. Saitoh F, Noma M, Kawashima N (1985) The alkaloid contents of sixty Nicotiana species. Phytochemistry 24: 477-480.
63. Saunders JW, Bush LP (1979) Nicotine biosynthetic enzyme activities in Nicotiana tabacum L. genotypes with different alkaloid levels. Plant Physiol 64: 236-240.
64. Sheard LB et al (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468: 400-405.
65. Shoji T, Hashimoto T (2008) Why does anatabine, but not nicotine, accumulate in jasmonate-elicited cultured tobacco BY-2 cells? Plant Cell Physiol 49: 1209-1216.
66. Shoji T, Hashimoto T (2011a) Recruitment of a duplicated primary metabolism gene into the nicotine biosynthesis regulon in tobacco. Plant J 67: 949-959.
67. Shoji T, Hashimoto T (2011b) Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes directly and by way of the NIC2-locus ERF genes. Plant Cell Physiol 52: 1117-1130.
68. Shoji T, Hashimoto T (2012) DNA-binding and transcriptional activation properties of tobacco NIC2-locus ERF189 and related transcription factors. Plant Biotechnol J 29: 35-42.
69. Shoji T, Yamada Y, Hashimoto T (2000) Jasmonate induction of putrescine N-methyltransferase genes in the root of Nicotiana sylvestris. Plant Cell Physiol 41: 831-839.
70. Shoji T, Ogawa T, Hashimoto T (2008) Jasmonate-induced nicotine formation in tobacco is mediated by tobacco COI1 and JAZ genes. Plant Cell Physiol 49: 1003-1012.
71. Shoji T, Kajikawa M, Hashimoto T (2010) Clustered transcription factor genes regulate nicotine biosynthesis in tobacco. Plant Cell 22: 3390-3409.
72. Sinclair SJ, Murphy KJ, Birch CD, Hamill JD (2000) Molecular characterization of quinolinate phosphoribosyltransferase (QPRTase) in Nicotiana. Plant Mol Biol 44: 603-617.
73. Sisson VA, Severson RF (1990) Alkaloid composition of the Nicotiana species. Beiträge zur Tabakforschung International 14: 327-339.
74. Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20: 1984-2000.
75. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
76. Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13: 66-71.
77. Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine's defensive function in nature. PLoS Biol 2: 1074-1080.
78. Subramanian C, Woo J, Cai X, Xu X, Servick S, Johnson CH, Nebenfuhr A, von Arnim AG (2006) A suite of tools and application notes for in vivo protein interaction assays using bioluminescence resonance energy transfer (BRET). Plant J 48: 138-152.
79. Thines B et al (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448: U661-U662.
80. Thurston R, Smith WT, Cooper BP (1966) Alkaloid secretion by trichomes of Nicotiana species and resistance to aphids. Entomol Exp Appl 9: 428-432.
81. Todd AT, Liu E, Polvi SL, Pammett RT, Page JE (2010) A functional genomics screen identifies diverse transcription factors that regulate alkaloid biosynthesis in Nicotiana benthamiana. Plant J 62: 589-600.
82. van der Fits L, Memelink J (2001) The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 25: 43-53.
83. Vanlerberghe GC, McIntosh L (1994) Mitochondrial electron transport regulation of nuclear gene expression (studies with the alternative oxidase gene of tobacco). Plant Physiol 105: 867-874.
84. Vidal G, Ribas-Carbo M, Garmier M, Dubertret G, Rasmusson AG, Mathieu C, Foyer CH, De Paepe R (2007) Lack of respiratory chain complex I impairs alternative oxidase engagement and modulates redox signaling during elicitor-induced cell death in tobacco. Plant Cell 19: 640-655.
85. Voelckel C, Krugel T, Gase K, Heidrich N, van Dam NM, Winz R, Baldwin IT (2001) Anti-sense expression of putrescine N-methyltransferase confirms defensive role of nicotine in Nicotiana sylvestris against Manduca sexta. Chemoecology 11: 121-126.
86. Vom Endt D, Soares e Silva M, Kijne JW, Pasquali G and Memelink J (2007) Identification of a bipartite jasmonate-responsive promoter element in the periwinkle ORCA3 transcription factor gene which interacts specifically with AT-hook DNA-binding proteins. Plant Physiol pp. 107. 096115.
87. Weber H, Vick BA, Farmer EE (1997) Dinor-oxo-phytodienoic acid: a new hexadecanoid signal in the jasmonate family. Proc Natl Acad Sci USA 94: 10473-10478.
88. Wink M, Schmeller T, Latz-Bruning B (1998) Modes of action of allelochemical alkaloids: interaction with neuroreceptors, DNA, and other molecular targets. J Chem Ecol 24: 1881-1937.
89. Wu M, Chatterji S, Eisen JA (2012) Accounting for alignment uncertainty in phylogenomics. PLoS ONE 7: e30288. doi: 30210. 31371/journal. pone. 0030288.
90. Xu BF, Timko MP (2004) Methyl jasmonate induced expression of the tobacco putrescine N-methyltransferase genes requires both G-box and GCC-motif elements. Plant Mol Biol 55: 743-761.
91. Xu B, Sheehan MJ, Timko MP (2004) Differential induction of ornithine decarboxylase (ODC) gene family members in transgenic tobacco (Nicotiana tabacum L. cv. Bright Yellow 2) cell suspensions by methyl-jasmonate treatment. J Plant Growth Regul 44: 101-116.
92. Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60: 3781-3796.
93. Zhang H, Hedhili S, Montiel G, Zhang Y, Chatel G, Pré M, Gantet P, Memelink J (2011) The basic helix-loop-helix transcription factor CrMYC2 controls the jasmonate-responsive expression of the ORCA genes regulating alkaloid biosynthesis in Catharanthus roseus. Plant J 52: 578-587.
94. Zhang H, Bokowiec MT, Rushton PJ, Han S, Timko MP (2012) Tobacco transcription factors NtMYC2a and NtMYC2b form nuclear complexes with the NtJAZ1 repressor and regulate multiple jasmonate-inducible steps in nicotine biosynthesis. Mol Plant 5: 73-84.