Transcriptome Profiling Identified Multiple Jasmonate ZIM-Domain Proteins Involved in the Regulation of Alkaloid Biosynthesis in Tobacco BY-2 Cells

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• 作者：Yuping Yang (1) (3)
  Jing Guo (1)
  Pengcheng Yan (2)
  Yunshuang Li (1)
  Kun Liu (1)
  Ping Gao (1)
  Heping Zhao (1)
  Yubao Chen (2)
  Yingdian Wang (1)
  Michael P. Timko (3)
  Shengcheng Han (1)
  
  1. Beijing Key Laboratory of Gene Resource and Molecular Development ; College of Life Sciences ; Beijing Normal University ; Beijing ; 100875 ; China
  3. Department of Biology ; University of Virginia ; Charlottesville ; VA ; 22904 ; USA
  2. Department of Computational Biology ; Beijing Computing Center ; Beijing ; 100094 ; China
  
• 关键词：Tobacco (Nicotiana tabacum L. cv. Bright Yellow ; 2) ; Alkaloid ; Jasmonate ZIM ; domain protein ; MeJA ; Putrescine N ; methyltransferase ; Transcriptional regulation
• 刊名：Plant Molecular Biology Reporter
• 出版年：2015
• 出版时间：February 2015
• 年：2015
• 卷：33
• 期：1
• 页码：153-166
• 全文大小：2,184 KB
• 参考文献：1. Baldwin IT (1999) Inducible nicotine production in native Nicotiana as an example of adaptive phenotypic plasticity. J Chem Ecol 25:3鈥?0. doi:10.1023/a:1020880931488 CrossRef
  2. 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鈥?157. doi:10.1007/bf02066250 CrossRef
  3. 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鈥?04. doi:10.1007/s004250050082 CrossRef
  4. 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鈥?20. doi:10.1071/fp04008 CrossRef
  5. Cheng ZW, Sun L, Qi TC, Zhang BS, Peng W, Liu YL, Xie DX (2011) The bHLH transcription factor MYC3 interacts with the jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis. Mol Plant 4:279鈥?88. doi:10.1093/mp/ssq073 CrossRef
  6. Chini A et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666鈥?71. doi:10.1038/nature06006 CrossRef
  7. Chini A, Fonseca S, Chico JM, Fernandez-Calvo P, Solano R (2009) The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins. Plant J 59:77鈥?7. doi:10.1111/j.1365-313X.2009.03852.x CrossRef
  8. Chung HS, Howe GA (2009) A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21:131鈥?45. doi:10.1105/tpc.108.064097 CrossRef
  9. Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis jasmonate ZIM-domain genes in response to wounding and herbivory. Plant Physiol 146:952鈥?64. doi:10.1104/pp. 107.115691 CrossRef
  10. Chung HS, Cooke TF, DePew CL, Patel LC, Ogawa N, Kobayashi Y, Howe GA (2010) Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling. Plant J 63:613鈥?22. doi:10.1111/j.1365-313X.2010.04265.x CrossRef
  11. Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of illumina second-generation sequencing data. BMC Bioinforma 11. Doi:10.1186/1471-2105-11-485
  12. Creelman RA, Tierney ML, Mullet JE (1992) Jasmonic acid methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene-expression. Proc Natl Acad Sci U S A 89:4938鈥?941. doi:10.1073/pnas.89.11.4938 CrossRef
  13. De Boer K, Lye JC, Aitken CD, Su AKK, 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鈥?12. doi:10.1007/s11103-008-9425-2 CrossRef
  14. De Luca V, St Pierre B (2000) The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci 5:168鈥?73. doi:10.1016/s1360-1385(00)01575-2 CrossRef
  15. Doares SH, Syrovets T, Weiler EW, Ryan CA (1995) Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc Natl Acad Sci U S A 92:4095鈥?098. doi:10.1073/pnas.92.10.4095 CrossRef
  16. 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鈥?6. doi:10.1146/annurev.arplant.52.1.29 CrossRef
  17. Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644鈥?52 CrossRef
  18. Gundlach H, Muller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant-cell cultures. Proc Natl Acad Sci U S A 89:2389鈥?393. doi:10.1073/pnas.89.6.2389 CrossRef
  19. Hashimoto T, Yamada Y (1994) Alkaloid biogenesis鈥攎olecular aspects. Annu Rev Plant Physiol Plant Mol Biol 45:257鈥?85. doi:10.1146/annurev.pp. 45.060194.001353 CrossRef
  20. Hibi N, Higashiguchi S, Hashimoto T, Yamada Y (1994) Gene-expression in tobacco low-nicotine mutants. Plant Cell 6:723鈥?35. doi:10.2307/3869875 CrossRef
  21. Hou X, Lee LYC, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19:884鈥?94 CrossRef
  22. Howe GA, Jander G (2008) Plant immunity to insect herbivores. In: Annual review of plant biology, vol 59. Annual Review of Plant Biology. pp 41鈥?6. Doi:10.1146/annurev.arplant.59.032607.092825
  23. Imanishi S et al (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鈥?111. doi:10.1023/a:1006058700949 CrossRef
  24. Kajikawa M, Hirai N, Hashimoto T (2009) A PIP-family protein is required for biosynthesis of tobacco alkaloids. Plant Mol Biol 69:287鈥?98. doi:10.1007/s11103-008-9424-3 CrossRef
  25. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97:2940鈥?945. doi:10.1073/pnas.97.6.2940 CrossRef
  26. Melotto M et al (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1F-box protein. Plant J 55:979鈥?88. doi:10.1111/j.1365-313X.2008.03566.x CrossRef
  27. Oh Y, Baldwin IT, Galis I (2012) NaJAZh regulates a subset of defense responses against herbivores and spontaneous leaf necrosis in Nicotiana attenuata plants. Plant Physiol 159:769鈥?88. doi:10.1104/pp. 112.193771 CrossRef
  28. Pauw B, Memelink J (2004) Jasmonate-responsive gene expression. J Plant Growth Regul 23:200鈥?10 CrossRef
  29. Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089鈥?100. doi:10.1105/tpc.111.089300 CrossRef
  30. Pauwels L et al (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788鈥?91. doi:10.1038/nature08854 CrossRef
  31. 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鈥?01. doi:10.1023/a:1006342018991 CrossRef
  32. Sato F et al (2001) Metabolic engineering of plant alkaloid biosynthesis. Proc Natl Acad Sci U S A 98:367鈥?72. doi:10.1073/pnas.011526398 CrossRef
  33. Sembdner G, Parthier B (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annu Rev Plant Physiol Plant Mol Biol 44:569鈥?89. doi:10.1146/annurev.pp. 44.060193.003033 CrossRef
  34. Seo JS et al (2011) OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65:907鈥?21. doi:10.1111/j.1365-313X.2010.04477.x CrossRef
  35. Sheard LB et al (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400鈥?05. doi:10.1038/nature09430 CrossRef
  36. 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鈥?216. doi:10.1093/pcp/pcn096 CrossRef
  37. Shoji T, Hashimoto T (2011a) Nicotine biosynthesis. In: Plant metabolism and biotechnology. John Wiley & Sons, Ltd, New York, pp 191鈥?16. doi:10.1002/9781119991311.ch7 CrossRef
  38. Shoji T, Hashimoto T (2011b) Recruitment of a duplicated primary metabolism gene into the nicotine biosynthesis regulon in tobacco. Plant J 67:949鈥?59. doi:10.1111/j.1365-313X.2011.04647.x CrossRef
  39. Shoji T, Hashimoto T (2011c) Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes directly and by way of the NIC2-locus ERF genes. Plant Cell Physiol 52:1117鈥?130. doi:10.1093/pcp/pcr063 CrossRef
  40. Shoji T, Hashimoto T (2012) DNA-binding and transcriptional activation properties of tobacco NIC2-locus ERF189 and related transcription factors. Plant Biotechnol 29:35鈥?2. doi:10.5511/plantbiotechnology.11.1216a CrossRef
  41. 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鈥?39. doi:10.1093/pcp/pcd001 CrossRef
  42. 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鈥?012. doi:10.1093/pcp/pcn077 CrossRef
  43. Shoji T, Kajikawa M, Hashimoto T (2010) Clustered transcription factor genes regulate nicotine biosynthesis in tobacco. Plant Cell 22:3390鈥?409. doi:10.1105/tpc.110.078543 CrossRef
  44. Sinclair SJ, Murphy KJ, Birch CD, Hamill JD (2000) Molecular characterization of quinolinate phosphoribosyltransferase (QPRTase) in Nicotiana. Plant Mol Biol 44:603鈥?17. doi:10.1023/a:1026590521318 CrossRef
  45. Song S et al (2011) The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in Arabidopsis. Plant Cell Online 23:1000鈥?013. doi:10.1105/tpc.111.083089 CrossRef
  46. Sun JQ, Jiang HL, Li CY (2011) Systemin/jasmonate-mediated systemic defense signaling in tomato. Mol Plant 4:607鈥?15. doi:10.1093/mp/ssr008 CrossRef
  47. Tang Q-Y, Zhang C-X (2013) Data processing system (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci 20:254鈥?60. doi:10.1111/j.1744-7917.2012.01519.x CrossRef
  48. Thines B et al (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448:661鈥?65. doi:10.1038/nature05960 CrossRef
  49. Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G (2007) The tify family previously known as ZIM. Trends Plant Sci 12:239鈥?44. doi:10.1016/j.tplants.2007.04.004 CrossRef
  50. 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鈥?26. doi:10.1007/pl00001841 CrossRef
  51. Wager A, Browse J (2012) Social network: JAZ protein interactions expand our knowledge of jasmonate signaling. Front Plant Sci 3:41. doi:10.3389/fpls.2012.00041 CrossRef
  52. Wang P, Zeng J, Liang ZF, Miao ZQ, Sun XF, Tang KX (2009) Silencing of PMT expression caused a surge of anatabine accumulation in tobacco. Mol Biol Rep 36:2285鈥?289. doi:10.1007/s11033-009-9446-1 CrossRef
  53. Winz RA, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiol 125:2189鈥?202. doi:10.1104/pp. 125.4.2189 CrossRef
  54. Xie J et al (2004) Biotechnology: a tool for reduced-risk tobacco products. Recent Adv Tob Sci 30:17鈥?7
  55. Yan YX, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, Farmer EE (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19:2470鈥?483. doi:10.1105/tpc.107.050708 CrossRef
  56. Yan JB et al (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220鈥?236. doi:10.1105/tpc.109.065730 CrossRef
  57. Zhang HB, 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鈥?4. doi:10.1093/mp/ssr056 CrossRef
  58. Zhu Z et al (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci 108:12539鈥?2544. doi:10.1073/pnas.1103959108 CrossRef
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Plant Sciences
  Plant Physiology
  
• 出版者：Springer Netherlands
• ISSN：1572-9818

文摘

Jasmonate (JA) zinc-finger expressed in inflorescence meristem (ZIM)-domain (JAZ) proteins are key regulators of the JA response in plants. Transcriptome profiling of tobacco BY-2 cells was used to identify 17 members of the NtJAZ family, which were divided into 12 distinct groups based on their predicted amino acid sequences and conserved domains. Transcript levels of eight of the NtJAZ groups increased rapidly upon JA treatment, whereas the remaining members did not show a significant response. The majority of JA-induced NtJAZs formed homo- and heteromers and interacted with NtMYC2a (but not NtERF189) in yeast two-hybrid assays. NtJAZ1, NtJAZ3b, NtJAZ7 and NtJAZ10 were localised in the nucleus and degraded rapidly via the 26S proteasome pathway following the treatment of BY-2 with MeJA. RNAi-induced silencing of NtJAZ1, NtJAZ3, NtJAZ7a and NtJAZ10 greatly reduced the levels of NtPMT transcripts and specifically decreased the nicotine content in the four RNAi transgenic BY-2 lines. The levels of transcripts encoding other nicotine biosynthesis enzymes, NtERF189 and NtMYC2a, and other NtJAZs exhibited different expression patterns in RNAi lines with or without MeJA treatment. Our results indicate that cross-talk occurs among different NtJAZs and forms a complex transcription regulatory scheme for JA-induced nicotine biosynthesis in tobacco.