Natural variation in monoterpene synthesis in kiwifruit: Transcriptional regulation of terpene synthases by NAC and ETHYLENE-INSENSITIVE3-like transcription factors

Plant Physiology

Volumn 167, Issue 4, 2015, Pages 1243-1258

  Nieuwenhuizen, Niels J ^a,b   Chen, Xiuyin ^a   Wang, Mindy Y ^a   Matich, Adam J ^a   Perez, Ramon Lopez ^a,c   Allan, Andrew C ^a,b   Green, Sol A ^a   Atkinson, Ross G ^a  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINIDIA; ACTINIDIA ARGUTA; ACTINIDIA CHINENSIS; ACTINIDIA DELICIOSA; ARABIDOPSIS; NICOTIANA BENTHAMIANA;

2-C-METHYLERYTHRITOL 4-PHOSPHATE; DEOXYXYLULOSE-5-PHOSPHATE SYNTHASE; ERYTHRITOL; ERYTHRITOL 4-PHOSPHATE; ETHYLENE; ETHYLENE DERIVATIVE; PLANT PROTEIN; SUGAR PHOSPHATE; TERPENE; TERPENE SYNTHASE; TRANSCRIPTION FACTOR; TRANSFERASE;

ACTINIDIA; ANALOGS AND DERIVATIVES; DNA SEQUENCE; ENZYMOLOGY; FRUIT; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT LEAF; PROMOTER REGION; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; TRANSGENIC PLANT;

ACTINIDIA; ALKYL AND ARYL TRANSFERASES; BASE SEQUENCE; ERYTHRITOL; ETHYLENES; FRUIT; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; MONOTERPENES; PHYLOGENY; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SUGAR PHOSPHATES; TRANSCRIPTION FACTORS; TRANSFERASES;

EID: 84926189423     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.254367     Document Type: Article

References (85)

1. Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53: 2039–2055.
2. Atkinson RG, Gunaseelan K, Wang MY, Luo L, Wang T, Norling CL, Johnston SL, Maddumage R, Schröder R, Schaffer RJ (2011) Dissecting the role of climacteric ethylene in kiwifruit (Actinidia chinensis) ripening using a 1-aminocyclopropane-1-carboxylic acid oxidase knockdown line. J Exp Bot 62: 3821–3835.
3. Banerjee A, Wu Y, Banerjee R, Li Y, Yan H, Sharkey TD (2013) Feedback inhibition of deoxy-D-xylulose-5-phosphate synthase regulates the methylerythritol 4-phosphate pathway. J Biol Chem 288: 16926–16936.
4. Barry CS, Llop-Tous MI, Grierson D (2000) The regulation of 1-aminocyclopropane- 1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123: 979–986.
5. Battilana J, Costantini L, Emanuelli F, Sevini F, Segala C, Moser S, Velasco R, Versini G, Stella Grando M (2009) The 1-deoxy-D: -xylulose 5-phosphate synthase gene co-localizes with a major QTL affecting monoterpene content in grapevine. Theor Appl Genet 118: 653–669.
6. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95: 4126–4133.
7. Botella-Pavía P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A, Rodríguez-Concepción M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40: 188–199.
8. Buttery RG, Teranishi R, Ling LC, Flath RA, Stern DJ (1988) Quantitative studies on origins of fresh tomato aroma volatiles. J Agric Food Chem 36: 1247–1250.
9. Cane DE, Kang I (2000) Aristolochene synthase: purification, molecular cloning, high-level expression in Escherichia coli, and characterization of the Aspergillus terreus cyclase. Arch Biochem Biophys 376: 354–364.
10. Carretero-Paulet L, Cairó A, Botella-Pavía P, Besumbes O, Campos N, Boronat A, Rodríguez-Concepción M (2006) Enhanced flux through the methylerythritol 4-phosphate pathway in Arabidopsis plants overexpressing deoxyxylulose 5-phosphate reductoisomerase. Plant Mol Biol 62: 683–695.
11. Chang KN, Zhong S, Weirauch MT, Hon G, Pelizzola M, Li H, Huang SS, Schmitz RJ, Urich MA, Kuo D, et al (2013) Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. eLife 2: e00675.
12. Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66: 212–229.
13. Chung MY, Vrebalov J, Alba R, Lee J, McQuinn R, Chung JD, Klein P, Giovannoni J (2010) A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J 64: 936–947.
14. Cordoba E, Salmi M, León P (2009) Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J Exp Bot 60: 2933–2943.
15. Crowhurst RN, Gleave AP, MacRae EA, Ampomah-Dwamena C, Atkinson RG, Beuning LL, Bulley SM, Chagne D, Marsh KB, Matich AJ, et al (2008) Analysis of expressed sequence tags from Actinidia: applications of a cross species EST database for gene discovery in the areas of flavor, health, color and ripening. BMC Genomics 9: 351.
16. Dong L, Miettinen K, Goedbloed M, Verstappen FW, Voster A, Jongsma MA, Memelink J, van der Krol S, Bouwmeester HJ (2013) Characterization of two geraniol synthases from Valeriana officinalis and Lippia dulcis: similar activity but difference in subcellular localization. Metab Eng 20: 198–211.
17. Duchêne E, Butterlin G, Claudel P, Dumas V, Jaegli N, Merdinoglu D (2009) A grapevine (Vitis vinifera L.) deoxy-D: -xylulose synthase gene colocates with a major quantitative trait loci for terpenol content. Theor Appl Genet 118: 541–552.
18. Dudareva N, Cseke L, Blanc VM, Pichersky E (1996) Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. Plant Cell 8: 1137–1148.
19. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978–984.
20. Enfissi EM, Fraser PD, Lois LM, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol J 3: 17–27.
21. Espley RV, Brendolise C, Chagné D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten HJ, Gardiner SE, Hellens RP, et al (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell 21: 168–183.
22. Estévez JM, Cantero A, Reindl A, Reichler S, León P (2001) 1-Deoxy-Dxylulose- 5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276: 22901–22909.
23. Green SA, Chen X, Matich AJ (2012a) In planta transient expression analysis of monoterpene synthases. Methods Enzymol 515: 43–61.
24. Green SA, Chen X, Nieuwenhuizen NJ, Matich AJ, Wang MY, Bunn BJ, Yauk YK, Atkinson RG (2012b) Identification, functional characterization, and regulation of the enzyme responsible for floral (E)-nerolidol biosynthesis in kiwifruit (Actinidia chinensis). J Exp Bot 63: 1951–1967.
25. Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115: 667–677.
26. Hall DE, Robert JA, Keeling CI, Domanski D, Quesada AL, Jancsik S, Kuzyk MA, Hamberger B, Borchers CH, Bohlmann J (2011) An integrated genomic, proteomic and biochemical analysis of (+)-3-carene biosynthesis in Sitka spruce (Picea sitchensis) genotypes that are resistant or susceptible to white pine weevil. Plant J 65: 936–948.
27. Hao YJ, Song QX, Chen HW, Zou HF, Wei W, Kang XS, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Plant NAC-type transcription factor proteins contain a NARD domain for repression of transcriptional activation. Planta 232: 1033–1043.
28. Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53: 383–397.
29. Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Gleave AP, Laing WA (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1: 13.
30. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24: 2635–2648.
31. Huang S, Ding J, Deng D, Tang W, Sun H, Liu D, Zhang L, Niu X, Zhang X, Meng M, et al (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat Commun 4: 2640.
32. Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A (2009) TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J 60: 1081–1095.
33. Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’Shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signalling. Biochem J 426: 183–196.
34. Jeong J, Park Y, Jung H, Park SH, Kim JK (2009) Rice NAC proteins act as homodimers and heterodimers. Plant Biotechnol Rep 3: 127–134.
35. Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, Fraser PD, Baxter C, Angenent GC, de Maagd RA (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23: 923–941.
36. Keeling CI, Weisshaar S, Lin RPC, Bohlmann J (2008) Functional plasticity of paralogous diterpene synthases involved in conifer defense. Proc Natl Acad Sci USA 105: 1085–1090.
37. Keller RK, Thompson R (1993) Rapid synthesis of isoprenoid diphosphates and their isolation in one step using either thin layer or flash chromatography. J Chromatogr A 645: 161–167.
38. Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20: 482–494.
39. Kou X, Watkins CB, Gan SS (2012) Arabidopsis AtNAP regulates fruit senescence. J Exp Bot 63: 6139–6147.
40. Li Y, Zhu B, Xu W, Zhu H, Chen A, Xie Y, Shao Y, Luo Y (2007) LeERF1 positively modulated ethylene triple response on etiolated seedling, plant development and fruit ripening and softening in tomato. Plant Cell Rep 26: 1999–2008.
41. Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D (2008) A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J 55: 301–310.
42. Lois LM, Rodríguez-Concepción M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose 5-phosphate synthase. Plant J 22: 503–513.
43. MacLeod AJ, Pieris NM (1984) Comparison of the volatile components of some mango cultivars. Phytochemistry 23: 361–366.
44. Mahmoud SS, Croteau RB (2001) Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proc Natl Acad Sci USA 98: 8915–8920.
45. Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38: 948–952.
46. Mansfield MA (1995) Rapid immunodetection on polyvinylidene fluoride membrane blots without blocking. Anal Biochem 229: 140–143.
47. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157: 1568–1579.
48. Matich AJ, Young H, Allen JM, Wang MY, Fielder S, McNeilage MA, MacRae EA (2003) Actinidia arguta: volatile compounds in fruit and flowers. Phytochemistry 63: 285–301.
49. Matthews PD, Wurtzel ET (2000) Metabolic engineering of carotenoid accumulation in Escherichia coli by modulation of the isoprenoid precursor pool with expression of deoxyxylulose phosphate synthase. Appl Microbiol Biotechnol 53: 396–400.
50. Montefiori M, Espley RV, Stevenson D, Cooney J, Datson PM, Saiz A, Atkinson RG, Hellens RP, Allan AC (2011) Identification and characterisation of F3GT1 and F3GGT1, two glycosyltransferases responsible for anthocyanin biosynthesis in red-fleshed kiwifruit (Actinidia chinensis). Plant J 65: 106–118.
51. Moufida S, Marzouk B (2003) Biochemical characterization of blood orange, sweet orange, lemon, bergamot and bitter orange. Phytochemistry 62: 1283–1289.
52. Muñoz-Bertomeu J, Arrillaga I, Ros R, Segura J (2006) Up-regulation of 1-deoxy-D-xylulose-5-phosphate synthase enhances production of essential oils in transgenic spike lavender. Plant Physiol 142: 890–900.
53. Nieuwenhuizen NJ, Beuning LL, Sutherland PW, Sharma NN, Cooney JM, Bieleski LRF, Schröder R, MacRae EA, Atkinson RG (2007) Identification and characterisation of acidic and novel basic forms of actinidin, the highly abundant cysteine protease from kiwifruit. Funct Plant Biol 34: 946–961.
54. Nieuwenhuizen NJ, Green SA, Chen X, Bailleul EJ, Matich AJ, Wang MY, Atkinson RG (2013) Functional genomics reveals that a compact terpene synthase gene family can account for terpene volatile production in apple. Plant Physiol 161: 787–804.
55. O’Maille PE, Malone A, Dellas N, Andes Hess B Jr, Smentek L, Sheehan I, Greenhagen BT, Chappell J, Manning G, Noel JP (2008) Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases. Nat Chem Biol 4: 617–623.
56. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, et al (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10: 239–247.
57. Orlova I, Nagegowda DA, Kish CM, Gutensohn M, Maeda H, Varbanova M, Fridman E, Yamaguchi S, Hanada A, Kamiya Y, et al (2009) The small subunit of snapdragon geranyl diphosphate synthase modifies the chain length specificity of tobacco geranylgeranyl diphosphate synthase in planta. Plant Cell 21: 4002–4017.
58. Phillips MA, León P, Boronat A, Rodríguez-Concepción M (2008) The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci 13: 619–623.
59. Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115: 679–689.
60. Rodríguez A, Alquézar B, Peña L (2013) Fruit aromas in mature fleshy fruits as signals of readiness for predation and seed dispersal. New Phytol 197: 36–48.
61. Rodríguez-Concepción M, Boronat A (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol 130: 1079–1089.
62. Rushton PJ, Bokowiec MT, Han S, Zhang H, Brannock JF, Chen X, Laudeman TW, Timko MP (2008) Tobacco transcription factors: novel insights into transcriptional regulation in the Solanaceae. Plant Physiol 147: 280–295.
63. Rynkiewicz MJ, Cane DE, Christianson DW (2001) Structure of trichodiene synthase from Fusarium sporotrichioides provides mechanistic inferences on the terpene cyclization cascade. Proc Natl Acad Sci USA 98: 13543–13548.
64. Schägger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368–379.
65. Shan W, Kuang JF, Chen L, Xie H, Peng HH, Xiao YY, Li XP, Chen WX, He QG, Chen JY, et al (2012) Molecular characterization of banana NAC transcription factors and their interactions with ethylene signalling component EIL during fruit ripening. J Exp Bot 63: 5171–5187.
66. Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12: 3703–3714.
67. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (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.
68. Triglia T (2000) Inverse PCR (IPCR) for obtaining promoter sequence. Methods Mol Biol 130: 79–83.
69. Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17: 1612–1624.
70. Vrebalov J, Pan IL, Arroyo AJ, McQuinn R, Chung M, Poole M, Rose J, Seymour G, Grandillo S, Giovannoni J, et al (2009) Fleshy fruit expansion and ripening are regulated by the Tomato SHATTERPROOF gene TAGL1. Plant Cell 21: 3041–3062.
71. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296: 343–346.
72. Wang MY, Wohlers M, Chen X, Marsh KB (2011) Changes in volatile production and sensory quality of Actinidia arguta fruit during fruit maturation. In G Costa, AR Ferguson, eds, Proceedings of the VIIth International Symposium on Kiwifruit, Faenza, Italy. Acta Hortic 913: 677–684.
73. Williams DC, McGarvey DJ, Katahira EJ, Croteau R (1998) Truncation of limonene synthase preprotein provides a fully active ‘pseudomature’ form of this monoterpene cyclase and reveals the function of the aminoterminal arginine pair. Biochemistry 37: 12213–12220.
74. Xiao YY, Chen JY, Kuang JF, Shan W, Xie H, Jiang YM, Lu WJ (2013) Banana ethylene response factors are involved in fruit ripening through their interactions with ethylene biosynthesis genes. J Exp Bot 64: 2499–2510.
75. 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.
76. Xu YH, Wang JW, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-d-cadinene synthase-A. Plant Physiol 135: 507–515.
77. Xue GP (2005) A CELD-fusion method for rapid determination of the DNAbinding sequence specificity of novel plant DNA-binding proteins. Plant J 41: 638–649.
78. Yamasaki K, Kigawa T, Inoue M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Tomo Y, Terada T, et al (2005) Solution structure of the major DNA-binding domain of Arabidopsis thaliana ethylene-insensitive3- like3. J Mol Biol 348: 253–264.
79. Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425: 521–525.
80. Yin XR, Allan AC, Chen KS, Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening. Plant Physiol 153: 1280–1292.
81. Yoshikuni Y, Ferrin TE, Keasling JD (2006) Designed divergent evolution of enzyme function. Nature 440: 1078–1082.
82. Zhang K, Gan SS (2012) An abscisic acid-AtNAP transcription factor- SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol 158: 961–969.
83. Zhang Z, Zhang H, Quan R, Wang XC, Huang R (2009) Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol 150: 365–377.
84. Zhu M, Chen G, Zhou S, Tu Y, Wang Y, Dong T, Hu Z (2014) A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol 55: 119–135.
85. Zvi MM, Shklarman E, Masci T, Kalev H, Debener T, Shafir S, Ovadis M, Vainstein A (2012) PAP1 transcription factor enhances production of phenylpropanoid and terpenoid scent compounds in rose flowers. New Phytol 195: 335–345.