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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Histone modifications at the grapevine VvOMT3 locus, which encodes an enzyme responsible for methoxypyrazine production in the berry

Juri Battilana A , Jake D. Dunlevy B and Paul K. Boss B C
+ Author Affiliations
- Author Affiliations

A FEM-IASMA Genomics and Biology of Fruit Crop Department, Research and Innovation Centre – Fondazione Edmund Mach. Via E. Mach 1, 38010 – S. Michele all’Adige (TN), Italy.

B CSIRO Agriculture and Food, PMB 2, Glen Osmond, SA 5064, Australia.

C Corresponding author. Email: paul.boss@csiro.au

Functional Plant Biology 44(7) 655-664 https://doi.org/10.1071/FP16434
Submitted: 16 December 2016  Accepted: 16 March 2017   Published: 26 April 2017

Abstract

Some herbaceous characters in wine are attributed to the presence of aroma compounds collectively known as methoxypyrazines (MPs). In grape berries their formation has been hypothesised to start from a reaction of two amino acids or an amino acid and an unknown 1,2-dicarbonyl compound, leading to the formation of hydroxypyrazine, which is then enzymatically methylated to form a MP. The enzyme responsible of the formation of 3-isobutyl-2-methoxypyrazine has been recently identified as VvOMT3 whose regulation is still not understood. The concentration of MPs in grapes is known to be influenced by development, environmental stimuli and most importantly grape variety. In order to investigate the chromatin arrangement of that region a chromatin immunoprecipitation analysis has been performed and putative differences in epigenetic regulation of VvOMT3 spatially between the skin and flesh tissues and also temporally during fruit development have been detected. There are also allelic differences in VvOMT3 histone modifications which are maintained in subsequent generations. This study provides evidence of histone tail modification of the VvOMT3 locus in grapevine, which may play a role in the spatial and developmental regulation of the expression of this gene.

Additional keywords: aroma, chromatin immunoprecipitation, IBMP, transposable element, Vitis vinifera.


References

Akkers RC, van Heeringen SJ, Jacobi UG, Janssen-Megens EM, Francoijs KJ, Stunnenberg HG, Veenstra GJC (2009) A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Developmental Cell 17, 425–434.
A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCiu7zO&md5=6f30d3e996a882a5859570a59516ef01CAS |

Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164–167.
Vernalization requires epigenetic silencing of FLC by histone methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFOnug%3D%3D&md5=2ed3c8f9c6e7ae036a68c050e5455256CAS |

Bayonove C, Cordonnier R, Dubois P (1975) Study of an aromatic characteristic fraction of Cabernet Sauvignon grape variety, identification of 2-methoxy-3-isobutyl-pyrazine. Comptes Rendus Hebdomadaires Des Seances De l’Academie Des Sciences Serie D 281, 75–78.

Benjak A, Boue S, Forneck A, Casacuberta JM (2009) Recent amplification and impact of MITEs on the genome of grapevine (Vitis vinifera L.). Genome Biology and Evolution 1, 75–84.
Recent amplification and impact of MITEs on the genome of grapevine (Vitis vinifera L.).Crossref | GoogleScholarGoogle Scholar |

Bernstein BE, Mikkelsen TS, Xie XH, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315–326.
A bivalent chromatin structure marks key developmental genes in embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1Oqur4%3D&md5=1045f47162f798e025eed3bf67bf3be8CAS |

Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416, 847–850.
Association of dwarfism and floral induction with a grape ‘green revolution’ mutation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFyksbs%3D&md5=21bf927e832a8cfd3c9e8ec0f5c4dc89CAS |

Buttery RG, Seifert RM, Guadagni DG, Ling LC (1969) Characterization of some volatile constituents of bell peppers. Journal of Agricultural and Food Chemistry 17, 1322–1327.
Characterization of some volatile constituents of bell peppers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXhtFCkug%3D%3D&md5=4ccc1d49de838c335952da487de691d1CAS |

Cedar H, Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nature Reviews. Genetics 10, 295–304.
Linking DNA methylation and histone modification: patterns and paradigms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksF2rsL0%3D&md5=b135c10c308fb8559732b27a3090030bCAS |

Cheng TB, Reineccius GA, Bjorklund JA, Leete E (1991) Biosynthesis of 2-methoxy-3-isopropylpyrazine in Pseudomonas perolens. Journal of Agricultural and Food Chemistry 39, 1009–1012.
Biosynthesis of 2-methoxy-3-isopropylpyrazine in Pseudomonas perolens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXit1Gnsrg%3D&md5=720e40294fb1c4f2e0cec8251ed3cfd5CAS |

Dunlevy JD (2011) Identification of O-methyltransferase genes involved in the biosynthesis of 3-alkyl-2-methoxypyrazines in grapevines (Vitis vinifera L.). PhD thesis. School of Biological Sciences, Flinders University, South Australia.

Dunlevy JD, Soole KL, Perkins MV, Dennis EG, Keyzers RA, Kalua CM, Boss PK (2010) Two O-methyltransferases involved in the biosynthesis of methoxypyrazines: grape-derived aroma compounds important to wine flavour. Plant Molecular Biology 74, 77–89.
Two O-methyltransferases involved in the biosynthesis of methoxypyrazines: grape-derived aroma compounds important to wine flavour.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVSmurrJ&md5=fbe6ba07681993ff13939b78bc209765CAS |

Dunlevy JD, Dennis EG, Soole KL, Perkins MV, Davies C, Boss PK (2013a) A methyltransferase essential for the methoxypyrazine-derived flavour of wine. The Plant Journal 75, 606–617.
A methyltransferase essential for the methoxypyrazine-derived flavour of wine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1ChsLrP&md5=37b58fcb3b801f55607957303b0958c8CAS |

Dunlevy JD, Soole KL, Perkins MV, Nicholson EL, Maffei SM, Boss PK (2013b) Determining the methoxypyrazine biosynthesis variables affected by light exposure and crop level in Cabernet Sauvignon. American Journal of Enology and Viticulture 64, 450–458.
Determining the methoxypyrazine biosynthesis variables affected by light exposure and crop level in Cabernet Sauvignon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVyqt7w%3D&md5=077526e8640960013eb69581e3606666CAS |

Fernandez L, Torregrosa L, Segura V, Bouquet A, Martinez-Zapater JM (2010) Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine. The Plant Journal 61, 545–557.
Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivVShur0%3D&md5=347d278f943f4ea5691485376e203b33CAS |

Fernandez L, Chaïb J, Martinez-Zapater JM, Thomas MR, Torregrosa L (2013) Mis-expression of a PISTILLATA-like MADS box gene prevents fruit development in grapevine. The Plant Journal 73, 918–928.
Mis-expression of a PISTILLATA-like MADS box gene prevents fruit development in grapevine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFWrsr8%3D&md5=fb5639b9f15503f656aeaf166201209eCAS |

Guillaumie S, Ilg A, Rety S, Brette M, Trossat-Magnin C, Decroocq S, Leon C, Keime C, Ye T, Baltenweck-Guyot R, Claudel P, Bordenave L, Vanbrabant S, Duchene E, Delrot S, Darriet P, Hugueney P, Gomes E (2013) Genetic analysis of the biosynthesis of 2-methoxy-3-isobutylpyrazine, a major grape-derived aroma compound impacting wine quality. Plant Physiology 162, 604–615.
Genetic analysis of the biosynthesis of 2-methoxy-3-isobutylpyrazine, a major grape-derived aroma compound impacting wine quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXps1Orurc%3D&md5=cfa1ac4cf34f954831cf7f5937ead5f2CAS |

Hashizume K, Samuta T (1999) Grape maturity and light exposure affect berry methoxypyrazine concentration. American Journal of Enology and Viticulture 50, 194–198.

Heard E, Martienssen RA (2014) Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157, 95–109.
Transgenerational epigenetic inheritance: myths and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtVCnurs%3D&md5=f148f62edb9f85d8d1e3d34e2d6ba383CAS |

Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447, 418–424.
Epigenetic inheritance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsFOgs78%3D&md5=33f0372d44c96a8665026eab56f41358CAS |

Holligan D, Zhang XY, Jiang N, Pritham EJ, Wessler SR (2006) The transposable element landscape of the model legume Lotus japonicus. Genetics 174, 2215–2228.
The transposable element landscape of the model legume Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1WgtLw%3D&md5=10d6d2fbc82a1d64a080035c6d713e3bCAS |

Johannes F, Colome-Tatche M (2011) Quantitative epigenetics through epigenomic perturbation of isogenic lines. Genetics 188, 215–227.
Quantitative epigenetics through epigenomic perturbation of isogenic lines.Crossref | GoogleScholarGoogle Scholar |

Johnson LM, Cao X, Jacobsen SE (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Current Biology 12, 1360–1367.
Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsVChs70%3D&md5=6c2be43a36815d8d6daec43f24996790CAS |

Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304, 982
Retrotransposon-induced mutations in grape skin color.Crossref | GoogleScholarGoogle Scholar |

Lacey MJ, Allen MS, Harris RLN, Brown WV (1991) Methoxypyrazines in Sauvignon blanc grapes and wines. American Journal of Enology and Viticulture 42, 103–108.

Lippman Z, Martienssen R (2004) The role of RNA interference in heterochromatic silencing. Nature 431, 364–370.
The role of RNA interference in heterochromatic silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsFahsr4%3D&md5=d93c461833eb859a76061310ff29a469CAS |

Murray KE, Shipton J, Whitfield FB (1970) 2-Methoxypyrazines and flavour of green peas (Pisum sativum). Chemistry & Industry 27, 897–898.

Ricardi MM, Gonzalez RM, Iusem ND (2010) Protocol: fine-tuning of a chromatin immunoprecipitation (ChIP) protocol in tomato. Plant Methods 6, 11
Protocol: fine-tuning of a chromatin immunoprecipitation (ChIP) protocol in tomato.Crossref | GoogleScholarGoogle Scholar |

Ringrose L, Paro R (2004) Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins. Annual Review of Genetics 38, 413–443.
Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlyjsw%3D%3D&md5=632acb295d3b177fcaa8075f47217319CAS |

Robinson AL, Boss PK, Solomon PS, Trengove RD, Heymann H, Ebeler SE (2014) Origins of grape and wine aroma. Part 1. Chemical components and viticultural impacts. American Journal of Enology and Viticulture 65, 1–24.
Origins of grape and wine aroma. Part 1. Chemical components and viticultural impacts.Crossref | GoogleScholarGoogle Scholar |

Rothschild M, Moore BP, Brown WV (1984) Pyrazines as waring odor components in the monach butterfly, Danaus plexippus, and in moths of the genera Zygaena and Amata (Lepidoptera). Biological Journal of the Linnean Society. Linnean Society of London 23, 375–380.
Pyrazines as waring odor components in the monach butterfly, Danaus plexippus, and in moths of the genera Zygaena and Amata (Lepidoptera).Crossref | GoogleScholarGoogle Scholar |

Roux F, Colome-Tatche M, Edelist C, Wardenaar R, Guerche P, Hospital F, Colot V, Jansen RC, Johannes F (2011) Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188, 1015–1017.
Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtF2ntLzP&md5=42a0601e420fbb04e6a4d7139820850bCAS |

Sims RJ, Millhouse S, Chen CF, Lewis BA, Erdjument-Bromage H, Tempst P, Manley JL, Reinberg D (2007) Recognition of trimethylated histone h3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Molecular Cell 28, 665–676.
Recognition of trimethylated histone h3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVGmurvF&md5=e062c8924657910d9bdf9a00202e347bCAS |

Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nature Reviews. Genetics 8, 272–285.
Transposable elements and the epigenetic regulation of the genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXivVGkurw%3D&md5=c3cc9b664fb2e0c8492aac908a7815f4CAS |

van Leeuwen H, Monfort A, Puigdomenech P (2007) Mutator-like elements identified in melon, Arabidopsis and rice contain ULP1 protease domains. Molecular Genetics and Genomics 277, 357–364.
Mutator-like elements identified in melon, Arabidopsis and rice contain ULP1 protease domains.Crossref | GoogleScholarGoogle Scholar |

Walker AR, Lee E, Bogs J, McDavid DAJ, Thomas MR, Robinson SP (2007) White grapes arose through the mutation of two similar and adjacent regulatory genes. The Plant Journal 49, 772–785.
White grapes arose through the mutation of two similar and adjacent regulatory genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1Wrt7c%3D&md5=6ef82bc8d7622bc3de68c3657ef8767bCAS |

Wei G, Wei L, Zhu JF, Zang CZ, Hu-Li J, Yao ZJ, Cui KR, Kanno Y, Roh TY, Watford WT, Schones DE, Peng WQ, Sun HW, Paul WE, O’Shea JJ, Zhao KJ (2009) Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30, 155–167.
Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells.Crossref | GoogleScholarGoogle Scholar |

Weigel D, Colot V (2012) Epialleles in plant evolution. Genome Biology 13, 249
Epialleles in plant evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKjtrvP&md5=7ffd67f4fac0095787284d7778357f2bCAS |

Xu ZN, Yan XH, Maurais S, Fu HH, O’Brien DG, Mottinger J, Dooner HK (2004) Jittery, a Mutator distant relative with a paradoxical mobile behavior: excision without reinsertion. The Plant Cell 16, 1105–1114.
Jittery, a Mutator distant relative with a paradoxical mobile behavior: excision without reinsertion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOqsLg%3D&md5=4adec52ac551e86c1f0d8e85ccbfa5ffCAS |

Xu L, Wang LJ, Liu T, Qlan WQ, Gao Y, An CC (2007) Triton, a novel family of miniature inverted-repeat transposable elements (MITEs) in Trichosanthes kirilowii Maximowicz and its effect on gene regulation. Biochemical and Biophysical Research Communications 364, 668–674.
Triton, a novel family of miniature inverted-repeat transposable elements (MITEs) in Trichosanthes kirilowii Maximowicz and its effect on gene regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Krur3I&md5=461426cb4420df4fc53a3794c05a1a97CAS |

Yang GJ, Lee YH, Jiang YM, Shi XY, Kertbundit S, Hall TC (2005) A two-edged role for the transposable element Kiddo in the rice ubiquitin2 promoter. The Plant Cell 17, 1559–1568.
A two-edged role for the transposable element Kiddo in the rice ubiquitin2 promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKksL4%3D&md5=c71ec24cf0d9a375c2bed865e9dc86b0CAS |