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Lipid droplet-associated gene expression and chromatin remodelling in LIPASE 5′-upstream region from beginning- to mid-endodormant bud in ‘Fuji’ apple

Plant Molecular Biology volume 95, pages 441–449 (2017)Cite this article

Abstract

Key message

We found that lipid accumulation in the meristem region and the expression of MdLIP2A, which appears to be regulated by chromatin remodeling, coincided with endodormancy induction in the ‘Fuji’ apple.

Abstract

In deciduous trees, including apples (Malus × domestica Borkh.), lipid accumulation in the meristem region towards endodormancy induction has been thought to be an important process for the acquisition of cold tolerance. In this study, we conducted histological staining of crude lipids in the meristem region of ‘Fuji’ apples and found that lipid accumulation coincided with endodormancy induction. Since a major component of lipid bodies (triacylglycerol) is esterified fatty acids, we analysed fatty acid-derived volatile compounds and genes encoding fatty acid-modifying enzymes (MdLOX1A and MdHPL2A); the reduction of lipid breakdown also coincided with endodormancy induction. We then characterised the expression patterns of lipid body-regulatory genes MdOLE1 and MdLIP2A during endodormancy induction and found that the expression of MdLIP2A correlated well with lipid accumulation towards endodormancy induction. Based on these results, we conducted chromatin remodelling studies and localized the cis-element in the 5′-upstream region of MdLIP2A to clarify its regulatory mechanism. Finally, we revealed that chromatin was concentrated − 764 to − 862 bp of the 5′-upstream region of MdLIP2A, which harbours the GARE [gibberellin responsive MYB transcription factor binding site] and CArG [MADS-box transcription factor binding site] motifs—meristem development-related protein-binding sites.

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Abbreviations

CArG:

MADS-box transcription factor-binding site

DAM:

Dormancy-associated MADS-box

EF1:

Elongation factor 1

FT:

FLOWERING LOCUS T

GARE:

Gibberellin-responsive MYB transcription factor-binding site

GDR:

Genome Database for Rosaceae

NCBI:

National Center for Biotechnology Information

QTL:

Quantitative trait locus

UBI:

Ubiquitin

References

  • Allard A, Bink MC, Martinez S, Kelner JJ, Legave JM, di Guardo M, di Pierro EA, Laurens F, van de Weg EW, Costes E (2016) Detecting QTLs and putative candidate genes involved in budbreak and flowering time in an apple multiparental population. J Exp Bot 67:2875–2888

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bai S, Tuan PA, Saito T, Honda C, Hatsuyama Y, Ito A, Moriguchi T (2016) Epigenetic regulation of MdMYB1 is associated with paper bagging-induced red pigmentation of apples. Planta 244:573–586

    CAS  Article  PubMed  Google Scholar 

  • Ban Y, Oyama-Okubo N, Honda C, Nakayama M, Moriguchi T (2010) Emitted and endogenous volatiles in ‘Tsugaru’ apple: The mechanism of ester and (E, E)-α-farnesene accumulation. Food Chem 118:272–277

    CAS  Article  Google Scholar 

  • Banfield MJ, Barker JJ, Perry AC, Brady RL (1998) Function from structure? The crystal structure of human phosphatidylethanolamine-binding protein suggests a role in membrane signal transduction. Structure 6:124–1254

    Article  Google Scholar 

  • Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043

    Article  PubMed  Google Scholar 

  • Chapman KD, Dyer JM, Mullen RT (2012) Biogenesis and functions of lipid droplets in plants: Thematic Review Series: Lipid Droplet Synthesis and Metabolism: from Yeast to Man. J Lipid Res 53:215–226

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Cooke JEK, Eriksoon ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 10:1707–1728

    Article  Google Scholar 

  • Faust M, Erez A, Rowland LJ, Wang SY, Norman HA (1997) Bud dormancy in perennial fruit trees: physiological basis for dormancy induction, maintenance and release. HortScience 32:623–629

    Google Scholar 

  • Heide OM (2008) Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species. Sci Hortic 115:309–314

    Article  Google Scholar 

  • Heide OM, Prestrud AK (2005) Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol 25:109–114

    CAS  Article  PubMed  Google Scholar 

  • Henderson DC, Hammond J (2013) CKC: isolation of nucleic acids from a diversity of plants using CTAB and silica columns. Mol Biotechnol 53:109–117

    CAS  Article  PubMed  Google Scholar 

  • Horvath DP, Sung S, Kim D, Chao W, Anderson J (2010) Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge. Plant Mol Biol 73:169–179

    CAS  Article  PubMed  Google Scholar 

  • Hu Y, Zhang L, Zhao L, Li J, He S, Zhou K, Huang M, Jiang L, Li L (2011) Trichostatin A selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize. PLoS ONE 6:e22132

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Huang AH (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Biol 43:177–200

    CAS  Article  Google Scholar 

  • Huang AH (1996) Oleosins and oil bodies in seeds and other organs. Plant Physiol 110:1055

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962

    CAS  Article  PubMed  Google Scholar 

  • Kuroda H, Sagisaka S (1993) Ultrastructural changes in cortical cells of apple (Malus pumila Mill.) associated with cold hardiness. Plant Cell Physiol 34:357–365

    Google Scholar 

  • Lang GA (1987) Dormancy: a new universal terminology. HortScience 22:817–820

    Google Scholar 

  • Leida C, Conesa A, Llácer G, Badenes ML, Ríos G (2012) Histone modifications and expression of DAM6 gene in peach are modulated during bud dormancy release in a cultivar-dependent manner. New Phytol 193:67–80

    CAS  Article  PubMed  Google Scholar 

  • Li Z, Reighard GL, Abbott AG, Bielenberg DG (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Liu D, Norman HA, Stutte GW, Faust M (1991) Lipase activity during endodormancy in leaf buds of apple. J Am Soc Hortic Sci 116:689–692

    CAS  Google Scholar 

  • Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280

    CAS  Article  PubMed  Google Scholar 

  • Mellén M, Ayata P, Dewell S, Kriaucionis S, Heintz N (2012) MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell 151:1417–1430

    Article  PubMed  PubMed Central  Google Scholar 

  • Mimida N, Saito T, Moriguchi T, Suzuki A, Komori S, Wada M (2015) Expression of DORMANCY-ASSOCIATED MADS-BOX (DAM)-like genes in apple. Biol Plantarum 59:237–244

    CAS  Article  Google Scholar 

  • Nakamura Y, Andrés F, Kanehara K, Liu YC, Dörmann P, Coupland G (2014) Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering. Nat Commun 5:3553

    PubMed  PubMed Central  Google Scholar 

  • Nakashima A, von Reuss SH, Tasaka H, Nomura M, Mochizuki S, Iijima Y, Aoki K, Shibata D, Boland M, Takabayashi J, Matsui K (2013) Traumatin-and dinortraumatin-containing galactolipids in arabidopsis their formation in tissue-disrupted leaves as counterparts of green leaf volatiles. J Biol Chem 9:274–280

    Google Scholar 

  • Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Porto DD, Bruneau M, Perini P, Anzanello R, Renou JP, dos Santos HP, Fialho FB, Revers LF (2015) Transcription profiling of the chilling requirement for bud break in apples: a putative role for FLC-like genes. J Exp Bot 66:2659–2672

    CAS  Article  PubMed  Google Scholar 

  • Putterill J, Varkonyi-Gasic E (2016) FT and florigen long-distance flowering control in plants. Curr Opin Plant Biol 33:77–82

    CAS  Article  PubMed  Google Scholar 

  • Rao S, Procko E, Shannon MF (2001) Chromatin remodeling, measured by a novel real-time polymerase chain reaction assay, across the proximal promoter region of the IL-2 gene. J Immunol 167:4494–4503

    CAS  Article  PubMed  Google Scholar 

  • Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjärvi J, van der Schoot C (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1, 3-β-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23:130–146

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ríos G, Leida C, Conejero A, Badenes ML (2014) Epigenetic regulation of bud dormancy events in perennial plants. Front Plant Sci 5:247

    PubMed  PubMed Central  Google Scholar 

  • Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223

    CAS  Article  PubMed  Google Scholar 

  • Saito T, Bai S, Imai T, Ito A, Nakajima I, Moriguchi T (2015) Histone modification and signalling cascade of the dormancy-associated MADS-box gene, PpMADS13-1, in Japanese pear (Pyrus pyrifolia) during endodormancy. Plant Cell Environ 38:1157–1166

    CAS  Article  PubMed  Google Scholar 

  • Sakamoto D, Nakamura Y, Sugiura H, Sugiura T, Asakura T, Yokoyama M, Moriguchi T (2010) Effect of 9-hydroxy-10-oxo-12 (Z), 15 (Z)-octadecadienoic acid (KODA) on endodormancy breaking in flower buds of Japanese pear. HortScience 45:1470–1474

    Google Scholar 

  • Saure MC (1985) Dormancy release in deciduous fruit trees. Hortic Rev 7:239–300

    Google Scholar 

  • Shimada TL, Hara-Nishimura I (2010) Oil-body-membrane proteins and their physiological functions in plants. Biol Pharm Bull 33:360–363

    CAS  Article  PubMed  Google Scholar 

  • Shimada TL, Shimada T, Takahashi H, Fukao Y, Hara-Nishimura I (2008) A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. Plant J 55:798–809

    CAS  Article  PubMed  Google Scholar 

  • Shlyueva D, Stelzer C, Gerlach D, Yáñez-Cuna JO, Rath M, Boryń ŁM, Arnold CD, Stark A (2014) Hormone-responsive enhancer-activity maps reveal predictive motifs, indirect repression, and targeting of closed chromatin. Mol Cell 54:180–192

    CAS  Article  PubMed  Google Scholar 

  • Siloto RM, Findlay K, Lopez-Villalobos A, Yeung EC, Nykiforuk CL, Moloney MM (2006) The accumulation of oleosins determines the size of seed oilbodies in Arabidopsis. Plant Cell 18:1961–1974

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Trelease RN (1984) Biogenesis of glyoxysomes. Annu Rev Plant Biol 35:321–347

    CAS  Article  Google Scholar 

  • Tzen JT, Peng CC, Cheng DJ, Chen EC, Chiu JM (1997) A new method for seed oil body purification and examination of oil body integrity following germination. J Biochem 121:762–768

    CAS  Article  PubMed  Google Scholar 

  • van der Schoot C, Paul LK, Rinne PL (2013) The embryonic shoot: a lifeline through winter. J Exp Bot 65:1699–1712

    Article  PubMed  Google Scholar 

  • van Dyk MM, Soeker MK, Labuschagne IF, Rees DJG (2010) Identification of a major QTL for time of initial vegetative budbreak in apple (Malus × domestica Borkh.). Tree Genet Genomes 6:489–502

    Article  Google Scholar 

  • van der Schoot C, Rinne PLH (2011) Dormancy cycling at the shoot apical meristem: transitioning between self-organization and self-arrest. Plant Sci 180:120–131

    Article  PubMed  Google Scholar 

  • van der Schoot C, Paul LK, Paul SB, Rinne PL (2011) Plant lipid bodies and cell-cell signaling: a new role for an old organelle? Plant Signal Behav 6:1732–1738

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang SY, Faust M (1990) Changes of membrane lipids in apple buds during dormancy and budbreak. J Am Soc Hortic Sci 115:803–808

    CAS  Google Scholar 

  • Yamane H, Ooka T, Jotatsu H, Hosaka Y, Sasaki R, Tao R (2011) Expressional regulation of PpDAM5 and PpDAM6, peach (Prunus persica) dormancy-associated MADS-box genes, by low temperature and dormancy-breaking reagent treatment. J Exp Bot 62:3481–3488

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the Program to Disseminate Tenure Tracking System from the Japanese Ministry of Education, Culture, Sports, Science and Technology, and by a grant from the Chiba University to TS.

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Affiliations

  1. Graduate School of Horticulture, Chiba University, Matsudo, 271-8510, Japan

    Takanori Saito, Shanshan Wang, Katsuya Ohkawa, Hitoshi Ohara, Yukiharu Ogawa & Satoru Kondo

  2. Center for Environment, Health and Field Sciences, Chiba University, Kashiwa-no-ha, 277-0882, Japan

    Hitoshi Ohara

  3. Organization for the Strategic Coordination of Research and Intellectual Properties, Meiji University, Kawasaki, 214-8571, Japan

    Hiromi Ikeura

Authors
  1. Takanori Saito
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  2. Shanshan Wang
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  3. Katsuya Ohkawa
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  4. Hitoshi Ohara
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  5. Hiromi Ikeura
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  6. Yukiharu Ogawa
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  7. Satoru Kondo
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Contributions

TS designed the study and wrote paper, WS and YO performed and supervised the microscopy experiments, respectively, HI performed GC/MS analysis, OK, HO, and SK revised the article and corrected the content.

Corresponding author

Correspondence to Satoru Kondo.

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Saito, T., Wang, S., Ohkawa, K. et al. Lipid droplet-associated gene expression and chromatin remodelling in LIPASE 5′-upstream region from beginning- to mid-endodormant bud in ‘Fuji’ apple. Plant Mol Biol 95, 441–449 (2017). https://doi.org/10.1007/s11103-017-0662-0

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  • DOI: https://doi.org/10.1007/s11103-017-0662-0

Keywords

  • CHART-PCR
  • Chromatin remodelling
  • Endodormancy induction
  • Lipid body