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

Depicting how Eucalyptus globulus survives drought: involvement of redox and DNA methylation events

Barbara Correia A , Luis Valledor B , Robert D. Hancock C , Cláudia Jesus A , Joana Amaral A , Mónica Meijón B and Glória Pinto A D
+ Author Affiliations
- Author Affiliations

A Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, 3810-193 Aveiro, Portugal.

B Plant Physiology, Department of Organisms and Systems Biology, University of Oviedo, 33005 Oviedo, Spain.

C Cell and Molecular Sciences, The James Hutton Institute, Invergowrie, DD2 5DA Dundee, UK.

D Corresponding author. Email: gpinto@ua.pt

Functional Plant Biology 43(9) 838-850 https://doi.org/10.1071/FP16064
Submitted: 17 February 2016  Accepted: 27 April 2016   Published: 6 June 2016

Abstract

Eucalyptus globulus Labill. is widely cultivated and used by industry but its productivity is currently restricted by drought events, so research focussing on supporting programs to breed adapted germplasm is needed. In the present work we monitored severity of acute drought stress (7 and 11 days after water withholding) and relief (2 h and 3 days after rewatering) by quantifying several biochemical markers of oxidative stress and DNA methylation patterns in leaves. Water withholding imposed a mild oxidative stress as estimated by redox shifts in the major antioxidant pools and increased lipid peroxidation. At the DNA level, global 5-methylcytosine distribution increased over the dehydration period especially in vascular tissue as estimated by immunolocalisation. Using methylation-sensitive RAPD analysis, which discriminates methylation changes occurring in specific DNA sequences, we found a high number of specific demethylation events also taking place. Immunolocalisation indicated a rapid reduction in global DNA methylation 2 h after rehydration; however, a large number of de novo methylation events were still detected by methylation-sensitive RAPD. These events were associated with decreased lipid peroxidation and high cellular GSH pools relative to unstressed plants. Our results indicate the parallel induction of redox and complex DNA methylation changes occurring during stress imposition and relief.

Additional keywords: antioxidant, ascorbate-glutathione cycle, epigenetics, oxidative stress, recovery, water stress.


References

Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiologia Plantarum 121, 472–480.
Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp.CrossRef | 1:CAS:528:DC%2BD2cXlvFOitbY%3D&md5=8700b9f4fffba5322a9fe2510b53e8a5CAS |

Booth TH (2013) Eucalypt plantations and climate change. Forest Ecology and Management 301, 28–34.
Eucalypt plantations and climate change.CrossRef |

Boyer JS (1968) Relationship of water potential to growth of leaves. Plant Physiology 43, 1056–1062.
Relationship of water potential to growth of leaves.CrossRef | 1:STN:280:DC%2BC3cngvFSltw%3D%3D&md5=bdef7d9cee21b38bb47df2e34cce242aCAS | 16656882PubMed |

Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environmental and Molecular Mutagenesis 49, 61–72.
Epigenetic control of plant stress response.CrossRef | 1:CAS:528:DC%2BD1cXhtlWhsL8%3D&md5=b79791c7392f0c51813def17d3670748CAS | 17948278PubMed |

Boyko A, Blevins T, Yao Y, Golubov A, Bilichak A, Ilnytskyy Y, Hollander J, Meins F, Kovalchuk I (2010) Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS One 5, e9514
Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins.CrossRef | 20209086PubMed |

Bräutigam K, Vining KJ, Lafon-Placette C, Fossdal CG, Mirouze M, Marcos JG, Fluch S, Fraga MF, Guevara M, Abarca D (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecology and Evolution 3, 399–415.
Epigenetic regulation of adaptive responses of forest tree species to the environment.CrossRef | 23467802PubMed |

Causevic A, Gentil M-V, Delaunay A, El-Soud WA, Garcia Z, Pannetier C, Brignolas F, Hagège D, Maury S (2006) Relationship between DNA methylation and histone acetylation levels, cell redox and cell differentiation states in sugarbeet lines. Planta 224, 812–827.
Relationship between DNA methylation and histone acetylation levels, cell redox and cell differentiation states in sugarbeet lines.CrossRef | 1:CAS:528:DC%2BD28XosFWktL8%3D&md5=80e0393661f059b2f4550720c9aa1ceaCAS | 16607556PubMed |

Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology 12, 133–139.
Epigenetic regulation of stress responses in plants.CrossRef | 1:CAS:528:DC%2BD1MXjsVOgtbw%3D&md5=7eb26fb6d4006f44c77f511a191f8b36CAS | 19179104PubMed |

Choi C-S, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Molecular Genetics and Genomics 277, 589–600.
Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants.CrossRef | 1:CAS:528:DC%2BD2sXksVarsbw%3D&md5=e62aed42453fea263372c8917dd83df0CAS | 17273870PubMed |

Considine MJ, Foyer CH (2014) Redox regulation of plant development. Antioxidants & Redox Signalling 21, 1305–1326.
Redox regulation of plant development.CrossRef | 1:CAS:528:DC%2BC2cXhsV2ltrzK&md5=4169740e0fb544b4b1df4356e2f04312CAS |

Correia B, Valledor L, Meijón M, Rodriguez JL, Dias MC, Santos C, Cañal MJ, Rodriguez R, Pinto G (2013) Is the interplay between epigenetic markers related to the acclimation of cork oak plants to high temperatures? PLoS One 8, e53543
Is the interplay between epigenetic markers related to the acclimation of cork oak plants to high temperatures?CrossRef | 1:CAS:528:DC%2BC3sXhsVGmtrY%3D&md5=e88f640725e1981097b184e7f9bc550aCAS | 23326451PubMed |

Correia B, Pintó-Marijuan M, Neves L, Brossa R, Dias MC, Costa A, Castro BB, Araújo C, Santos C, Chaves MM (2014) Water stress and recovery in the performance of two Eucalyptus globulus clones: physiological and biochemical profiles. Physiologia Plantarum 150, 580–592.
Water stress and recovery in the performance of two Eucalyptus globulus clones: physiological and biochemical profiles.CrossRef | 1:CAS:528:DC%2BC2cXktVyqtLs%3D&md5=330fe046817581c4f4e3baa56bd9d824CAS | 24117924PubMed |

Cyr AR, Domann FE (2011) The redox basis of epigenetic modifications: from mechanisms to functional consequences. Antioxidants & Redox Signalling 15, 551–589.
The redox basis of epigenetic modifications: from mechanisms to functional consequences.CrossRef | 1:CAS:528:DC%2BC3MXnslKqu70%3D&md5=b71e85faf5aa2255a08f2bd0a017170aCAS |

Davidson NJ, Reid JB (1989) Response of eucalypt species to drought. Australian Journal of Ecology 14, 139–156.
Response of eucalypt species to drought.CrossRef |

Dietz K-J (2014) Redox regulation of transcription factors in plant stress acclimation and development. Antioxidants & Redox Signalling 21, 1356–1372.
Redox regulation of transcription factors in plant stress acclimation and development.CrossRef | 1:CAS:528:DC%2BC2cXhsV2ltr%2FL&md5=a20cdc92616cb2afc09515506a46d6beCAS |

Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiology 147, 1984–1993.
Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells.CrossRef | 1:CAS:528:DC%2BD1cXhtVSrt7vF&md5=d07b5b9f1232b89aee91032e5864e09eCAS | 18550687PubMed |

Filek M, Keskinen R, Hartikainen H, Szarejko I, Janiak A, Miszalski Z, Golda A (2008) The protective role of selenium in rape seedlings subjected to cadmium stress. Journal of Plant Physiology 165, 833–844.
The protective role of selenium in rape seedlings subjected to cadmium stress.CrossRef | 1:CAS:528:DC%2BD1cXntFaltLk%3D&md5=9e0ca749970b4dd7b0bd9696402ae9c2CAS | 17913288PubMed |

Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants & Redox Signalling 11, 861–905.
Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications.CrossRef | 1:CAS:528:DC%2BD1MXitlWhsr0%3D&md5=61427b96b3326974becfe2c5fa66c476CAS |

Franco R, Schoneveld O, Georgakilas AG, Panayiotidis MI (2008) Oxidative stress, DNA methylation and carcinogenesis. Cancer Letters 266, 6–11.
Oxidative stress, DNA methylation and carcinogenesis.CrossRef | 1:CAS:528:DC%2BD1cXmsFKksrw%3D&md5=843a724dea5e15e52456821666e9a2c7CAS | 18372104PubMed |

Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. The Plant Journal 33, 691–705.
Control of Ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves.CrossRef | 1:CAS:528:DC%2BD3sXislWiurk%3D&md5=a9218e70760f109748cd73df7c57cf93CAS | 12609042PubMed |

Galant A, Preuss ML, Cameron JC, Jez JM (2011) Plant glutathione biosynthesis: diversity in biochemical regulation and reaction products. Frontiers in Plant Science 2, 45
Plant glutathione biosynthesis: diversity in biochemical regulation and reaction products.CrossRef | 22645536PubMed |

Gamboa M, Baltierra F, Leon G, Krauskopf E (2013) Drought and salt tolerance enhancement of transgenic Arabidopsis by overexpression of the vacuolar pyrophosphatase 1 (EVP1) gene from Eucalyptus globulus. Plant Physiology and Biochemistry 73, 99–105.
Drought and salt tolerance enhancement of transgenic Arabidopsis by overexpression of the vacuolar pyrophosphatase 1 (EVP1) gene from Eucalyptus globulus.CrossRef | 1:CAS:528:DC%2BC3sXhvV2qu7zK&md5=8c08abd3febcfdece49919d705755df0CAS | 24080396PubMed |

González RM, Ricardi MM, Iusem ND (2013) Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics 8, 864–872.
Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions.CrossRef | 23807313PubMed |

Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178–D1186.
Phytozome: a comparative platform for green plant genomics.CrossRef | 1:CAS:528:DC%2BC3MXhs12htbjE&md5=ecfe37e12f00b4aaf4f361e191ef246eCAS | 22110026PubMed |

Gourcilleau D, Bogeat-Triboulot M-B, Le Thiec D, Lafon-Placette C, Delaunay A, El-Soud WA, Brignolas F, Maury S (2010) DNA methylation and histone acetylation: genotypic variations in hybrid poplars, impact of water deficit and relationships with productivity. Annals of Forest Science 67, 208
DNA methylation and histone acetylation: genotypic variations in hybrid poplars, impact of water deficit and relationships with productivity.CrossRef |

Granda V, Cuesta C, Alvarez R, Ordas R, Centeno ML, Rodriguez A, Majada JP, Fernandez B, Feito I (2011) Rapid responses of C14 clone of Eucalyptus globulus to root drought stress: Time-course of hormonal and physiological signaling. Journal of Plant Physiology 168, 661–670.
Rapid responses of C14 clone of Eucalyptus globulus to root drought stress: Time-course of hormonal and physiological signaling.CrossRef | 1:CAS:528:DC%2BC3MXjtFGisLc%3D&md5=fb85cd3b4abb4e2f4f71f358c2f1e8d5CAS | 21144618PubMed |

Guangyuan L, Xiaoming W, Biyun C, Gao G, Kun X (2007) Evaluation of genetic and epigenetic modification in rapeseed (Brassica napus) induced by salt stress. Journal of Integrative Plant Biology 49, 1599–1607.
Evaluation of genetic and epigenetic modification in rapeseed (Brassica napus) induced by salt stress.CrossRef |

Gutzat R, Scheid OM (2012) Epigenetic responses to stress: triple defense? Current Opinion in Plant Biology 15, 568–573.
Epigenetic responses to stress: triple defense?CrossRef | 1:CAS:528:DC%2BC38XhtlWksb3P&md5=0564dc1947826e40ed92cf95117c1e5aCAS | 22960026PubMed |

Han S-K, Wagner D (2013) Role of chromatin in water stress responses in plants. Journal of Experimental Botany 65, 2785–2799.
Role of chromatin in water stress responses in plants.CrossRef | 24302754PubMed |

Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604–611.
Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.CrossRef | 1:CAS:528:DyaK1MXhslKisLw%3D&md5=1186ca6d85ae4bd80c52db3c9f00c2bfCAS |

Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends in Plant Science 6, 431–438.
Mechanisms of plant desiccation tolerance.CrossRef | 1:CAS:528:DC%2BD3MXmvF2hurs%3D&md5=fad6a8f9168bb8239713b579b13485c8CAS | 11544133PubMed |

Jesus C, Meijón M, Monteiro P, Correia B, Amaral J, Escandón M, Cañal MJ, Pinto G (2015) Salicylic acid application modulates physiological and hormonal changes in Eucalyptus globulus under water deficit. Environmental and Experimental Botany 118, 56–66.
Salicylic acid application modulates physiological and hormonal changes in Eucalyptus globulus under water deficit.CrossRef | 1:CAS:528:DC%2BC2MXhtVektL3J&md5=9af223177475dcb077888e6e9cc10f18CAS |

Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654–657.
Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis.CrossRef | 1:CAS:528:DyaK1MXislyrtbc%3D&md5=5613e3a62109dd9e3ca8a27780ce127dCAS | 10213690PubMed |

Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Infestation of potato (Solanum tuberosum L.) by the peach-potato aphid (Myzus persicae Sulzer) alters cellular redox status and is influenced by ascorbate. Plant, Cell & Environment 35, 430–440.
Infestation of potato (Solanum tuberosum L.) by the peach-potato aphid (Myzus persicae Sulzer) alters cellular redox status and is influenced by ascorbate.CrossRef | 1:CAS:528:DC%2BC38XjtVKntrY%3D&md5=bef15fc4ef31cfd9767f81b9d82e24e0CAS |

Kovarik A, Koukalova B, Bezde M, Opatrn Z (1997) Hypermethylation of tobacco heterochromatic loci in response to osmotic stress. Theoretical and Applied Genetics 95, 301–306.
Hypermethylation of tobacco heterochromatic loci in response to osmotic stress.CrossRef |

Lawlor D, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell & Environment 25, 275–294.
Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants.CrossRef | 1:CAS:528:DC%2BD38Xhslakur0%3D&md5=31c19dc2e8192524951d716544b1e06dCAS |

Luger E (2003) ‘Eucalypt: introduction as an energy crop.’ (BLT Wieselburg: Wieselburg, Austria)

Meijón M, Valledor L, Santamaría E, Testillano PS, Risueño MC, Rodríguez R, Feito I, Cañal MJ (2009) Epigenetic characterization of the vegetative and floral stages of azalea buds: dynamics of DNA methylation and histone H4 acetylation. Journal of Plant Physiology 166, 1624–1636.
Epigenetic characterization of the vegetative and floral stages of azalea buds: dynamics of DNA methylation and histone H4 acetylation.CrossRef | 19523713PubMed |

Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Current Opinion in Plant Biology 14, 267–274.
Epigenetic contribution to stress adaptation in plants.CrossRef | 1:CAS:528:DC%2BC3MXnt1KmsLw%3D&md5=d381b473e67a367ab02e37121db94ad5CAS | 21450514PubMed |

Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. Journal of Plant Physiology 162, 743–748.
The role of α-tocopherol in plant stress tolerance.CrossRef | 16008098PubMed |

Murshed R, Lopez-Lauri F, Sallanon H (2008) Microplate quantification of enzymes of the plant ascorbate–glutathione cycle. Analytical Biochemistry 383, 320–322.
Microplate quantification of enzymes of the plant ascorbate–glutathione cycle.CrossRef | 1:CAS:528:DC%2BD1cXht12rsrzL&md5=09d95fad2b2035071e47c910bb3f1ef6CAS | 18682244PubMed |

Osório J, Osório ML, Chaves MM, Pereira JS (1998) Effects of water deficits on 13C discrimination and transpiration efficiency of Eucalyptus globulus clones. Functional Plant Biology 25, 645–653.

Pascual J, Cañal MJ, Correia B, Escandon M, Hasbún R, Meijón M, Pinto G, Valledor L (2014) Can epigenetics help forest plans to adapt to climate change? In ‘Epigenetics in plants of agronomic importance: fundamentals and applications’. (Eds R Alvarez-Venegas, C De la Peña, JA Casas-Mollano) pp. 125–146. (Springer: Berlin, Germany)

Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2013) Primed plants do not forget. Environmental and Experimental Botany 94, 46–56.
Primed plants do not forget.CrossRef | 1:CAS:528:DC%2BC3sXht1aqsb3O&md5=e2491f548aff211da72e4a3f004b3554CAS |

Pérez-Pérez JG, Syvertsen JP, Botía P, García-Sánchez F (2007) Leaf water relations and net gas exchange responses of salinized carrizo citrange seedlings during drought stress and recovery. Annals of Botany 100, 335–345.
Leaf water relations and net gas exchange responses of salinized carrizo citrange seedlings during drought stress and recovery.CrossRef | 17575285PubMed |

Piller LE, Glauser G, Kessler F, Besagni C (2014) Role of plastoglobules in metabolite repair in the tocopherol redox cycle. Frontiers in Plant Science 5, 298
Role of plastoglobules in metabolite repair in the tocopherol redox cycle.CrossRef |

Pintó-Marijuan M, Munné-Bosch S (2014) Photo-oxidative stress markers as a measure of abiotic stress-induced leaf senescence: advantages and limitations. Journal of Experimental Botany 65, 3845–3857.
Photo-oxidative stress markers as a measure of abiotic stress-induced leaf senescence: advantages and limitations.CrossRef | 24683180PubMed |

Pita P, Pardos JA (2001) Growth, leaf morphology, water use and tissue water relations of Eucalyptus globulus clones in response to water deficit. Tree Physiology 21, 599–607.
Growth, leaf morphology, water use and tissue water relations of Eucalyptus globulus clones in response to water deficit.CrossRef | 1:STN:280:DC%2BD38%2Fht1KjsA%3D%3D&md5=2caa0fa75ab03a65f5137f8eb431cc66CAS | 11390304PubMed |

Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Analytical Biochemistry 363, 58–69.
A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development.CrossRef | 1:CAS:528:DC%2BD2sXislWksbc%3D&md5=962f8a6e66d6b0866e78b651bd2f2b22CAS | 17288982PubMed |

Rahman I, Marwick J, Kirkham P (2004) Redox modulation of chromatin remodeling: impact on histone acetylation and deacetylation, NF-kB and pro-inflammatory gene expression. Biochemical Pharmacology 68, 1255–1267.
Redox modulation of chromatin remodeling: impact on histone acetylation and deacetylation, NF-kB and pro-inflammatory gene expression.CrossRef | 1:CAS:528:DC%2BD2cXmslOnsLo%3D&md5=0bb370bd25bbf9a58dfabf24b9908c7bCAS | 15313424PubMed |

Raj S, Bräutigam K, Hamanishi ET, Wilkins O, Thomas BR, Schroeder W, Mansfield SD, Plant AL, Campbell MM (2011) Clone history shapes Populus drought responses. Proceedings of the National Academy of Sciences of the United States of America 108, 12521–12526.
Clone history shapes Populus drought responses.CrossRef | 1:CAS:528:DC%2BC3MXpvV2qtbc%3D&md5=ef01ff796743dc6ab222bb6351693098CAS | 21746919PubMed |

Rico L, Ogaya R, Barbeta A, Penuelas J (2014) Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change. Plant Biology 16, 419–427.
Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change.CrossRef | 1:CAS:528:DC%2BC2cXjsFGgtbw%3D&md5=3f0102cbd8e056e0a43acbf938c46192CAS | 23889779PubMed |

Scarpa M, Rigo A, Maiorino M, Ursini F, Gregolin C (1984) Formation of α-tocopherol radical and recycling of α-tocopherol by ascorbate during peroxidation of phosphatidylcholine liposomes: an electron paramagnetic resonance study. Biochimica et Biophysica Acta (BBA) – General Subjects 801, 215–219.
Formation of α-tocopherol radical and recycling of α-tocopherol by ascorbate during peroxidation of phosphatidylcholine liposomes: an electron paramagnetic resonance study.CrossRef | 1:CAS:528:DyaL2cXlvVKmsrc%3D&md5=aab443173364eccc3568b0bc60b2fd2aCAS |

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676–682.
Fiji: an open-source platform for biological-image analysis.CrossRef | 1:CAS:528:DC%2BC38XhtVKnurbJ&md5=060368a7328d919667971be43691ba09CAS | 22743772PubMed |

Shvaleva AL, Silva FCE, Breia E, Jouve J, Hausman JF, Almeida MH, Maroco JP, Rodrigues ML, Pereira JS, Chaves MM (2006) Metabolic responses to water deficit in two Eucalyptus globulus clones with contrasting drought sensitivity. Tree Physiology 26, 239–248.
Metabolic responses to water deficit in two Eucalyptus globulus clones with contrasting drought sensitivity.CrossRef | 1:CAS:528:DC%2BD28XhslWqs78%3D&md5=0e99821b2ef9cea74043eb40636ba682CAS | 16356921PubMed |

Sofo A, Tuzio AC, Dichio B, Xiloyannis C (2005) Influence of water deficit and rewatering on the components of the ascorbate–glutathione cycle in four interspecific Prunus hybrids. Plant Science 169, 403–412.
Influence of water deficit and rewatering on the components of the ascorbate–glutathione cycle in four interspecific Prunus hybrids.CrossRef | 1:CAS:528:DC%2BD2MXlvFaltrw%3D&md5=871f22b523acd967aaeeda2bd730a43fCAS |

Solís M-T, Rodríguez-Serrano M, Meijón M, Cañal M-J, Cifuentes A, Risueño MC, Testillano PS (2012) DNA methylation dynamics and MET1a-like gene expression changes during stress-induced pollen reprogramming to embryogenesis. Journal of Experimental Botany 63, 6431–6444.
DNA methylation dynamics and MET1a-like gene expression changes during stress-induced pollen reprogramming to embryogenesis.CrossRef | 23175669PubMed |

Tan MP (2010) Analysis of DNA methylation of maize in response to osmotic and salt stress based on methylation-sensitive amplified polymorphism. Plant Physiology and Biochemistry 48, 21–26.
Analysis of DNA methylation of maize in response to osmotic and salt stress based on methylation-sensitive amplified polymorphism.CrossRef | 1:CAS:528:DC%2BD1MXhs1Wlu7nN&md5=8cf6e38cdc62e5af63541f197a7ed748CAS | 19889550PubMed |

Testillano PS, Solís MT, Risueño MC (2013) The 5-methyl-deoxy-cytidine (5mdC) localization to reveal in situ the dynamics of DNA methylation chromatin pattern in a variety of plant organ and tissue cells during development. Physiologia Plantarum 149, 104–113.
The 5-methyl-deoxy-cytidine (5mdC) localization to reveal in situ the dynamics of DNA methylation chromatin pattern in a variety of plant organ and tissue cells during development.CrossRef | 1:CAS:528:DC%2BC3sXhsFWrtrfM&md5=0244a8ab842c77af6604c6152a166051CAS | 23193951PubMed |

Valdés AE, Irar S, Majada JP, Rodriguez A, Férnandez B, Pages M (2013) Drought tolerance acquisition in Eucalyptus globulus (Labill.): a research on plant morphology, physiology and proteomics. Journal of Proteomics 79, 263–276.
Drought tolerance acquisition in Eucalyptus globulus (Labill.): a research on plant morphology, physiology and proteomics.CrossRef | 23313219PubMed |

Valledor L, Meijón M, Hasbún R, Jesús Cañal M, Rodríguez R (2010) Variations in DNA methylation, acetylated histone H4, and methylated histone H3 during Pinus radiata needle maturation in relation to the loss of in vitro organogenic capability. Journal of Plant Physiology 167, 351–357.
Variations in DNA methylation, acetylated histone H4, and methylated histone H3 during Pinus radiata needle maturation in relation to the loss of in vitro organogenic capability.CrossRef | 1:CAS:528:DC%2BC3cXltFSksrY%3D&md5=493c3ab7171a5bb2ed8fd75bce893ef1CAS | 19931210PubMed |

Valledor L, Escandón M, Meijón M, Nukarinen E, Cañal MJ, Weckwerth W (2014) A universal protocol for the combined isolation of metabolites, DNA, long RNAs, small RNAs, and proteins from plants and microorganisms. The Plant Journal 79, 173–180.
A universal protocol for the combined isolation of metabolites, DNA, long RNAs, small RNAs, and proteins from plants and microorganisms.CrossRef | 1:CAS:528:DC%2BC2cXhtVahtb3N&md5=0cf565b1f4fe5c43ee50a01dbca1f838CAS | 24804825PubMed |

Valledor L, Pascual J, Meijón M, Escandón M, Cañal MJ (2015) Conserved epigenetic mechanisms could play a key role in regulation of photosynthesis and development-related genes during needle development of Pinus radiata. PLoS One 10, e0126405
Conserved epigenetic mechanisms could play a key role in regulation of photosynthesis and development-related genes during needle development of Pinus radiata.CrossRef | 25965766PubMed |

Villar E, Klopp C, Noirot C, Novaes E, Kirst M, Plomion C, Gion JM (2011) RNA-Seq reveals genotype-specific molecular responses to water deficit in Eucalyptus. BMC Genomics 12, 538
RNA-Seq reveals genotype-specific molecular responses to water deficit in Eucalyptus.CrossRef | 1:CAS:528:DC%2BC3MXhsV2lurjI&md5=f9534b0c3967e83c15f6a8fcfbd5f0dfCAS | 22047139PubMed |

Wang M, Qin L, Xie C, Li W, Yuan J, Kong L, Yu W, Xia G, Liu S (2014) Induced and constitutive DNA methylation in a salinity tolerant wheat introgression line. Plant & Cell Physiology 55, 1354–1365.
Induced and constitutive DNA methylation in a salinity tolerant wheat introgression line.CrossRef | 1:CAS:528:DC%2BC2cXhtFCru7nP&md5=89b2feee8aac77aff5adf7f018e77145CAS |

White D, Beadle C, Worledge D (1996) Leaf water relations of Eucalyptus globulus ssp. globulus and E. nitens: seasonal, drought and species effects. Tree Physiology 16, 469–476.
Leaf water relations of Eucalyptus globulus ssp. globulus and E. nitens: seasonal, drought and species effects.CrossRef | 14871715PubMed |



Rent Article (via Deepdyve) Supplementary MaterialSupplementary Material (57 KB) Export Citation Cited By (1)

View Altmetrics