Elucidation of molecular and hormonal background of early growth cessation and endodormancy induction in two contrasting Populus hybrid cultivars

. 2021 Feb 24 ; 21 (1) : 111. [epub] 20210224

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu srovnávací studie, časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33627081

Grantová podpora
K-111879 National Research Development and Innovation Office 'NKFIH'
K-128575 National Research Development and Innovation Office 'NKFIH'
PD-116564 National Research Development and Innovation Office 'NKFIH'
EFOP-3.6.3 Human Resources Development Operational Programme 'EFOP'
VEKOP-16-2017-00008 Competitive Central Hungary Operational Programme 'VEKOP'

Odkazy

PubMed 33627081
PubMed Central PMC7905644
DOI 10.1186/s12870-021-02828-7
PII: 10.1186/s12870-021-02828-7
Knihovny.cz E-zdroje

BACKGROUND: Over the life cycle of perennial trees, the dormant state enables the avoidance of abiotic stress conditions. The growth cycle can be partitioned into induction, maintenance and release and is controlled by complex interactions between many endogenous and environmental factors. While phytohormones have long been linked with dormancy, there is increasing evidence of regulation by DAM and CBF genes. To reveal whether the expression kinetics of CBFs and their target PtDAM1 is related to growth cessation and endodormancy induction in Populus, two hybrid poplar cultivars were studied which had known differential responses to dormancy inducing conditions. RESULTS: Growth cessation, dormancy status and expression of six PtCBFs and PtDAM1 were analyzed. The 'Okanese' hybrid cultivar ceased growth rapidly, was able to reach endodormancy, and exhibited a significant increase of several PtCBF transcripts in the buds on the 10th day. The 'Walker' cultivar had delayed growth cessation, was unable to enter endodormancy, and showed much lower CBF expression in buds. Expression of PtDAM1 peaked on the 10th day only in the buds of 'Okanese'. In addition, PtDAM1 was not expressed in the leaves of either cultivar while leaf CBFs expression pattern was several fold higher in 'Walker', peaking at day 1. Leaf phytohormones in both cultivars followed similar profiles during growth cessation but differentiated based on cytokinins which were largely reduced, while the Ox-IAA and iP7G increased in 'Okanese' compared to 'Walker'. Surprisingly, ABA concentration was reduced in leaves of both cultivars. However, the metabolic deactivation product of ABA, phaseic acid, exhibited an early peak on the first day in 'Okanese'. CONCLUSIONS: Our results indicate that PtCBFs and PtDAM1 have differential kinetics and spatial localization which may be related to early growth cessation and endodormancy induction under the regime of low night temperature and short photoperiod in poplar. Unlike buds, PtCBFs and PtDAM1 expression levels in leaves were not associated with early growth cessation and dormancy induction under these conditions. Our study provides new evidence that the degradation of auxin and cytokinins in leaves may be an important regulatory point in a CBF-DAM induced endodormancy. Further investigation of other PtDAMs in bud tissue and a study of both growth-inhibiting and the degradation of growth-promoting phytohormones is warranted.

Zobrazit více v PubMed

Smithberg MH, Weiser CJ. Patterns of variation among climatic races of red-osier dogwood. Ecology. 1968;49:495–505. doi: 10.2307/1934116. DOI

Kobayashi KD, Fuchigami LH. Modelling temperature effects in breaking rest in red-osier dogwood (Cornus sericea L.)*. Ann Bot. 1983;52:205–215. doi: 10.1093/oxfordjournals.aob.a086566. DOI

Kramer PJ. Effect of variation in length of day on growth and dormancy of trees. Plant Physiol. 1936;11:127–137. doi: 10.1104/pp.11.1.127. PubMed DOI PMC

Downs R, Borthwick H. Effects of photoperiod on growth of trees. Bot Gaz. 1956;117:310–326. doi: 10.1086/335918. DOI

Nitsch J. Photoperiodism in woody plants. Am Soc Hortic Sci. 1957;70:526–544.

Weiser CJ. Cold Resistance and Injury in Woody Plants: Knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science. 1970;169:1269–1278. doi: 10.1126/science.169.3952.1269. PubMed DOI

Heide OM. Growth and dormancy in Norway spruce ecotypes (Picea abies) I. interaction of photoperiod and temperature. Physiol Plant. 1974;30:1–12. doi: 10.1111/j.1399-3054.1974.tb04983.x. DOI

Junttila O. Effect of photoperiod and temperature on apical growth cessation in two ecotypes of Salix and Betula. Physiol Plant. 1980;48:347–352. doi: 10.1111/j.1399-3054.1980.tb03266.x. DOI

Tanino KK, Kalcsits L, Silim S, Kendall E, Gray GR. Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol Biol. 2010;73:49–65. doi: 10.1007/s11103-010-9610-y. PubMed DOI

Svendsen E, Wilen R, Stevenson R, Liu R, Tanino KK. A molecular marker associated with low-temperature induction of dormancy in red osier dogwood (Cornus sericea) Tree Physiol. 2007;27:385–397. doi: 10.1093/treephys/27.3.385. PubMed DOI

Olsen JE, Lee Y, Junttila O. Effect of alternating day and night temperature on short day-induced bud set and subsequent bud burst in long days in Norway spruce. Front Plant Sci. 2014:1–11. 10.3389/fpls.2014.00691. PubMed PMC

Strømme CB, Julkunen-Tiitto R, Olsen JE, Nybakken L. High daytime temperature delays autumnal bud formation in Populus tremula under field conditions. Tree Physiol. 2016;37:71–81. doi: 10.1093/treephys/tpw089. PubMed DOI

Kalcsits LA, Silim S, Tanino K. Warm temperature accelerates short photoperiod-induced growth cessation and dormancy induction in hybrid poplar (Populus × spp.) Trees. 2009;23:971–979. doi: 10.1007/s00468-009-0339-7. DOI

Stinziano JR, Way DA. Autumn photosynthetic decline and growth cessation in seedlings of white spruce are decoupled under warming and photoperiod manipulations. Plant Cell Environ. 2017;40:1296–1316. doi: 10.1111/pce.12917. PubMed DOI

Lang GA, Early JD, Martin GC, Darnell RL. Endo-, Para-, and ecodormancy: physiological terminology and classification for dormancy research. HortScience (USA) 1987;22:22371–22377.

Chao WS, Doğramacı M, Horvath DP, Foley ME, Anderson JV. Advances in Plant Dormancy. Cham: Springer International Publishing; 2015. Dormancy Induction and Release in Buds and Seeds; pp. 235–256.

Hänninen H, Tanino K. Tree seasonality in a warming climate. Trends Plant Sci. 2011;16:412–416. doi: 10.1016/j.tplants.2011.05.001. PubMed DOI

Anderson JV, Horvath DP, Chao WS, Foley ME. Dormancy and Resistance in Harsh Environments. 2010. Bud Dormancy in Perennial Plants: A Mechanism for Survival; pp. 69–90.

Campoy JA, Ruiz D, Egea J. Dormancy in temperate fruit trees in a global warming context: a review. Sci Hortic (Amsterdam) 2011;130:357–372. doi: 10.1016/j.scienta.2011.07.011. DOI

Ding J, Nilsson O. Molecular regulation of phenology in trees—because the seasons they are a-changin. Curr Opin Plant Biol. 2016;29:73–79. doi: 10.1016/j.pbi.2015.11.007. PubMed DOI

Singh RK, Svystun T, AlDahmash B, Jönsson AM, Bhalerao RP. Photoperiod- and temperature-mediated control of phenology in trees – a molecular perspective. New Phytol. 2017;213:511–524. doi: 10.1111/nph.14346. PubMed DOI

Maurya JP, Bhalerao RP. Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees: a molecular perspective. Ann Bot. 2017;120:351–360. doi: 10.1093/aob/mcx061. PubMed DOI PMC

Beauvieux R, Wenden B, Dirlewanger E. Bud Dormancy in Perennial Fruit Tree Species: A Pivotal Role for Oxidative Cues. Front Plant Sci. 2018:1–13. 10.3389/fpls.2018.00657. PubMed PMC

Wisniewski M, Nassuth A, Arora R. Cold Hardiness in Trees: A Mini-Review. Front Plant Sci. 2018:1–9. 10.3389/fpls.2018.01394. PubMed PMC

Liu J, Sherif SM. Hormonal Orchestration of Bud Dormancy Cycle in Deciduous Woody Perennials. Front Plant Sci. 2019:1–21. 10.3389/fpls.2019.01136. PubMed PMC

Stockinger EJ, Gilmour SJ, Thomashow MF. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci. 1997;94:1035–1040. doi: 10.1073/pnas.94.3.1035. PubMed DOI PMC

Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, et al. Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low- Temperature-Responsive Gene Expression, Respectively, in Arabidopsis. Plant Cell. 1998:1391–406 http://www.plantcell.org/cgi/content/abstract/10/8/1391. PubMed PMC

Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol. 2006;57:781–803. doi: 10.1146/annurev.arplant.57.032905.105444. PubMed DOI

Zhao C, Lang Z, Zhu J-K. Cold responsive gene transcription becomes more complex. Trends Plant Sci. 2015;20:466–468. doi: 10.1016/j.tplants.2015.06.001. PubMed DOI PMC

Wisniewski M, Nassuth A, Teulières C, Marque C, Rowland J, Cao PB, et al. Genomics of cold hardiness in Woody plants. CRC Crit Rev Plant Sci. 2014;33:92–124. doi: 10.1080/07352689.2014.870408. DOI

Wisniewski M, Norelli J, Bassett C, Artlip T, Macarisin D. Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta. 2011;233:971–983. doi: 10.1007/s00425-011-1358-3. PubMed DOI

Wisniewski M, Norelli J, Artlip T. Overexpression of a peach CBF gene in apple: a model for understanding the integration of growth, dormancy, and cold hardiness in woody plants. Front Plant Sci. 2015:1–13. 10.3389/fpls.2015.00085. PubMed PMC

Zhao K, Zhou Y, Ahmad S, Yong X, Xie X, Han Y, et al. PmCBFs synthetically affect PmDAM6 by alternative promoter binding and protein complexes towards the dormancy of bud for Prunus mume. Sci Rep. 2018;8:4527. doi: 10.1038/s41598-018-22537-w. PubMed DOI PMC

Zhao K, Zhou Y, Li Y, Zhuo X, Ahmad S, Han Y, et al. Crosstalk of PmCBFs and PmDAMs based on the changes of Phytohormones under seasonal cold stress in the stem of Prunus mume. Int J Mol Sci. 2018;19:15. doi: 10.3390/ijms19020015. PubMed DOI PMC

Benedict C, Skinner JS, Meng R, Chang Y, Bhalerao R, Huner NPA, et al. The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ. 2006;29:1259–1272. doi: 10.1111/j.1365-3040.2006.01505.x. PubMed DOI

Zhang Z, Zhuo X, Zhao K, Zheng T, Han Y, Yuan C, et al. Transcriptome profiles reveal the crucial roles of hormone and sugar in the bud dormancy of Prunus mume. Sci Rep. 2018;8:5090. doi: 10.1038/s41598-018-23108-9. PubMed DOI PMC

Li J, Yan X, Yang Q, Ma Y, Yang B, Tian J, et al. PpCBFs selectively regulate PpDAMs and contribute to the pear bud endodormancy process. Plant Mol Biol. 2019;99:575–586. doi: 10.1007/s11103-019-00837-7. PubMed DOI

Niu Q, Li J, Cai D, Qian M, Jia H, Bai S, et al. Dormancy-associated MADS-box genes and microRNAs jointly control dormancy transition in pear (Pyrus pyrifolia white pear group) flower bud. J Exp Bot. 2016;67:239–257. doi: 10.1093/jxb/erv454. PubMed DOI PMC

Horvath D. Common mechanisms regulate flowering and dormancy. Plant Sci. 2009;177:523–531. doi: 10.1016/j.plantsci.2009.09.002. DOI

Rodriguez AJ, Sherman WB, Scorza R, Wisniewski M, Okie WR. “Evergreen” peach, its inheritance and dormant behavior. J Am Soc Hortic Sci. 1994;119:789–792. doi: 10.21273/JASHS.119.4.789. DOI

Bielenberg DG, Wang Y, Fan S, Reighard GL, Scorza R, Abbott AG. A deletion affecting several gene candidates is present in the Evergrowing peach mutant. J Hered. 2004;95:436–444. doi: 10.1093/jhered/esh057. PubMed DOI

Bielenberg DG, Eileen WY, Li Z, Zhebentyayeva T, Fan S, Reighard GL, et al. Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes. 2008;4:495–507. doi: 10.1007/s11295-007-0126-9. DOI

Horvath DP. Advances in plant dormancy. Cham: Springer International Publishing; 2015. Dormancy-associated MADS-BOX genes: a review; pp. 137–146.

da Silveira Falavigna V, Guitton B, Costes E, Andrés F. I Want to (Bud) Break Free: The Potential Role of DAM and SVP-Like Genes in Regulating Dormancy Cycle in Temperate Fruit Trees. Front Plant Sci. 2019:1–17. 10.3389/fpls.2018.01990. PubMed PMC

Li Z, Reighard GL, Abbott AG, Bielenberg DG. Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot. 2009;60:3521–3530. doi: 10.1093/jxb/erp195. PubMed DOI PMC

Jiménez S, Li Z, Reighard GL, Bielenberg DG. Identification of genes associated with growth cessation and bud dormancy entrance using a dormancy-incapable tree mutant. BMC Plant Biol. 2010;10:25. doi: 10.1186/1471-2229-10-25. PubMed DOI PMC

Sasaki R, Yamane H, Ooka T, Jotatsu H, Kitamura Y, Akagi T, et al. Functional and expressional analyses of PmDAM genes associated with endodormancy in Japanese apricot. Plant Physiol. 2011;157:485–497. doi: 10.1104/pp.111.181982. PubMed DOI PMC

Mimida N, Saito T, Moriguchi T, Suzuki A, Komori S, Wada M. Expression of DORMANCY-ASSOCIATED MADS-BOX (DAM)-like genes in apple. Biol Plant. 2015;59:237–244. doi: 10.1007/s10535-015-0503-4. DOI

Ubi BE, Sakamoto D, Ban Y, Shimada T, Ito A, Nakajima I, et al. Molecular cloning of dormancy-associated MADS-box gene homologs and their characterization during seasonal endodormancy transitional phases of Japanese pear. J Am Soc Hortic Sci. 2010;135:174–182. doi: 10.21273/JASHS.135.2.174. DOI

Saito T, Bai S, Ito A, Sakamoto D, Saito T, Ubi BE, et al. Expression and genomic structure of the dormancy-associated MADS box genes MADS13 in Japanese pears (Pyrus pyrifolia Nakai) that differ in their chilling requirement for endodormancy release. Tree Physiol. 2013;33:654–667. doi: 10.1093/treephys/tpt037. PubMed DOI

Chen K-Y. Type II MADS-BOX genes associated with poplar apical bud development and dormancy: University of Maryland; 2008. https://drum.lib.umd.edu/handle/1903/8152

Horvath DP, Sung S, Kim D, Chao W, Anderson J. Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge. Plant Mol Biol. 2010;73:169–179. doi: 10.1007/s11103-009-9596-5. PubMed DOI

Howe GT, Horvath DP, Dharmawardhana P, Priest HD, Mockler TC, Strauss SH. Extensive Transcriptome changes during natural onset and release of vegetative bud dormancy in Populus. Front Plant Sci. 2015;6:1–28. doi: 10.3389/fpls.2015.00989. PubMed DOI PMC

Balogh E, Halász J, Soltész A, Erös-Honti Z, Gutermuth Á, Szalay L, et al. Identification, Structural and Functional Characterization of Dormancy Regulator Genes in Apricot (Prunus armeniaca L.). Front Plant Sci. 2019:1–16. 10.3389/fpls.2019.00402. PubMed PMC

Horvath DP, Kudrna D, Talag J, Anderson JV, Chao WS, Wing R, et al. BAC Library Development and Clone Characterization for Dormancy-Responsive DREB4A , DAM , and FT from Leafy Spurge (Euphorbia esula) Identifies Differential Splicing and Conserved Promoter Motifs. Weed Sci. 2013;61:303–309. doi: 10.1614/WS-D-12-00175.1. DOI

Saito T, Bai S, Imai T, Ito A, Nakajima I, Moriguchi T. Histone modification and signalling cascade of the dormancy-associatedMADS-box gene, PpMADS13-1, in Japanese pear (Pyrus pyrifolia) during endodormancy. Plant Cell Environ. 2015;38:1157–1166. doi: 10.1111/pce.12469. PubMed DOI

Perry TO. Dormancy of Trees in Winter. Science. 1971;171:29–36. doi: 10.1126/science.171.3966.29. PubMed DOI

Menon M, Barnes WJ, Olson MS. Population genetics of freeze tolerance among natural populations of Populus balsamifera across the growing season. New Phytol. 2015;207:710–722. doi: 10.1111/nph.13381. PubMed DOI

Urrestarazu J, Muranty H, Denancé C, Leforestier D, Ravon E, Guyader A, et al. Genome-wide association mapping of flowering and ripening periods in apple. Front Plant Sci. 2017;8:1923. doi: 10.3389/fpls.2017.01923. PubMed DOI PMC

Wells CE, Vendramin E, Jimenez Tarodo S, Verde I, Bielenberg DG. A genome-wide analysis of MADS-box genes in peach [Prunus persica (L.) Batsch] BMC Plant Biol. 2015;15:41. doi: 10.1186/s12870-015-0436-2. PubMed DOI PMC

Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, et al. The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) Science. 2006;313:1596–1604. doi: 10.1126/science.1128691. PubMed DOI

Yamane H, Ooka T, Jotatsu H, Hosaka Y, Sasaki R, Tao R. 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. 2011;62:3481–3488. doi: 10.1093/jxb/err028. PubMed DOI PMC

Jiménez S, Reighard GL, Bielenberg DG. Gene expression of DAM5 and DAM6 is suppressed by chilling temperatures and inversely correlated with bud break rate. Plant Mol Biol. 2010;73:157–167. doi: 10.1007/s11103-010-9608-5. PubMed DOI

Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, et al. A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell. 2007;19:2370–2390. doi: 10.1105/tpc.107.052811. PubMed DOI PMC

Chao WS, Foley ME, Horvath DP, Anderson JV. Signals regulating dormancy in vegetative buds. Int J Plant Dev Biol. 2007;1:49–56.

Cooke JEK, Eriksson ME, Junttila O. The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ. 2012;35:1707–1728. doi: 10.1111/j.1365-3040.2012.02552.x. PubMed DOI

Tanino KK. Hormones and Endodormancy induction in Woody plants. J Crop Improv. 2004;10:157–199. doi: 10.1300/J411v10n01_08. DOI

Wingler A. Comparison of signaling interactions determining annual and perennial plant growth in response to low temperature. Front Plant Sci. 2015:1–9. 10.3389/fpls.2014.00794. PubMed PMC

Hemberg T. Growth-inhibiting substances in terminal buds of Fraxinus. Physiol Plant. 1949;2:37–44. doi: 10.1111/j.1399-3054.1949.tb07646.x. DOI

Dennis F, Edgerton L. The relationship between an inhibitor and rest in peach flower buds. Am Soc Hortic Sci. 1961;77:107–116.

Eagles CF, Wareing PE. The role of growth substances in the regulation of bud dormancy. Physiol Plant. 1964;17:697–709. doi: 10.1111/j.1399-3054.1964.tb08196.x. DOI

Olsen JE, Junttila O, Nilsen J, Eriksson ME, Martinussen I, Olsson O, et al. Ectopic expression of oat phytochrome a in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. Plant J. 1997;12:1339–1350. doi: 10.1046/j.1365-313x.1997.12061339.x. DOI

Tylewicz S, Petterle A, Marttila S, Miskolczi P, Azeez A, Singh RK, et al. Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science. 2018;360:212–215. doi: 10.1126/science.aan8576. PubMed DOI

Singh RK, Miskolczi P, Maurya JP, Bhalerao RP. A Tree Ortholog of SHORT VEGETATIVE PHASE Floral Repressor Mediates Photoperiodic Control of Bud Dormancy. Curr Biol. 2019;29:128–133. doi: 10.1016/j.cub.2018.11.006. PubMed DOI

Kosová K, Prášil IT, Vítámvás P, Dobrev P, Motyka V, Floková K, et al. Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol. 2012;169:567–576. doi: 10.1016/j.jplph.2011.12.013. PubMed DOI

Djilianov DL, Dobrev PI, Moyankova DP, Vankova R, Georgieva DT, Gajdošová S, et al. Dynamics of endogenous Phytohormones during desiccation and recovery of the resurrection plant species Haberlea rhodopensis. J Plant Growth Regul. 2013;32:564–574. doi: 10.1007/s00344-013-9323-y. DOI

Hu Y, Jiang L, Wang F, Yu D. Jasmonate regulates the INDUCER OF CBF EXPRESSION–C-REPEAT BINDING FACTOR/DRE BINDING FACTOR1 Cascade and freezing tolerance in Arabidopsis. Plant Cell. 2013;25:2907–2924. doi: 10.1105/tpc.113.112631. PubMed DOI PMC

Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P. The cold-inducible CBF1 factor–dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell. 2008;20:2117–2129. doi: 10.1105/tpc.108.058941. PubMed DOI PMC

Hou X, Lee LYC, Xia K, Yan Y, Yu H. DELLAs modulate Jasmonate signaling via competitive binding to JAZs. Dev Cell. 2010;19:884–894. doi: 10.1016/j.devcel.2010.10.024. PubMed DOI

Um TY, Lee HY, Lee S, Chang SH, Chung PJ, Oh K-B, et al. Jasmonate Zim-Domain Protein 9 Interacts With Slender Rice 1 to Mediate the Antagonistic Interaction Between Jasmonic and Gibberellic Acid Signals in Rice. Front Plant Sci. 2018:1–11. 10.3389/fpls.2018.01866. PubMed PMC

Gondor OK, Szalai G, Kovács V, Janda T, Pál M. Relationship between polyamines and other cold-induced response mechanisms in different cereal species. J Agron Crop Sci. 2016;202:217–230. doi: 10.1111/jac.12144. DOI

Baldwin BD, Bandara MS, Tanino KK. Bud scale maturation in Saskatoon Berry (Amelanchier alnifolia Nutt.) plantlets following in vitro hormonal treatments. Acta Hortic. 2000:203–8. 10.17660/ActaHortic.2000.520.21.

Tuan PA, Bai S, Saito T, Ito A, Moriguchi T. Dormancy-Associated MADS-Box (DAM) and the Abscisic acid pathway regulate pear Endodormancy through a feedback mechanism. Plant Cell Physiol. 2017;58:1378–1390. doi: 10.1093/pcp/pcx074. PubMed DOI

Wu R, Wang T, Warren BAW, Allan AC, Macknight RC, Varkonyi-Gasic E. Kiwifruit SVP2 gene prevents premature budbreak during dormancy. J Exp Bot. 2017;68:1071–1082. doi: 10.1093/jxb/erx014. PubMed DOI PMC

Wu R, Wang T, Warren BAW, Thomson SJ, Allan AC, Macknight RC, et al. Kiwifruit SVP2 controls developmental and drought-stress pathways. Plant Mol Biol. 2018;96:233–244. doi: 10.1007/s11103-017-0688-3. PubMed DOI

Knight H, Zarka DG, Okamoto H, Thomashow MF, Knight MR. Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol. 2004;135:1710–1717. doi: 10.1104/pp.104.043562. PubMed DOI PMC

Singh RK, Maurya JP, Azeez A, Miskolczi P, Tylewicz S, Stojkovič K, et al. A genetic network mediating the control of bud break in hybrid aspen. Nat Commun. 2018;9:4173. 10.1038/s41467-018-06696-y. PubMed PMC

Soltész A, Smedley M, Vashegyi I, Galiba G, Harwood W, Vágújfalvi A. Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance. J Exp Bot. 2013;64:1849–1862. doi: 10.1093/jxb/ert050. PubMed DOI PMC

Heide OM, Prestrud AK. Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol. 2005;25:109–114. doi: 10.1093/treephys/25.1.109. PubMed DOI

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

Perez-Llamas C, Lopez-Bigas N. Gitools: analysis and visualisation of genomic data using interactive heat-maps. PLoS One. 2011;6:e19541. doi: 10.1371/journal.pone.0019541. PubMed DOI PMC

Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Informatics. 2009;23:205–211. doi: 10.1142/9781848165632_0019. PubMed DOI

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Ivanov Dobrev P, Kamínek M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A. 2002;950:21–9. 10.1016/S0021-9673(02)00024-9. PubMed

Dobrev PI, Vankova R. Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. In: Shabala S, Cuin TA, editors. Plant Salt Tolerance. Totowa: Humana Press; 2012. p. 251–61. 10.1007/978-1-61779-986-0_17. PubMed

Svačinova J, Novák O, Plačková L, Lenobel R, Holík J, Strnad M, et al. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods. 2012;8:17. PubMed PMC

Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, et al. Scikit-learn: machine learning in Python. J Mach Learn Res. 2011;12:2825–2830. doi: 10.1145/2786984.2786995. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...