Light on perenniality: Para-dormancy is based on ABA-GA antagonism and endo-dormancy on the shutdown of GA biosynthesis.
1,3-β-glucanase
abscisic acid
branching
callose
gibberellins
plasmodesmata
prolepsis
syllepsis
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
revised:
23
01
2023
received:
30
09
2022
accepted:
07
02
2023
medline:
1
5
2023
pubmed:
11
2
2023
entrez:
10
2
2023
Statut:
ppublish
Résumé
Perennial para- and endo-dormancy are seasonally separate phenomena. Whereas para-dormancy is the suppression of axillary buds (AXBs) by a growing shoot, endo-dormancy is the short-day elicited arrest of terminal and AXBs. In hybrid aspen (Populus tremula x P. tremuloides) compromising the apex releases para-dormancy, whereas endo-dormancy requires chilling. ABA and GA are implicated in both phenomena. To untangle their roles, we blocked ABA biosynthesis with fluridone (FD), which significantly reduced ABA levels, downregulated GA-deactivation genes, upregulated the major GA3ox-biosynthetic genes, and initiated branching. Comprehensive GA-metabolite analyses suggested that FD treatment shifted GA production to the non-13-hydroxylation pathway, enhancing GA
Substances chimiques
Gibberellins
0
Abscisic Acid
72S9A8J5GW
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1785-1804Informations de copyright
© 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.
Références
Alazem, M. & Lin, N.S. (2017) Antiviral roles of abscisic acid in plants. Frontiers in Plant Science, 8, 1760.
Aloni, R. & Peterson, C.A. (1997) Auxin promotes dormancy callose removal from the phloem of Magnolia kobus and callose accumulation and earlywood vessel differentiation in Quercus robur. Journal of Plant Research, 110, 37-44.
Aloni, R., Raviv, A. & Peterson, C.A. (1991) The role of auxin in the removal of dormancy callose and resumption of phloem activity in Vitis vinifera. Canadian Journal of Botany, 69, 1825-1832.
André, D., Marcon, A., Lee, K.C., Goretti, D., Zhang, B., Delhomme, N. et al. (2022) FLOWERING LOCUS T paralogs control the annual growth cycle in Populus trees. Current Biology, 32, 2988-2996.
Antoni, R., Gonzalez-Guzman, M., Rodriguez, L., Rodrigues, A., Pizzio, G.A. & Rodriguez, P.L. (2012) Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiology, 158, 970-980.
Archacki, R., Buszewicz, D., Sarnowski, T.J., Sarnowska, E., Rolicka, A.T., Tohge, T. et al. (2013) BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin-mediated responses in Arabidopsis. PLoS One, 8, e58588.
Arend, M., Schnitzler, J.P., Ehlting, B., Hänsch, R., Lange, T., Rennenberg, H. et al. (2009) Expression of the Arabidopsis mutant abi1 gene alters abscisic acid sensitivity, stomatal development, and growth morphology in gray poplars. Plant Physiology, 151, 2110-2119.
Arora, R., Rowland, L.J. & Tanino, K. (2003) Induction and release of bud dormancy in woody perennials: a science comes of age. HortScience, 38, 911-921.
Asselbergh, B. & Höfte, M. (2007) Basal tomato defences to Botrytis cinerea include abscisic acid-dependent callose formation. Physiological and Molecular Plant Pathology, 71, 33-40.
Bacic, A., Fincher, G. & Stone, B. (2009) Chemistry, biochemistry, and biology of (1-3)-β-glucans and related polysaccharides. New York: Academic Press.
Barreto, L.C., Herken, D.M.D., Silva, B.M.R., Munné-Bosch, S. & Garcia, Q.S. (2020) ABA and GA(4) dynamic modulates secondary dormancy and germination in Syngonanthus verticillatus seeds. Planta, 251, 86.
Barthélémy, D. & Caraglio, Y. (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Annals of Botany, 99, 375-407.
Battey, N.H. & Lyndon, R.F. (1990) Reversion of flowering. The Botanical Review, 56, 162-189.
Bennett, T. & Leyser, O. (2014) Strigolactone signalling: standing on the shoulders of DWARFs. Current Opinion in Plant Biology, 22, 7-13.
Boyd, J., Gai, Y., Nelson, K.M., Lukiwski, E., Talbot, J., Loewen, M.K. et al. (2009) Sesquiterpene-like inhibitors of a 9-cis-epoxycarotenoid dioxygenase regulating abscisic acid biosynthesis in higher plants. Bioorganic & Medicinal Chemistry, 17, 2902-2912.
Brewer, P.B., Koltai, H. & Beveridge, C.A. (2013) Diverse roles of strigolactones in plant development. Molecular Plant, 6, 18-28.
Chan, S.W.L., Henderson, I.R. & Jacobsen, S.E. (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nature Reviews Genetics, 6, 351-360.
Chen, W.X., Tamada, Y., Yamane, H., Matsushita, M., Osako, Y. & Gao-Takai, M. et al. (2022) H3K4me3 plays a key role in establishing permissive chromatin states during bud dormancy and bud break in apple. Plant Journal, 1111, 1015-1031.
Choubane, D., Rabot, A., Mortreau, E., Legourrierec, J., Péron, T., Foucher, F. et al. (2012) Photocontrol of bud burst involves gibberellin biosynthesis in Rosa sp. Journal of Plant Physiology, 169, 1271-1280.
Chow, C.N., Lee, T.Y., Hung, Y.C., Li, G.Z., Tseng, K.C., Liu, Y.H. et al. (2019) PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants. Nucleic Acids Research, 47, D1155-D1163.
Cline, M.G. (1997) Concepts and terminology of apical dominance. American Journal of Botany, 84, 1064-1069.
Cline, M.G. & Oh, C. (2006) A reappraisal of the role of abscisic acid and its interaction with auxin in apical dominance. Annals of Botany, 98, 891-897.
Cooke, J.E.K., Eriksson, M.E. & Junttila, O. (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant, Cell & Environment, 35, 1707-1728.
Costes, E. & Gion, J.M. (2015) Genetics and genomics of tree architecture. In: Adam-Blondon, A. F. & Plomion, C. (Eds.) Land plants - trees. Amsterdam: Elsevier Ltd Academic Press, pp. 157-200.
Doxey, A.C., Yaish, M.W.F., Moffatt, B.A., Griffith, M. & McConkey, B.J. (2007) Functional divergence in the arabidopsis -1,3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Molecular Biology and Evolution, 24, 1045-1055.
Eagles, C.F. & Wareing, P.E. (1964) The role of growth substances in the regulation of bud dormancy. Physiologia Plantarum, 17, 697-709.
Eriksson, M. & Moritz, T. (2002) Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen (Populus tremula L. x P. tremuloides Michx.). Planta, 214, 920-930.
Fang, J., Chai, C., Qian, Q., Li, C., Tang, J., Sun, L. et al. (2008) Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. The Plant Journal, 54, 177-189.
Ferguson, B.J. & Beveridge, C.A. (2009) Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiology, 149, 1929-1944.
Flors, V., Ton, J., Jakab, G. & Mauch-Mani, B. (2005) Abscisic acid and callose: team players in defence against pathogens? Journal of Phytopathology, 153, 377-383.
Frommer, M., McDonald, L.E., Millar, D.S., Collis, C.M., Watt, F., Grigg, G.W. et al. (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proceedings of the National Academy of Sciences, 89, 1827-1831.
Gaaliche, B., Aїachi-Mezghani, M., Trad, M., Costes, E., Lauri, P.E. & Mars, M. (2016) Shoot architecture and morphology of different branch orders in fig tree (Ficus carica L.). International Journal of Fruit Science, 16, 378-394.
García-Andrade, J., Ramírez, V., Flors, V. & Vera, P. (2011) Arabidopsis ocp3 mutant reveals a mechanism linking ABA and JA to pathogen-induced callose deposition. The Plant Journal, 67, 783-794.
Geisler-Lee, J., Geisler, M., Coutinho, P.M., Segerman, B., Nishikubo, N., Takahashi, J. et al. (2006) Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiology, 140, 946-962.
Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pagès, V., Dun, E.A., Pillot, J.P. et al. (2008) Strigolactone inhibition of shoot branching. Nature, 455, 189-194.
Gonzalez-Grandio, E., Pajoro, A., Franco-Zorrilla, J.M., Tarancon, C., Immink, R.G.H. & Cubas, P. (2017) Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds. Proceedings of the National Academy of Sciences of the United States of America, 114, E245-E254.
Graeber, K., Nakabayashi, K., Miatton, E., Leubner-Metzger, G. & Soppe, W.J.J. (2012) Molecular mechanisms of seed dormancy. Plant, Cell & Environment, 35, 1769-1786.
Grappin, P., Bouinot, D., Sotta, B., Miginiac, E. & Jullien, M. (2000) Control of seed dormancy in Nicotiana plumbaginifolia: post-imbibition abscisic acid synthesis imposes dormancy maintenance. Planta, 210, 279-285.
Gruntman, E., Qi, Y., Slotkin, R.K., Roeder, T., Martienssen, R.A. & Sachidanandam, R. (2008) Kismeth: analyzer of plant methylation states through bisulfite sequencing. BMC Bioinformatics, 9, 371.
Guseman, J.M., Lee, J.S., Bogenschutz, N.L., Peterson, K.M., Virata, R.E., Xie, B. et al. (2010) Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis CHORUS (GLUCAN SYNTHASE-LIKE 8). Development, 137, 1731-1741.
Gusta, L.V., Trischuk, R. & Weiser, C.J. (2005) Plant cold acclimation: the role of abscisic acid. Journal of Plant Growth Regulation, 24, 308-318.
Hallé, F., Oldeman, R. & Tomlinson, P. (1978) Tropical trees and forests. An architectural analysis. Berlin, Heidelberg, New York: Springer.
Hanada, K., Hase, T., Toyoda, T., Shinozaki, K. & Okamoto, M. (2011) Origin and evolution of genes related to ABA metabolism and its signaling pathways. Journal of Plant Research, 124, 455-465.
Hansen, E., Olsen, J.E. & Junttila, O. (1999) Gibberellins and subapical cell divisions in relation to bud set and bud break in Salix pentandra. Journal of Plant Growth Regulation, 18, 167-170.
Hayward, A., Stirnberg, P., Beveridge, C. & Leyser, O. (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiology, 151, 400-412.
Hazebroek, J.P., Metzger, J.D. & Mansager, E.R. (1993) Thermoinductive regulation of gibberellin metabolism in Thlaspi arvense L. (II. Cold Induction of Enzymes in Gibberellin Biosynthesis). Plant Physiology, 102, 547-552.
Hedden, P. & Thomas, S.G. (2012) Gibberellin biosynthesis and its regulation. Biochemical Journal, 444, 11-25.
Holalu, S.V., Reddy, S.K., Blackman, B.K. & Finlayson, S.A. (2020) Phytochrome interacting factors 4 and 5 regulate axillary branching via bud abscisic acid and stem auxin signalling. Plant, Cell & Environment, 43, 2224-2238.
Immanen, J., Nieminen, K., Duchens Silva, H., Rodríguez Rojas, F., Meisel, L.A., Silva, H. et al. (2013) Characterization of cytokinin signaling and homeostasis gene families in two hardwood tree species: Populus trichocarpa and Prunus persica. BMC Genomics, 14, 885.
Jamil, M., Charnikhova, T., Verstappen, F. & Bouwmeester, H. (2010) Carotenoid inhibitors reduce strigolactone production and Striga hermonthica infection in rice. Archives of Biochemistry and Biophysics, 504, 123-131.
Junttila, O. & Jensen, E. (1988) Gibberellins and photoperiodic control of shoot elongation in Salix. Physiologia Plantarum, 74, 371-376.
Katyayini, N.U., Rinne, P.L.H. & van der Schoot, C. (2019) Strigolactone-based node-to-bud signaling may restrain shoot branching in hybrid aspen. Plant and Cell Physiology, 60, 2797-2811.
Katyayini, N.U., Rinne, P.L.H., Tarkowská, D., Strnad, M. & van der Schoot, C. (2020) Dual role of gibberellin in perennial shoot branching: inhibition and activation. Frontiers in Plant Science, 11, 736.
Kiyosue, T., Yamaguchishinozaki, K. & Shinozaki, K. (1994) Cloning of cDNAs for genes that are early-responsive to dehydration stress (ERDs) in Arabidopsis thaliana L.: identification of three ERDs as HSP cognate genes. Plant Molecular Biology, 25, 791-798.
Lang, G.A., Early, J.D., Martin, G.C. & Darnell, R.L. (1987) Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. HortScience, 22, 371-377.
Lefebvre, V., North, H., Frey, A., Sotta, B., Seo, M., Okamoto, M. et al. (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. The Plant Journal, 45, 309-319.
Leubner-Metzger, G. (2002) Seed after-ripening and over-expression of class I β-1,3-glucanase confer maternal effects on tobacco testa rupture and dormancy release. Planta, 215, 959-968.
Leung, J. & Giraudat, J. (1998) Abscisic acid signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 199-222.
Levy, A., Erlanger, M., Rosenthal, M. & Epel, B.L. (2007) A plasmodesmata-associated β-1,3-glucanase in Arabidopsis. The Plant Journal, 49, 669-682.
Li, S., Wang, Q., Wen, B., Zhang, R., Jing, X., Xiao, W. et al. (2021) Endodormancy release can be modulated by the GA(4)-GID1c-DELLA2 module in peach leaf buds. Frontiers in Plant Science, 12, 713514.
Lichtenthaler, H.K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350-382.
Lo, S.F., Yang, S.Y., Chen, K.T., Hsing, Y.I., Zeevaart, J.A.D., Chen, L.J. et al. (2008) A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. The Plant Cell, 20, 2603-2618.
López-Ráez, J.A., Kohlen, W., Charnikhova, T., Mulder, P., Undas, A.K., Sergeant, M.J. et al. (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytologist, 187, 343-354.
Lucas, W.J., Ding, B. & van der Schoot, C. (1993) Plasmodesmata and the supracellular nature of plants. New Phytologist, 125, 435-476.
Martínez-Bello, L., Moritz, T. & López-Díaz, I. (2015) Silencing C19-GA 2-oxidases induces parthenocarpic development and inhibits lateral branching in tomato plants. Journal of Experimental Botany, 66, 5897-5910.
Mason, M.G., Ross, J.J., Babst, B.A., Wienclaw, B.N. & Beveridge, C.A. (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proceedings of the National Academy of Sciences, 111, 6092-6097.
Mauch-Mani, B. & Mauch, F. (2005) The role of abscisic acid in plant-pathogen interactions. Current Opinion in Plant Biology, 8, 409-414.
Mauriat, M., Sandberg, L.G. & Moritz, T. (2011) Proper gibberellin localization in vascular tissue is required to control auxin-dependent leaf development and bud outgrowth in hybrid aspen. The Plant Journal, 67, 805-816.
Middleton, A.M., Úbeda-Tomás, S., Griffiths, J., Holman, T., Hedden, P., Thomas, S.G. et al. (2012) Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling. Proceedings of the National Academy of Sciences, 109, 7571-7576.
Muhr, M., Prüfer, N., Paulat, M. & Teichmann, T. (2016) Knockdown of strigolactone biosynthesis genes in Populus affects BRANCHED1 expression and shoot architecture. New Phytologist, 212, 613-626.
Müller, D. & Leyser, O. (2011) Auxin, cytokinin and the control of shoot branching. Annals of Botany, 107, 1203-1212.
Mutasa-Gottgens, E. & Hedden, P. (2009) Gibberellin as a factor in floral regulatory networks. Journal of Experimental Botany, 60, 1979-1989.
Nambara, E. & Marion-Poll, A. (2005) Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology, 56, 165-185.
Ni, J., Gao, C., Chen, M.S., Pan, B.Z., Ye, K. & Xu, Z.F. (2015) Gibberellin promotes shoot branching in the perennial woody plant Jatropha curcas. Plant and Cell Physiology, 56, 1655-1666.
Ni, J., Zhao, M.L., Chen, M.S., Pan, B.Z., Tao, Y.B. & Xu, Z.F. (2017) Comparative transcriptome analysis of axillary buds in response to the shoot branching regulators gibberellin A3 and 6-benzyladenine in Jatropha curcas. Scientific Reports, 7, 11417.
Okada, K., Wada, M., Takebayashi, Y., Kojima, M., Sakakibara, H., Nakayasu, M. et al. (2020) Columnar growth phenotype in apple results from gibberellin deficiency by ectopic expression of a dioxygenase gene. Tree Physiology, 40, 1205-1216.
Or, E., Belausov, E., Popilevsky, I. & Ben Tal, Y. (2000) Changes in endogenous ABA level in relation to the dormancy cycle in grapevines grown in a hot climate. Journal of Horticultural Science & Biotechnology, 75, 190-194.
Osnato, M., Castillejo, C., Matías-Hernández, L. & Pelaz, S. (2012) TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis. Nature Communications, 3, 808.
Paul, L.K., Rinne, P.L.H. & van der Schoot, C. (2014a) Shoot meristems of deciduous woody perennials: self-organization and morphogenetic transitions. Current Opinion in Plant Biology, 17, 86-95.
Paul, L.K., Rinne, P.L.H. & van der Schoot, C. (2014b) Refurbishing the plasmodesmal chamber: a role for lipid bodies? Frontiers in Plant Science, 5, 40.
Phillips, I.D.J. (1975) Apical dominance. Annual Review of Plant Physiology, 26, 341-367.
Rameau, C., Bertheloot, J., Leduc, N., Andrieu, B., Foucher, F. & Sakr, S. (2015) Multiple pathways regulate shoot branching. Frontiers in Plant Science, 5, 15.
Rinne, P., Welling, A. & Kaikuranta, P. (1998) Onset of freezing tolerance in birch (Betula pubescens Ehrh.) involves LEA proteins and osmoregulation and is impaired in an ABA-deficient genotype. Plant, Cell and Environment, 21, 601-611.
Rinne, P.L.H., Kaikuranta, P.M. & van der Schoot, C. (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. The Plant Journal, 26, 249-264.
Rinne, P.L.H., Paul, L.K. & van der Schoot, C. (2018) Decoupling photo- and thermoperiod by projected climate change perturbs bud development, dormancy establishment and vernalization in the model tree Populus. BMC Plant Biology, 18, 220.
Rinne, P.L.H., Paul, L.K., Vahala, J., Kangasjärvi, J. & van der Schoot, C. (2016) Axillary buds are dwarfed shoots that tightly regulate GA pathway and GA-inducible 1,3-β-glucanase genes during branching in hybrid aspen. Journal of Experimental Botany, 67, 5975-5991.
Rinne, P.L.H., Paul, L.K., Vahala, J., Ruonala, R., Kangasjärvi, J. & van der Schoot, C. (2015) Long and short photoperiod buds in hybrid aspen share structural development and expression patterns of marker genes. Journal of Experimental Botany, 66, 6745-6760.
Rinne, P.L.H. & van der Schoot, C. (2004) Cell-cell communication as a key factor in dormancy cycling. Journal of Crop Improvement, 10, 113-156.
Rinne, P.L.H., Welling, A., Vahala, J., Ripel, L., Ruonala, R., Kangasjärvi, J. et al. (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. The Plant Cell, 23, 130-146.
Rohde, A., Prinsen, E., De Rycke, R., Engler, G., Van Montagu, M. & Boerjan, W. (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. The Plant Cell, 14, 1885-1901.
Rubio, S., Noriega, X. & Pérez, F.J. (2019) ABA promotes starch synthesis and storage metabolism in dormant grapevine buds. Journal of Plant Physiology, 234-235, 1-8.
Ruonala, R., Rinne, L.H., Kangasjärvi, J. & van der Schoot, C. (2008) CENL1 expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. The Plant Cell, 20, 59-74.
Ruttink, T., Arend, M., Morreel, K., Storme, V., Rombauts, S., Fromm, J. et al. (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. The Plant Cell, 19, 2370-2390.
Saure, M.C. (1985) Dormancy release in deciduous fruit trees. Horticultural Reviews, 7, 239-300.
Seo, M., Hanada, A., Kuwahara, A., Endo, A., Okamoto, M., Yamauchi, Y. et al. (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. The Plant Journal, 48, 354-366.
Shimada, T.L., Hayashi, M. & Hara-Nishimura, I. (2018) Membrane dynamics and multiple functions of oil bodies in seeds and leaves. Plant Physiology, 176, 199-207.
Shu, K., Zhou, W., Chen, F., Luo, X. & Yang, W. (2018) Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Frontiers in Plant Science, 9, 8.
Silverstone, A.L., Chang, C., Krol, E. & Sun, T. (1997) Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. The Plant Journal, 12, 9-19.
Singh, R.K., Miskolczi, P., Maurya, J.P. & Bhalerao, R.P. (2019) A tree ortholog of SHORT VEGETATIVE PHASE floral repressor mediates photoperiodic control of bud dormancy. Current Biology, 29, 128-133.
Susan, J.C., Harrison, J., Paul, C.L. & Frommer, M. (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Research, 22, 2990-2997.
Tan, B.C., Joseph, L.M., Deng, W.T., Liu, L., Li, Q.B., Cline, K. et al. (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. The Plant Journal, 35, 44-56.
Tian, F., Yang, D.C., Meng, Y.Q., Jin, J. & Gao, G. (2020) PlantRegMap: charting functional regulatory maps in plants. Nucleic Acids Research, 48, 1104.
Tomczynska, I., Stumpe, M., Doan, T.G. & Mauch, F. (2020) A Phytophthora effector protein promotes symplastic cell-to-cell trafficking by physical interaction with plasmodesmata-localised callose synthases. New Phytologist, 227, 1467-1478.
Turečková, V., Novák, O. & Strnad, M. (2009) Profiling ABA metabolites in Nicotiana tabacum L. leaves by ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Talanta, 80, 390-399.
Tuskan, G.A., DiFazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U. et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science, 313, 1596-1604.
Tylewicz, S., Petterle, A., Marttila, S., Miskolczi, P., Azeez, A., Singh, R.K. et al. (2018) Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science, 360, 212-215.
Urbanová, T., Tarkowská, D., Novák, O., Hedden, P. & Strnad, M. (2013) Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta, 112, 85-94.
van der Schoot, C., Paul, L.K. & Rinne, P.L.H. (2014) The embryonic shoot: a lifeline through winter. Journal of Experimental Botany, 65, 1699-1712.
Veerabagu, M., Paul, L.K., Rinne, P.L.H. & van der Schoot, C. (2020) Plant lipid bodies traffic on actin to plasmodesmata motorized by myosin XIs. International Journal of Molecular Sciences, 21, 1422.
Veerabagu, M., Rinne, P.L.H., Skaugen, M., Paul, L.K. & van der Schoot, C. (2021) Lipid body dynamics in shoot meristems: production, enlargement, and putative organellar interactions and plasmodesmal targeting. Frontiers in Plant Science, 12, 674031.
Vinces, M.D., Legendre, M., Caldara, M., Hagihara, M. & Verstrepen, K.J. (2009) Unstable tandem repeats in promoters confer transcriptional evolvability. Science, 324, 1213-1216.
Wang, M., Le Moigne, M.A., Bertheloot, J., Crespel, L., Perez-Garcia, M.D., Ogé, L. et al. (2019) BRANCHED1: a key hub of shoot branching. Frontiers in Plant Science, 10, 12.
Ward, S.P. & Leyser, O. (2004) Shoot branching. Current Opinion in Plant Biology, 7, 73-78.
Welling, A., Kaikuranta, P. & Rinne, P. (1997) Photoperiodic induction of dormancy and freezing tolerance in Betula pubescens. involvement of ABA and dehydrins. Physiologia Plantarum, 100, 119-125.
Welling, A. & Palva, E.T. (2006) Molecular control of cold acclimation in trees. Physiologia Plantarum, 127, 167-181.
White, C.N., Proebsting, W.M., Hedden, P. & Rivin, C.J. (2000) Gibberellins and seed development in maize. I. Evidence that gibberellin/abscisic acid balance governs germination versus maturation pathways. Plant Physiology, 122, 1081-1088.
Wu, S.W., Kumar, R., Iswanto, A.B.B. & Kim, J.Y. (2018) Callose balancing at plasmodesmata. Journal of Experimental Botany, 69, 5325-5339.
Yao, C. & Finlayson, S.A. (2015) Abscisic acid is a general negative regulator of Arabidopsis axillary bud growth. Plant Physiology, 169, 611-626.
Ye, Y., Zhou, L., Liu, X., Liu, H., Li, D., Cao, M. et al. (2017) A novel chemical inhibitor of ABA signaling targets all ABA receptors. Plant Physiology, 173, 2356-2369.
Yokoyama, T., Ohkubo, T., Kamiya, K. & Hara, M. (2020) Cryoprotective activity of Arabidopsis KS-type dehydrin depends on the hydrophobic amino acids of two active segments. Archives of Biochemistry and Biophysics, 691, 108510.
Yoneyama, K. & Brewer, P.B. (2021) Strigolactones, how are they synthesized to regulate plant growth and development? Current Opinion in Plant Biology, 63, 102072.
Zanewich, K.P. & Rood, S.B. (1995) Vernalization and gibberellin physiology of winter canola. Endogenous gibberellin (GA) content and metabolism of [3H]GA1 and [3H] GA20. Plant Physiology, 108, 615-621.
Zawaski, C. & Busov, V.B. (2014) Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in Populus trees. PLoS One, 9, e86217.
Zheng, C., Halaly, T., Acheampong, A.K., Takebayashi, Y., Jikumaru, Y., Kamiya, Y. et al. (2015) Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. Journal of Experimental Botany, 66, 1527-1542.
Zheng, C.L., Acheampong, A.K., Shi, Z.W., Halaly, T., Kamiya, Y., Ophir, R. et al. (2018a) Distinct gibberellin functions during and after grapevine bud dormancy release. Journal of Experimental Botany, 69, 1635-1648.
Zheng, C.L., Acheampong, A.K., Shi, Z.W., Mugzech, A., Halaly-Basha, T., Shaya, F. et al. (2018b) Abscisic acid catabolism enhances dormancy release of grapevine buds. Plant, Cell and Environment, 41, 2490-2503.