BACKGROUND AND AIMS: Turions are vegetative, dormant overwintering organs formed in aquatic plants in response to unfavourable ecological conditions. Contents of cytokinin (CK), auxin metabolites and abscisic acid (ABA) as main growth and development regulators were compared in innately dormant autumnal turions of 22 aquatic plant species of different functional ecological or taxonomic groups with those in non-dormant winter apices in three aquatic species and with those in spring turions of four species after their overwintering. METHODS: The hormones were analysed in miniature turion samples using ultraperformance liquid chromatography coupled with triple quadrupole mass spectrometry. KEY RESULTS: In innately dormant turions, the total contents of each of the four main CK types, biologically active forms and total CKs differed by two to three orders of magnitude across 22 species; the proportion of active CK forms was 0.18-67 %. Similarly, the content of four auxin forms was extremely variable and the IAA proportion as the active form was 0.014-99 %. The ABA content varied from almost zero to 54 µmol kg-1 dry weight and after overwintering it usually significantly decreased. Of all functional traits studied, hormone profiles depended most on the place of turion sprouting (surface vs bottom) and we suggest that this trait is crucial for turion ecophysiology. CONCLUSIONS: The key role of ABA in regulating turion dormancy was confirmed. However, the highly variable pattern of the ABA content in innately dormant and in overwintered turions indicates that the hormonal mechanism regulating the innate dormancy and its breaking in turions is not uniform within aquatic plants.

Department of Chemical Biology Faculty of Science Palacký University CZ 783 71 Olomouc Czech Republic

Institute of Botany of the Czech Academy of Sciences CZ 379 01 Třeboň Czech Republic

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany AS CR CZ 783 71 Olomouc Czech Republic

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Adamec L. 2003. Ecophysiological characterization of dormancy states in turions of the aquatic carnivorous plant Aldrovanda vesiculosa. Biologia Plantarum 46: 395–402.

Adamec L. 2006. Respiration and photosynthesis of bladders and leaves of aquatic Utricularia species. Plant Biology 8: 765–769. PubMed

Adamec L. 2008. Respiration of turions and winter apices in aquatic carnivorous plants. Biologia 63: 515–520.

Adamec L. 2010. Tissue mineral nutrient content in turions of aquatic plants: does it represent a storage function? Fundamental and Applied Limnology 176: 145–151.

Adamec L. 2011. Dark respiration and photosynthesis of dormant and sprouting turions of aquatic plants. Fundamental and Applied Limnology 179: 151–158.

Adamec L. 2013. A comparison of photosynthetic and respiration rates in six aquatic carnivorous Utricularia species differing in morphology. Aquatic Botany 111: 89–94.

Adamec L. 2018. Ecophysiological characteristics of turions of aquatic plants: a review. Aquatic Botany 148: 64–77.

Adamec L, Kučerová A, Janeček S.. 2020. Mineral nutrients, photosynthetic pigments and storage carbohydrates in turions of 21 aquatic plant species. Aquatic Botany 165: 103238.

Adamec L, Plačková L, Doležal K.. 2022. Cytokinins and auxins in organs of aquatic carnivorous plants: what do they reflect? Annals of Botany 130: 869–882. PubMed PMC

Adamec L, Plačková L, Doležal K.. 2024. Characteristics of turion development in two aquatic carnivorous plants: hormonal profiles, gas exchange and mineral nutrient content. Plant Direct 8: e558. PubMed PMC

Bartley MR, Spence DHN.. 1987. Dormancy and propagation in helophytes and hydrophytes. Archiv für Hydrobiologie (Beiheft) 27: 139–155.

Best EPH. 1979. Growth substances and dormancy in Ceratophyllum demersum. Physiologia Plantarum 45: 399–406.

Davies PJ. 2010. Plant hormones: biosynthesis, signal transduction, action. Dordrecht: Springer.

DeBusk TA, Hanisak MD, Williams LD, Ryther JH.. 1981. Effects of seasonality and plant density on the productivity of some freshwater macrophytes. Aquatic Botany 10: 133–142.

Hadfield JD. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software 33: 1–22. PubMed PMC

Hadfield JD, Nakagawa S.. 2010. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. Journal of Evolutionary Biology 23: 494–508. PubMed

Hussain S, Nanda S, Zhang JH, et al.. 2021. Auxin and cytokinin interplay during leaf morphogenesis and phyllotaxy. Plants 10: 1732. PubMed PMC

Hyldgaard B, Sorrell B, Brix H.. 2014. Closely related freshwater macrophyte species, Ceratophyllum demersum and C. submersum, differ in temperature response. Freshwater Biology 59: 777–788.

Jin Y, Qian H.. 2022. V.PhyloMaker2: an updated and enlarged R package that can generate very large phylogenies for vascular plants. Plant Diversity 44: 335–339. PubMed PMC

Klaine SJ, Ward CH.. 1984. Environmental and chemical control of vegetative dormant bud production in Hydrilla verticillata. Annals of Botany 53: 503–514.

Kruskal JB. 1964. Nonmetric multidimensional scaling: a numerical method. Psychometrika 29: 115–129.

Li CY, Welling A, Puhakainen T, et al.. 2005. Differential responses of silver birch (Betula pendula) ecotypes to short-day photoperiod and low temperature. Tree Physiology 25: 1563–1569. PubMed

Li G, Chen Y, Zhao X, et al.. 2022. Genome-wide analysis of the growth-regulating factor (GRF) family in aquatic plants and their roles in the ABA-induced turion formation of Spirodela polyrhiza. International Journal of Molecular Sciences 23: 10485. PubMed PMC

Noriega X, Pérez F.. 2017. ABA biosynthesis genes are down-regulated while auxin and cytokinin biosynthesis genes are up-regulated during the release of grapevine buds from endodormancy. Journal of Plant Growth Regulators 36: 814–823.

Novák O, Hauserová E, Amakorová P, Doležal K, Strnad M.. 2008. Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69: 2214–2224. PubMed

Oksanen J, Simpson G, Blanchet F, et al.2022. vegan: Community Ecology Package. R package version 2.6-4.https://CRAN.R-project.org/package=vegan (01 December 2023, date last accessed).

Pasaribu B, Acosta K, Aylward A, et al.. 2023. Genomics of turions from the greater duckweed reveal its pathways for dormancy and re-emergence strategy. New Phytologist 239: 116–131. PubMed

Pěnčík A, Rolčík J, Novák O, et al.. 2009. Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. Talanta 80: 651–655. PubMed

R Core Team. 2022. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. https://www.r-project.org (01 December 2023, date last accessed).

Rubio S, Noriega X, Pérez FJ.. 2019. ABA promotes starch synthesis and storage metabolism in dormant grapevine buds. Journal of Plant Physiology 234-235: 1–8. PubMed

Sculthorpe CD. 1967. The biology of aquatic vascular plants. London: Edward Arnold.

Šimura J, Spíchal L, Adamec L, et al.. 2016. Cytokinin, auxin and physiological polarity in the aquatic carnivorous plants Aldrovanda vesiculosa and Utricularia australis. Annals of Botany 117: 1037–1044. PubMed PMC

Skoog F, Miller CO.. 1957. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symposia of The Society For Experimental Biology 54: 118–130. PubMed

Smart CC, Trewavas AJ.. 1983. Abscisic-acid-induced turion germination in Spirodela polyrhiza L. I. Production and development of the turion. Plant, Cell & Environment 6: 507–514.

Smart CC, Fleming AJ, Chaloupková K, Hanke DE.. 1995. The physiological role of abscisic acid in eliciting turion morphogenesis. Plant Physiology 108: 623–632. PubMed PMC

Svačinová J, Novák O, Plačková L, et al.. 2012. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 8: e17. PubMed PMC

Tarkowská D, Novák O, Floková K, et al.. 2014. Quo vadis plant hormone analysis? Planta 240: 55–76. PubMed

Utami D, Kawahata A, Sugawara M, Jog RN, Miwa K, Morikawa M.. 2018. Effect of exogenous general plant growth regulators on the growth of the duckweed Lemna minor. Frontiers in Chemistry 6: e251. PubMed PMC

Van de Haterd RJW, Broeckx P-B, Inberg JA.. 2016. Nieuwe vondsten van Ceratophyllum submersum L. (Fijn hoornblad) in de Maas en de IJsselvallei; uitbreiding als gevolg van klimaatverandering? [New records of Ceratophyllum submersum L. in the River ‘Meuse’ and in the ‘IJssel Valley’; an expansion caused by climate change?] Gorteria 38: 29–33.

Vegis A. 1964. Dormancy in higher plants. Annual Review of Plant Physiology 15: 185–224.

Villemereuil P, Nakagawa S.. 2014. General quantitative genetic methods for comparative biology. In: Garamszegi LZ. ed. Modern phylogenetic comparative methods and their application in evolutionary biology. Berlin: Springer, 287–303.

Wang WQ, Wu YR, Messing J.. 2014. RNA-Seq transcriptome analysis of Spirodela dormancy without reproduction. BMC Genomics 15: 60. PubMed PMC

Wareing PF. 1969. The control of dormancy of seed plants. Symposia of the Society for Experimental Biology 23: 241–262. PubMed

Weber JA, Noodén LD.. 1976. Environmental and hormonal control of turion formation in Myriophyllum verticillatum. Plant and Cell Physiology 17: 721–731.

Wickham H. 2016. ggplot2: elegant graphics for data analysis. New York: Springer.

Winston RD, Gorham PR.. 1979a. Turions and dormancy states in Utricularia vulgaris. Canadian Journal of Botany 57: 2740–2749.

Winston RD, Gorham PR.. 1979b. Roles of endogenous and exogenous growth regulators in dormancy of Utricularia vulgaris. Canadian Journal of Botany 57: 2750–2759.

Yi XK, Xu YL, Gao ZH, et al.. 2020. Warm winter temperature induced changes in the dormant buds of ‘Dangshansuli’ pear (Pyrus bretschneideri Rehd.). Indian Journal of Horticulture 77: 273–278.

Yu G, Smith DK, Zhu H, Guan Y, Lam TT.. 2017. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution 8: 28–36.

Zhang C, Zukauskaite A, Petrík I, et al.. 2021. In situ characterisation of phytohormones from wounded Arabidopsis leaves using desorption electrospray ionisation mass spectrometry imaging. Analyst 146: 2653–2663. PubMed

Ziegler P, Appenroth KJ, Sree KS.. 2023. Survival strategies of duckweeds, the world’s smallest angiosperms. Plants 12: 2215. PubMed PMC