Group of the role of phytohormones in the interaction with environment

Plant growth and development as well as their responses to environment are regulated by plant hormones. The unique feature of phytohormone action is their intensive cross-talk in the regulation of different processes. Simultaneously, individual phytohormones exhibit multiple functions, being involved in the control of a broad range of processes. Temporal and spatial regulation of the levels of physiologically active hormones is very strict (Dobrev et al., Plant Physiol. Biochem. 2002, Nováková et al., J. Exp. Bot. 2005), both at the level of tissues (e.g. developing meristems) and individual cell compartments (Polanská et al., J. Exp. Bot. 2007). Our Laboratory has been involved in the study of hormone cross-talk (Vaňková et al., in Physiology and Biochemistry of Cytokinins 1992), mechanisms involved in the regulation of the levels of physiologically active forms (Veach et al., 2003, Blagoeva et al., Physiol. Plant. 2004, Mok et al., 2005) and elucidation of their role during ontogenesis (Rodó et al., 2008).

We were the first describing the establishment of active cytokinin gradient in favour of upper leaves in response to water deficit (Havlová et al., Plant Cell Environ. 2008). Elevated cytokinin content enhanced the sink strength of the upper leaves, which was important for their preferential protection. Comparison of transgenic tobacco plants with constitutively enhanced cytokinin turn-over and plants with cytokinin elevation driven by senescence induced promoter revealed that enhanced cytokinin content (before stress initiation) might delay stimulation of defence mechanisms, namely increase of abscisic acid and xanthophyll cycle pigments (Haisel et al., Biol. Plant. 2008). Determination of SAG12 expression profiles showed that recovery after drought stress is an active process and not only the return to control conditions (Vanková et al., Plant Signaling Behaviour 2012). The impact of cytokinin down-regulation on drought responses was characterized in tobacco (Macková et al., J. Exp. Bot. 2013) and in cooperation with Prof. Lam-Son Tran (RIKEN Plant Science Centre, Yokohama, Japan) in Arabidopsis (Nishiyama et al., 2011) and soybean (Le et al., 2012). Evaluation of hormonal dynamics during desiccation and recovery of resurrection species Haberlea rhodopensis revealed important role of jasmonic acid during dehydration (Djilianov et al., 2013) – cooperation with Dr. Dimitar Djilianov (AgroBioInstitute). Our experience in evaluation of cytokinin roles in abiotic stress responses was summarized in a review (Ha et al., Trends in Plant Science 2012). As both cytokinin decrease and up-regulation may diminish drought impact, we performed extensive comparative study in cooperation with Dr. Fabio Fiorani and Prof. Ulrich Schurr (Research Centre Julich, Germany). Cytokinin down-regulation had positive impact on retention of water potential, while their increase promoted plant recovery after re-watering (Přerostová et al., Front. in Plant Sci. 2018).

Hormonal as well as transcriptome changes observed in the early phase of heat stress response, i.e. transient elevation of cytokinins and simultaneous down-regulation of abscisic acid, indicated short-term stomata opening (Dobrá et al., J. Plant Physiol. 2010). As abiotic stresses occur in nature usually in combination, we compared heat stress response of well-watered and drought stressed plants. High increase of the heat stress severity under the conditions of water deficit confirmed the importance of enhanced transpiration for cooling of the leaf surface, at least during the early stage of the response. Monitoring of stomata aperture upon transfer of tobacco plants into elevated temperature confirmed assumed dynamics of stomata movement (Macková et al., J. Exp. Bot. 2013). Targeting of the heat stress to Arabidopsis shoots, roots or to the whole plant revealed fast communication within the plant, associated with transient up-regulation of cytokinin signalling in the non-exposed organ (Dobrá et al., Plant Sci. 2015).

Elevation of cytokinin content had positive effect on leaf proteome in case of heat stress targeted to roots, while rather negative effect was observed in case of shoot targeted heat stress (Skalák et al., J. Exp. Bot. 2016). Transcription of individual antioxidant enzymes was followed during heat and/or drought stress (Lubovská et al., J. Plant Physiol. 2014). During adverse conditions, transcription of chloroplast antioxidant enzymes was suppressed (simultaneously with the decrease of photosynthesis), while transcription of cytoplasmic ones was enhanced under stress conditions. The impact of heat acclimation on heat stress response was characterized in Arabidopsis (Přerostová et al., under review). Application of the inhibitor of cytokinin oxidase/dehydrogenase INCYDE revealed the crucial effect of timing of cytokinin modulation.

Mechanisms underlying salt stress tolerance were studied comparing the stress response of of glycophyte Arabidopsis thaliana and halophyte Thellungiella salsuginea (Přerostová et al., Plant Sci. 2017). Enhanced salinity tolerance was associated with higher basal levels of abscisic and jasmonic acid in apices as well as faster and stronger up-regulation of stress-related genes in the whole plant. In cooperation with Prof. Ewa Niewiadomska (Institute of Plant Physiology, Krakow, Poland) we found that Thellungiella had higher levels of hydrogen peroxide (and lower ratio superoxide/hydrogen peroxide) as well as activity of antioxidant enzymes in thylakoids (Pilarská et al., 2016).

Dynamics of hormonal levels and proteome were characterized during individual phases of cold stress response in winter and spring wheat (Kosová et al., J. Plant Physiol. 2012, J. Proteome Res. 2013). Hormonal changes during long-term cold response of two Triticum monococcum lines confirmed decisive role of cytokinins in vegetative/generative transition (Vankova et al., Environ. Exp. Bot. 2014). Hormonal regulations of cold stress responses were studied in intensive cooperation with Prof. Gábor Galiba, Dr. Tibor Janda and Dr. Gabriela Szalai (Departments of Genetics and Plant Physiology, Agricultural Research Institute, Martonvásár, Hungary) – Majláth et al., 2011, 2012, Vashegyi et al., 2013, Boldizsar et al., 2016, Kalapos et al., 2017, Szalai et al., 2018, Pal et al., 2019) In characterization of responses to extreme temperatures we collaborate with Prof. Břetislav Brzobohatý (Faculty of Agronomy, Mendel University, Brno) and Dr. I. T. Prášil (Institute of Crop Research, Prague).

The effects of abscisic acid on the transcription of chloroplast genes were described in barley (Yamburenko et al., 2013), in cooperation with Prof. Thomas Bőrner (Humboldt University, Berlin, Germany). Cross-talk among brassinosteroids, cytokinins after exposition to green or white light and their impact on expression of plastid genes and photoreceptors (Efimova et al., 2017) was followed in cooperation with Prof. Vladimir V. Kusnetsov (Timiryazev Institute of Plant Physiology, Moscow, Russia). In cooperation with Prof. Joe Kieber (University of North Carolina, USA) we contributed to the characterization of the function of cytokinin response factors (CRFs) (Raines et al., 2016).

Organ-specific response to phosphate deficiency was characterized in Arabidopsis (Přerostová et al., Environ. Exp. Bot., 2018). Nutrient deficiency was associated with down-regulation of active cytokinins (especially of trans-zeatin) and gibberellins predominantly in apices and leaves. In roots, up-regulation of cis-zeatin (low active cytokinin in stimulation of cell division, associated with stress responses) was observed. Decisive role of strigolactones was indicated by down-regulation of strigolactone repressors and after exogenous strigolactone application. The effect of nitrogen deficiency on phenotypic reactions and cytokinin dynamics was characterized in two contrasting Plectranthus genotypes (Paparozzi et al., 2016) in cooperation with Dr. E.T. Paparozzi (University of Nebraska-Lincoln, USA).

Apart from the study of the role of plant hormones during abiotic stress responses, we are interested also in mechanisms of defence to biotic stresses. We found that Blackcurrant reversion virus (BRV) infection in flowers of white and red currant was associated with flower malformation (full blossom) caused by elevation of active cytokinins at the early flower stage (Gaudinová et al., Physiol. Mol. Plant Pathol. 2009). In cooperation with Prof. Krzysztof Wieczorek and Dr. Nina Kammerhofer (University of Natural Resources and Life Sciences, Tulln, Austria) we characterized hormonal changes accompanying infection of Arabidopsis roots with nematode (Kammerhofer et al., 2015a, b). The importance of cytokinins in the establishment of preferential protection of tissues most important for plant fitness during response to wounding and herbivore attack (Schäfer et al., 2015, Brüttig et al., 2017) was described in cooperation with Prof. Martin Schäfer and Dr. Stefan Meldau (Max Planck Institute for Chemical Ecology, Jena, Germany). The positive effect of down-regulation of auxin levels by enhanced conjugation on the tolerance of Solanaceous plants to biotrophic and hemibiotrophic pathogens (D´Ippolito et al., 2016) was described in cooperation with Prof. C.A. Casalongue (National University of Mar del Plata, Argentina). Hormonal dynamics after Plasmodiophora brassicae infection were compared in two Brassica napus cultivars —more resistant SY Alister and more sensitive Hornet (Prerostova et al., Int. J. Mol. Sci. 2018). Enhanced resistance was associated with faster down-regulation of auxins and cytokinins as well as more profound stimulation of salicylic acid levels and signal transduction. Sensitive cultivar exhibited higher increase of jasmonic acid. In cooperation with Astrid Forneck (Institute of Viticulture and Pomology, BOKU, Tulln, Austria) significant induction of jasmonic acid signal transduction was observed in during insect probing by grape phylloxera Daktulosphaira vitifoliae, significant reduction being found during early gall formation (Eitle et al., 2019). Modulation of plant cytokinin levels by the leaf-mining moth Phyllonorycter mespilella, which causes “green islands” in leaves, (Zhang et al., 2018) was characterized in cooperation with Prof. David Giron (Institut de Recherche sur la Biologie de l’Insecte, CNRS/Universite Francois-Rabelais de Tours, Tours, France). Application of ozonated water as a soil drench or foliar spray was tested in cooperation with Dr. Pasqua Veronico (Institute for Sustainable Plant Protection, CNR, Bari, Italy) for the potential control of the root-knot nematode Meloidogyne incognita and the airborne pathogen Tomato spotted wilt virus infection in tomato (Prigigallo et al., 2019). Ozonated water diminished infection in the place of application, but no systemic effects were observed.

We highly appreciate the existing collaboration with other scientific institutions such as

  • University of North Carolina, USA – Prof. Joe Kieber
  • Departments of Genetics and Plant Physiology, Agricultural Research Institute, Martonvásár, Hungary – Prof. Gábor Galiba, Dr. Tibor Janda and Dr. Gabriela Szalai
  • RIKEN Plant Science Centre, Yokohama, Japan – Prof. Lam-Son Tran
  • Research Centre Julich, Germany – Dr. Fabio Fiorani and Prof. Ulrich Schurr
  • Timiryazev Institute of Plant Physiology, Moscow, Russia – Prof. Vladimir V. Kusnetsov

and with other numerous colleagues in the Czech Republic as well as abroad.