Most cited article - PubMed ID 31682013
Distinct metabolism of N-glucosides of isopentenyladenine and trans-zeatin determines cytokinin metabolic spectrum in Arabidopsis
Belowground interactions of plants with other organisms in the rhizosphere rely on extensive small-molecule communication. Chemical signals released from host plant roots ensure the development of beneficial arbuscular mycorrhizal (AM) fungi which in turn modulate host plant growth and stress tolerance. However, parasitic plants have adopted the capacity to sense the same signaling molecules and to trigger their own seed germination in the immediate vicinity of host roots. The contribution of AM fungi and parasitic plants to the regulation of phytohormone levels in host plant roots and root exudates remains largely obscure. Here, we studied the hormonome in the model system comprising tobacco as a host plant, Phelipanche spp. as a holoparasitic plant, and the AM fungus Rhizophagus irregularis. Co-cultivation of tobacco with broomrape and AM fungi alone or in combination led to characteristic changes in the levels of endogenous and exuded abscisic acid, indole-3-acetic acid, cytokinins, salicylic acid, and orobanchol-type strigolactones. The hormonal content in exudates of broomrape-infested mycorrhizal roots resembled that in exudates of infested non-mycorrhizal roots and differed from that observed in exudates of non-infested mycorrhizal roots. Moreover, we observed a significant reduction in AM colonization of infested tobacco plants, pointing to a dominant role of the holoparasite within the tripartite system.
- Keywords
- mycorrhizal fungi, parasitic plants, plant hormones, rhizosphere, root exudates, small-molecule communication, strigolactones,
- MeSH
- Chromatography, Liquid MeSH
- Cytokinins metabolism MeSH
- Heterocyclic Compounds, 3-Ring metabolism MeSH
- Mass Spectrometry MeSH
- Fungi physiology MeSH
- Host-Pathogen Interactions MeSH
- Plant Roots metabolism microbiology MeSH
- Abscisic Acid metabolism MeSH
- Salicylic Acid metabolism MeSH
- Indoleacetic Acids metabolism MeSH
- Lactones metabolism MeSH
- Mycorrhizae physiology MeSH
- Orobanche growth & development microbiology MeSH
- Nicotiana growth & development microbiology MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Cytokinins MeSH
- GR24 strigolactone MeSH Browser
- Heterocyclic Compounds, 3-Ring MeSH
- indoleacetic acid MeSH Browser
- Abscisic Acid MeSH
- Salicylic Acid MeSH
- Indoleacetic Acids MeSH
- Lactones MeSH
Adventitious rooting is a de novo organogenesis process that enables plants to propagate clonally and cope with environmental stresses. Adventitious root initiation (ARI) is controlled by interconnected transcriptional and hormonal networks, but there is little knowledge of the genetic and molecular programs orchestrating these networks. Thus, we have applied genome-wide transcriptome profiling to elucidate the transcriptional reprogramming events preceding ARI. These reprogramming events are associated with the down-regulation of cytokinin (CK) signaling and response genes, which could be triggers for ARI. Interestingly, we found that CK free base (iP, tZ, cZ, and DHZ) content declined during ARI, due to down-regulation of de novo CK biosynthesis and up-regulation of CK inactivation pathways. We also found that MYC2-dependent jasmonate (JA) signaling inhibits ARI by down-regulating the expression of the CYTOKININ OXIDASE/DEHYDROGENASE1 (CKX1) gene. We also demonstrated that JA and CK synergistically activate expression of the transcription factor RELATED to APETALA2.6 LIKE (RAP2.6L), and constitutive expression of this transcription factor strongly inhibits ARI. Collectively, our findings reveal that previously unknown genetic interactions between JA and CK play key roles in ARI.
- Keywords
- Adventitious roots, Arabidopsis, CKX1, MYC2, RAP2.6L, cytokinins, jasmonate, light, vegetative propagation,
- MeSH
- Arabidopsis * genetics metabolism MeSH
- Cyclopentanes MeSH
- Plant Roots genetics metabolism MeSH
- Oxylipins MeSH
- Arabidopsis Proteins * genetics metabolism MeSH
- Gene Expression Regulation, Plant MeSH
- Transcription Factors genetics metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Cyclopentanes MeSH
- jasmonic acid MeSH Browser
- Oxylipins MeSH
- Arabidopsis Proteins * MeSH
- RAP2.6L protein, Arabidopsis MeSH Browser
- Transcription Factors MeSH
Plant microgametogenesis involves stages leading to the progressive development of unicellular microspores into mature pollen. Despite the active and continuing interest in the study of male reproductive development, little is still known about the hormonomics at each ontogenetic stage. In this work, we characterized the profiles and dynamics of phytohormones during the process of microgametogenesis in four Nicotiana species (Nicotiana tabacum, Nicotiana alata, Nicotiana langsdorffii, and Nicotiana mutabilis). Taking advantage of advanced HPLC-ESI-MS/MS, twenty to thirty endogenous hormone derivatives were identified throughout pollen ontogenesis, including cytokinins, auxins, ABA and its derivatives, jasmonates, and phenolic compounds. The spectra of endogenous phytohormones changed dynamically during tobacco pollen ontogeny, indicating their important role in pollen growth and development. The different dynamics in the accumulation of endogenous phytohormones during pollen ontogenesis between N. tabacum (section Nicotiana) and the other three species (section Alatae) reflects their different phylogenetic positions and origin within the genus Nicotiana. We demonstrated the involvement of certain phytohormone forms, such as cis-zeatin- and methylthiol-type CKs, some derivatives of abscisic acid, phenylacetic and benzoic acids, in pollen development for the first time here. Our results suggest that unequal levels of endogenous hormones and the presence of specific derivatives may be characteristic for pollen development in different phylogenetic plant groups. These results represent the currently most comprehensive study of plant hormones during the process of pollen development.
- Keywords
- Nicotiana spp., hormonome, male gametophyte, ontogeny, phytohormones, pollen development,
- Publication type
- Journal Article MeSH
De novo shoot organogenesis (DNSO) is a procedure commonly used for the in vitro regeneration of shoots from a variety of plant tissues. Shoot regeneration occurs on nutrient media supplemented with the plant hormones cytokinin (CK) and auxin, which play essential roles in this process, and genes involved in their signaling cascades act as master regulators of the different phases of shoot regeneration. In the last 20 years, the genetic regulation of DNSO has been characterized in detail. However, as of today, the CK and auxin signaling events associated with shoot regeneration are often interpreted as a consequence of these hormones simply being present in the regeneration media, whereas the roles for their prior uptake and transport into the cultivated plant tissues are generally overlooked. Additionally, sucrose, commonly added to the regeneration media as a carbon source, plays a signaling role and has been recently shown to interact with CK and auxin and to affect the efficiency of shoot regeneration. In this review, we provide an integrative interpretation of the roles for CK and auxin in the process of DNSO, adding emphasis on their uptake from the regeneration media and their interaction with sucrose present in the media to their complex signaling outputs that mediate shoot regeneration.
- Keywords
- DNSO, auxin, cytokinin, de novo shoot organogenesis, gene regulatory network, hormone uptake, shoot regeneration, sucrose, transport,
- MeSH
- Cytokinins metabolism MeSH
- Indoleacetic Acids metabolism MeSH
- Organogenesis, Plant * MeSH
- Plant Growth Regulators metabolism MeSH
- Plant Shoots cytology metabolism MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Cytokinins MeSH
- Indoleacetic Acids MeSH
- Plant Growth Regulators MeSH
It has been known for quite some time that cytokinins, hormones typical of plants, are also produced and metabolized in bacteria. Most bacteria can only form the tRNA-bound cytokinins, but there are examples of plant-associated bacteria, both pathogenic and beneficial, that actively synthesize cytokinins to interact with their host. Similar to plants, bacteria produce diverse cytokinin metabolites, employing corresponding metabolic pathways. The identification of genes encoding the enzymes involved in cytokinin biosynthesis and metabolism facilitated their detailed characterization based on both classical enzyme assays and structural approaches. This review summarizes the present knowledge on key enzymes involved in cytokinin biosynthesis, modifications, and degradation in bacteria, and discusses their catalytic properties in relation to the presence of specific amino acid residues and protein structure.
- Keywords
- CKX, LOG, cytochrome P450 monooxygenase, cytokinin, isopentenyl transferase, tRNA modification,
- Publication type
- Journal Article MeSH
- Review MeSH
The spatial location and timing of plant developmental events are largely regulated by the well balanced effects of auxin and cytokinin phytohormone interplay. Together with transport, localized metabolism regulates the concentration gradients of their bioactive forms, ultimately eliciting growth responses. In order to explore the dynamics of auxin and cytokinin metabolism during early seedling growth in Theobroma cacao (cacao), we have performed auxin and cytokinin metabolite profiling in hypocotyls and root developmental sections at different times by using ultra-high-performance liquid chromatography-electrospray tandem mass spectrometry (UHPLC-MS/MS). Our work provides quantitative characterization of auxin and cytokinin metabolites throughout early root and hypocotyl development and identifies common and distinctive features of auxin and cytokinin metabolism during cacao seedling development.
- Keywords
- Theobroma cacao, auxin, cytokinin, phytohormone metabolism, root development,
- Publication type
- Journal Article MeSH
Cytokinins are a class of phytohormones, signalling molecules specific to plants. They act as regulators of diverse physiological processes in complex signalling pathways. It is necessary for plants to continuously regulate cytokinin distribution among different organs, tissues, cells, and compartments. Such regulatory mechanisms include cytokinin biosynthesis, metabolic conversions and degradation, as well as cytokinin membrane transport. In our review, we aim to provide a thorough picture of the latter. We begin by summarizing cytokinin structures and physicochemical properties. Then, we revise the elementary thermodynamic and kinetic aspects of cytokinin membrane transport. Next, we review which membrane-bound carrier proteins and protein families recognize cytokinins as their substrates. Namely, we discuss the families of "equilibrative nucleoside transporters" and "purine permeases", which translocate diverse purine-related compounds, and proteins AtPUP14, AtABCG14, AtAZG1, and AtAZG2, which are specific to cytokinins. We also address long-distance cytokinin transport. Putting all these pieces together, we finally discuss cytokinin distribution as a net result of these processes, diverse in their physicochemical nature but acting together to promote plant fitness.
- Keywords
- ABCG14, AZG1, AZG2, PUP14, cytokinin distribution, cytokinin hydrophobicity, cytokinin transport, membrane transport,
- MeSH
- Arabidopsis metabolism MeSH
- Biological Transport MeSH
- Cell Membrane metabolism MeSH
- Cytokinins metabolism MeSH
- Homeostasis MeSH
- Hydrophobic and Hydrophilic Interactions MeSH
- Kinetics MeSH
- Plant Roots metabolism MeSH
- Membrane Transport Proteins metabolism MeSH
- Arabidopsis Proteins genetics MeSH
- Gene Expression Regulation, Plant MeSH
- Plant Growth Regulators metabolism MeSH
- Signal Transduction physiology MeSH
- Thermodynamics MeSH
- Plant Shoots metabolism MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Cytokinins MeSH
- Membrane Transport Proteins MeSH
- Arabidopsis Proteins MeSH
- Plant Growth Regulators MeSH
Cytokinins are plant hormones, derivatives of adenine with a side chain at the N6-position. They are involved in many physiological processes. While the metabolism of trans-zeatin and isopentenyladenine, which are considered to be highly active cytokinins, has been extensively studied, there are others with less obvious functions, such as cis-zeatin, dihydrozeatin, and aromatic cytokinins, which have been comparatively neglected. To help explain this duality, we present a novel hypothesis metaphorically comparing various cytokinin forms, enzymes of CK metabolism, and their signalling and transporter functions to the comics superheroes Hulk and Deadpool. Hulk is a powerful but short-lived creation, whilst Deadpool presents a more subtle and enduring force. With this dual framework in mind, this review compares different cytokinin metabolites, and their biosynthesis, translocation, and sensing to illustrate the different mechanisms behind the two CK strategies. This is put together and applied to a plant developmental scale and, beyond plants, to interactions with organisms of other kingdoms, to highlight where future study can benefit the understanding of plant fitness and productivity.
- Keywords
- Hulk/Deadpool, aromatic cytokinins, cis-zeatin, cytokinin biosynthesis, cytokinin oxidase/dehydrogenase, cytokinin signalling, cytokinin transport, cytokinins, isopentenyl transferase,
- MeSH
- Arabidopsis metabolism MeSH
- Models, Biological MeSH
- Biological Transport MeSH
- Biological Assay MeSH
- Cytokinins metabolism MeSH
- Plant Physiological Phenomena * MeSH
- Glycosylation MeSH
- Hydrolysis MeSH
- Kinetics MeSH
- Kinetin metabolism MeSH
- Oxidoreductases metabolism MeSH
- Plant Growth Regulators metabolism MeSH
- Plants metabolism MeSH
- Signal Transduction * MeSH
- Protein Binding MeSH
- Zeatin analogs & derivatives MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- cytokinin oxidase MeSH Browser
- Cytokinins MeSH
- dihydrozeatin MeSH Browser
- Kinetin MeSH
- Oxidoreductases MeSH
- Plant Growth Regulators MeSH
- Zeatin MeSH
Cytokinins (CKs) are a class of phytohormones affecting many aspects of plant growth and development. In the complex process of CK homeostasis in plants, N-glucosylation represents one of the essential metabolic pathways. Its products, CK N7- and N9-glucosides, have been largely overlooked in the past as irreversible and inactive CK products lacking any relevant physiological impact. In this work, we report a widespread distribution of CK N-glucosides across the plant kingdom proceeding from evolutionary older to younger plants with different proportions between N7- and N9-glucosides in the total CK pool. We show dramatic changes in their profiles as well as in expression levels of the UGT76C1 and UGT76C2 genes during Arabidopsis ontogenesis. We also demonstrate specific physiological effects of CK N-glucosides in CK bioassays including their antisenescent activities, inhibitory effects on root development, and activation of the CK signaling pathway visualized by the CK-responsive YFP reporter line, TCSv2::3XVENUS. Last but not least, we present the considerable impact of CK N7- and N9-glucosides on the expression of CK-related genes in maize and their stimulatory effects on CK oxidase/dehydrogenase activity in oats. Our findings revise the apparent irreversibility and inactivity of CK N7- and N9-glucosides and indicate their involvement in CK evolution while suggesting their unique function(s) in plants.
- Keywords
- Arabidopsis, N-glucosides, Zea mays, [2-3H]tZ9G, cis-zeatin, cytokinin, cytokinin oxidase/dehydrogenase, oat, senescence, trans-zeatin, β-D-glucosidase Zm-p60.1,
- MeSH
- Arabidopsis genetics metabolism MeSH
- Cytokinins genetics MeSH
- Glucosides genetics MeSH
- Glucosyltransferases genetics MeSH
- Zea mays genetics metabolism MeSH
- Evolution, Molecular * MeSH
- Oxidoreductases genetics MeSH
- Gene Expression Regulation, Plant genetics MeSH
- Plant Growth Regulators genetics metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Cytokinins MeSH
- Glucosides MeSH
- Glucosyltransferases MeSH
- Oxidoreductases MeSH
- Plant Growth Regulators MeSH
Drought and salinity reduce seed germination, seedling emergence, and early seedling establishment, affect plant metabolism, and hence, reduce crop yield. Development of technologies that can increase plant tolerance of these challenging growth conditions is a major current interest among plant scientists and breeders. Seed priming has become established as one of the practical approaches that can alleviate the negative impact of many environmental stresses and improve the germination and overall performance of crops. Hormopriming using different plant growth regulators has been widely demonstrated as effective, but information about using cytokinins (CKs) as priming agents is limited to only a few studies using kinetin or 6-benzylaminopurine (BAP). Moreover, the mode of action of these compounds in improving seed and plant fitness through priming has not yet been studied. For many years, BAP has been one of the CKs most commonly applied exogenously to plants to delay senescence and reduce the impact of stress. However, rapid endogenous N 9-glucosylation of BAP can result in negative effects. This can be suppressed by hydroxylation of the benzyl ring or by appropriate N 9 purine substitution. Replacement of the 2' or 3' hydroxyl groups of a nucleoside with a fluorine atom has shown promising results in drug research and biochemistry as a means of enhancing biological activity and increasing chemical or metabolic stability. Here, we show that the application of this chemical modification in four new N 9-substituted CK derivatives with a fluorinated carbohydrate moiety improved the antisenescence properties of CKs. Besides, detailed phenotypical analysis of the growth and development of Arabidopsis plants primed with the new CK analogs over a broad concentration range and under various environmental conditions revealed that they improve growth regulation and antistress activity. Seed priming with, for example, 6-(3-hydroxybenzylamino)-2'-deoxy-2'-fluoro-9-(β)-D-arabinofuranosylpurine promoted plant growth under control conditions and alleviated the negative effects of the salt and osmotic stress. The mode of action of this hormopriming and its effect on plant metabolism were further analyzed through quantification of the endogenous levels of phytohormones such as CKs, auxins and abscisic acid, and the results are discussed.
- Keywords
- Arabidopsis, abiotic stress, antisenescence, cytokinin analogs, hormopriming, plant biostimulant characterization index,
- Publication type
- Journal Article MeSH