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Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 December 2021) | Viewed by 37208

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Special Issue Editor

Prof. Dr. Georgy A. Romanov

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Guest Editor

Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia
Interests: plant hormones; auxins; cytokinins; phytohormone receptors; phytohormone signaling; arabidopsis; potato

Special Issue Information

Dear Colleagues,

Auxins and cytokinins are considered the most important plant hormones, responsible for fundamental traits of the plant organism. These hormones determine the uniqueness of the plant hormonal system: the main sites of their synthesis are localized at opposite plant body poles, auxins at the top and cytokinins at the bottom. From their synthesis sites, these hormones move along the main plant axis in opposite directions. This pivotal auxin–cytokinin countercurrent creates hormonal gradients that affect cell behavior. Both hormones act synergistically in stimulating cell division but antagonistically in shoot or root branching. In this way, these two hormones determine, to a large extent, the overall plant phenotype. Other important plant traits including resistance to biotic and abiotic stresses are also auxin-/cytokinin-dependent. In the 21st century, great progress has been achieved in dissecting the molecular mechanisms of auxin/cytokinin perception and signal transduction. Both mechanisms were shown to be specific for plants; they do not copy mechanisms typical for animal hormones.

This Special Issue is aimed at unifying researchers studying various aspects of the molecular basis of auxin and/or cytokinin perception and signal transduction. Study on this topic is quickly developing and always attracts great attention from plant biologists due to the central role that these phytohormones play in plant growth, development and resistance. We hope that this issue will serve to promote such studies and make them more visible to the scientific community.

Prof. Dr. Georgy A. Romanov
Guest Editor

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Keywords

auxin signaling
auxin receptors
cytokinin signaling
cytokinin receptors
auxin–cytokinin signaling crosstalk
structural basis for auxin/cytokinin perception
structural basis for auxin/cytokinin signal transduction
subcellular localization of auxin/cytokinin receptors
interference of other hormones with auxin/cytokinin signaling
evolution of auxin/cytokinin signaling
species and tissue specificity of auxin/cytokinin signaling
modifications of auxin/cytokinin signaling
cis-elements in promoters of auxin/cytokinin sensitive genes

Published Papers (11 papers)

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Editorial

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5 pages, 503 KiB

Open AccessEditorial

Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals

by Georgy A. Romanov

Int. J. Mol. Sci. 2022, 23(21), 13150; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232113150 - 29 Oct 2022

Cited by 2 | Viewed by 1613

Abstract

Auxins and cytokinins are considered the most important plant hormones, responsible for fundamental traits of the plant organism [...] Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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Research

Jump to: Editorial, Review

25 pages, 31223 KiB

Open AccessArticle

In Planta, In Vitro and In Silico Studies of Chiral N⁶-Benzyladenine Derivatives: Discovery of Receptor-Specific S-Enantiomers with Cytokinin or Anticytokinin Activities

by Ekaterina M. Savelieva, Anastasia A. Zenchenko, Mikhail S. Drenichev, Anna A. Kozlova, Nikolay N. Kurochkin, Dmitry V. Arkhipov, Alexander O. Chizhov, Vladimir E. Oslovsky and Georgy A. Romanov

Int. J. Mol. Sci. 2022, 23(19), 11334; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms231911334 - 26 Sep 2022

Cited by 7 | Viewed by 1542

Abstract

Cytokinins, classical phytohormones, affect all stages of plant ontogenesis, but their application in agriculture is limited because of the lack of appropriate ligands, including those specific for individual cytokinin receptors. In this work, a series of chiral N⁶-benzyladenine derivatives were studied as potential cytokinins or anticytokinins. All compounds contained a methyl group at the α-carbon atom of the benzyl moiety, making them R- or S-enantiomers. Four pairs of chiral nucleobases and corresponding ribonucleosides containing various substituents at the C2 position of adenine heterocycle were synthesized. A nucleophilic substitution reaction by secondary optically active amines was used. A strong influence of the chirality of studied compounds on their interaction with individual cytokinin receptors of Arabidopsis thaliana was uncovered in in vivo and in vitro assays. The AHK2 and CRE1/AHK4 receptors were shown to have low affinity for the studied S-nucleobases while the AHK3 receptor exhibited significant affinity for most of them. Thereby, three synthetic AHK3-specific cytokinins were discovered: N⁶-((S)-α-methylbenzyl)adenine (S-MBA), 2-fluoro,N⁶-((S)-α-methylbenzyl)adenine (S-FMBA) and 2-chloro,N⁶-((S)-α-methylbenzyl)adenine (S-CMBA). Interaction patterns between individual receptors and specific enantiomers were rationalized by structure analysis and molecular docking. Two other S-enantiomers (N⁶-((S)-α-methylbenzyl)adenosine, 2-amino,N⁶-((S)-α-methylbenzyl)adenosine) were found to exhibit receptor-specific and chirality-dependent anticytokinin properties. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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15 pages, 4712 KiB

Open AccessArticle

The Photoperiod Stress Response in Arabidopsis thaliana Depends on Auxin Acting as an Antagonist to the Protectant Cytokinin

by Manuel Frank, Anne Cortleven, Aleš Pěnčík, Ondrej Novak and Thomas Schmülling

Int. J. Mol. Sci. 2022, 23(6), 2936; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23062936 - 08 Mar 2022

Cited by 1 | Viewed by 1976

Abstract

Fluctuating environmental conditions trigger adaptive responses in plants, which are regulated by phytohormones. During photoperiod stress caused by a prolongation of the light period, cytokinin (CK) has a protective function. Auxin often acts as an antagonist of CK in developmental processes and stress responses. Here, we investigated the regulation of the photoperiod stress response in Arabidopsis thaliana by auxin and its interaction with CK. Transcriptome analysis revealed an altered transcript abundance of numerous auxin metabolism and signaling genes after photoperiod stress treatment. The changes appeared earlier and were stronger in the photoperiod-stress-sensitive CK receptor mutant arabidopsis histidine kinase 2 (ahk2),3 compared to wild-type plants. The concentrations of indole-3-acetic acid (IAA), IAA-Glc and IAA-Asp increased in both genotypes, but the increases were more pronounced in ahk2,3. Genetic analysis revealed that the gain-of-function YUCCA 1 (YUC1) mutant, yuc1D, displayed an increased photoperiod stress sensitivity. In contrast, a loss of the auxin receptors TRANSPORT-INHIBITOR-RESISTANT 1 (TIR1), AUXIN SIGNALING F-BOX 2 (AFB2) and AFB3 in wild-type and ahk2,3 background caused a reduced photoperiod stress response. Overall, this study revealed that auxin promotes response to photoperiod stress antagonizing the protective CK. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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19 pages, 2361 KiB

Open AccessArticle

Cytokinin Perception in Ancient Plants beyond Angiospermae

by Sergey N. Lomin, Ekaterina M. Savelieva, Dmitry V. Arkhipov, Pavel P. Pashkovskiy, Yulia A. Myakushina, Alexander Heyl and Georgy A. Romanov

Int. J. Mol. Sci. 2021, 22(23), 13077; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222313077 - 03 Dec 2021

Cited by 9 | Viewed by 1854

Abstract

Cytokinins (CKs) control many plant developmental processes and responses to environmental cues. Although the CK signaling is well understood, we are only beginning to decipher its evolution. Here, we investigated the CK perception apparatus in early-divergent plant species such as bryophyte Physcomitrium patens, lycophyte Selaginella moellendorffii, and gymnosperm Picea abies. Of the eight CHASE-domain containing histidine kinases (CHKs) examined, two CHKs, PpCHK3 and PpCHK4, did not bind CKs. All other CHK receptors showed high-affinity CK binding (K_D of nM range), with a strong preference for isopentenyladenine over other CK nucleobases in the moss and for trans-zeatin over cis-zeatin in the gymnosperm. The pH dependences of CK binding for these six CHKs showed a wide range, which may indicate different subcellular localization of these receptors at either the plasma- or endoplasmic reticulum membrane. Thus, the properties of the whole CK perception apparatuses in early-divergent lineages were demonstrated. Data show that during land plant evolution there was a diversification of the ligand specificity of various CHKs, in particular, the rise in preference for trans-zeatin over cis-zeatin, which indicates a steadily increasing specialization of receptors to various CKs. Finally, this distinct preference of individual receptors to different CK versions culminated in vascular plants, especially angiosperms. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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23 pages, 6124 KiB

Open AccessArticle

Hormonal Regulation and Crosstalk of Auxin/Cytokinin Signaling Pathways in Potatoes In Vitro and in Relation to Vegetation or Tuberization Stages

by Oksana O. Kolachevskaya, Yulia A. Myakushina, Irina A. Getman, Sergey N. Lomin, Igor V. Deyneko, Svetlana V. Deigraf and Georgy A. Romanov

Int. J. Mol. Sci. 2021, 22(15), 8207; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22158207 - 30 Jul 2021

Cited by 18 | Viewed by 2441

Abstract

Auxins and cytokinins create versatile regulatory network controlling virtually all aspects of plant growth and development. These hormonal systems act in close contact, synergistically or antagonistically, determining plant phenotype, resistance and productivity. However, the current knowledge about molecular interactions of these systems is still scarce. Our study with potato plants aimed at deciphering potential interactions between auxin and cytokinin signaling pathways at the level of respective gene expression. Potato plants grown on sterile medium with 1.5% (vegetation) or 5% (tuberization) sucrose were treated for 1 h with auxin or cytokinin. Effects of these two hormones on expression profiles of genes belonging to main signaling pathways of auxin and cytokinin were quantified by RT-qPCR. As a result, several signaling genes were found to respond to auxin and/or cytokinin by up- or down-regulation. The observed effects were largely organ-specific and depended on sucrose content. Auxin strongly reduced cytokinin perception apparatus while reciprocal cytokinin effect was ambiguous and sucrose-dependent. In many cases, functional clustering of genes of the same family was observed. Promoters in some clusters are enriched with canonic hormone-response cis-elements supporting their direct sensitivity to hormones. Collectively, our data shed new light on the crosstalk between auxin- and cytokinin signaling pathways. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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13 pages, 3330 KiB

Open AccessArticle

Reconstitution of Cytokinin Signaling in Rice Protoplasts

by Eunji Ga, Jaeeun Song, Myung Ki Min, Jihee Ha, Sangkyu Park, Saet Buyl Lee, Jong-Yeol Lee and Beom-Gi Kim

Int. J. Mol. Sci. 2021, 22(7), 3647; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22073647 - 31 Mar 2021

Cited by 5 | Viewed by 2281

Abstract

The major components of the cytokinin (CK) signaling pathway have been identified from the receptors to their downstream transcription factors. However, since signaling proteins are encoded by multigene families, characterizing and quantifying the contribution of each component or their combinations to the signaling cascade have been challenging. Here, we describe a transient gene expression system in rice (Oryza sativa) protoplasts suitable to reconstitute CK signaling branches using the CK reporter construct TCSn:fLUC, consisting of a synthetic CK-responsive promoter and the firefly luciferase gene, as a sensitive readout of signaling output. We used this system to systematically test the contributions of CK signaling components, either alone or in various combinations, with or without CK treatment. The type-B response regulators (RRs) OsRR16, OsRR17, OsRR18, and OsRR19 all activated TCSn:fLUC strongly, with OsRR18 and OsRR19 showing the strongest induction by CK. Cotransfecting the reporter with OsHP01, OsHP02, OsHP05, or OsHK03 alone resulted in much weaker effects relative to those of the type-B OsRRs. When we tested combinations of OsHK03, OsHPs, and OsRRs, each combination exhibited distinct CK signaling activities. This system thus allows the rapid and high-throughput exploration of CK signaling in rice. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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20 pages, 10840 KiB

Open AccessArticle

Light Quality and Intensity Modulate Cold Acclimation in Arabidopsis

by Sylva Prerostova, Petre I. Dobrev, Vojtech Knirsch, Jana Jarosova, Alena Gaudinova, Barbara Zupkova, Ilja T. Prášil, Tibor Janda, Břetislav Brzobohatý, Jan Skalák and Radomira Vankova

Int. J. Mol. Sci. 2021, 22(5), 2736; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22052736 - 08 Mar 2021

Cited by 30 | Viewed by 3352

Abstract

Plant survival in temperate zones requires efficient cold acclimation, which is strongly affected by light and temperature signal crosstalk, which converge in modulation of hormonal responses. Cold under low light conditions affected Arabidopsis responses predominantly in apices, possibly because energy supplies were too limited for requirements of these meristematic tissues, despite a relatively high steady-state quantum yield. Comparing cold responses at optimal light intensity and low light, we found activation of similar defence mechanisms—apart from CBF1–3 and CRF3–4 pathways, also transient stimulation of cytokinin type-A response regulators, accompanied by fast transient increase of trans-zeatin in roots. Upregulated expression of components of strigolactone (and karrikin) signalling pathway indicated involvement of these phytohormones in cold responses. Impaired response of phyA, phyB, cry1 and cry2 mutants reflected participation of these photoreceptors in acquiring freezing tolerance (especially cryptochrome CRY1 at optimal light intensity and phytochrome PHYA at low light). Efficient cold acclimation at optimal light was associated with upregulation of trans-zeatin in leaves and roots, while at low light, cytokinin (except cis-zeatin) content remained diminished. Cold stresses induced elevation of jasmonic acid and salicylic acid (in roots). Low light at optimal conditions resulted in strong suppression of cytokinins, jasmonic and salicylic acid. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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Review

Jump to: Editorial, Research

15 pages, 1772 KiB

Open AccessReview

Auxin/Cytokinin Antagonistic Control of the Shoot/Root Growth Ratio and Its Relevance for Adaptation to Drought and Nutrient Deficiency Stresses

by Jasmina Kurepa and Jan A. Smalle

Int. J. Mol. Sci. 2022, 23(4), 1933; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23041933 - 09 Feb 2022

Cited by 35 | Viewed by 5891

Abstract

The hormones auxin and cytokinin regulate numerous aspects of plant development and often act as an antagonistic hormone pair. One of the more striking examples of the auxin/cytokinin antagonism involves regulation of the shoot/root growth ratio in which cytokinin promotes shoot and inhibits root growth, whereas auxin does the opposite. Control of the shoot/root growth ratio is essential for the survival of terrestrial plants because it allows growth adaptations to water and mineral nutrient availability in the soil. Because a decrease in shoot growth combined with an increase in root growth leads to survival under drought stress and nutrient limiting conditions, it was not surprising to find that auxin promotes, while cytokinin reduces, drought stress tolerance and nutrient uptake. Recent data show that drought stress and nutrient availability also alter the cytokinin and auxin signaling and biosynthesis pathways and that this stress-induced regulation affects cytokinin and auxin in the opposite manner. These antagonistic effects of cytokinin and auxin suggested that each hormone directly and negatively regulates biosynthesis or signaling of the other. However, a growing body of evidence supports unidirectional regulation, with auxin emerging as the primary regulatory component. This master regulatory role of auxin may not come as a surprise when viewed from an evolutionary perspective. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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19 pages, 1059 KiB

Open AccessReview

MicroRNAs Are Involved in Regulating Plant Development and Stress Response through Fine-Tuning of TIR1/AFB-Dependent Auxin Signaling

by Pan Luo, Dongwei Di, Lei Wu, Jiangwei Yang, Yufang Lu and Weiming Shi

Int. J. Mol. Sci. 2022, 23(1), 510; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23010510 - 03 Jan 2022

Cited by 24 | Viewed by 3574

Abstract

Auxin, primarily indole-3-acetic acid (IAA), is a versatile signal molecule that regulates many aspects of plant growth, development, and stress response. Recently, microRNAs (miRNAs), a type of short non-coding RNA, have emerged as master regulators of the auxin response pathways by affecting auxin homeostasis and perception in plants. The combination of these miRNAs and the autoregulation of the auxin signaling pathways, as well as the interaction with other hormones, creates a regulatory network that controls the level of auxin perception and signal transduction to maintain signaling homeostasis. In this review, we will detail the miRNAs involved in auxin signaling to illustrate its in planta complex regulation. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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35 pages, 1412 KiB

Open AccessReview

Integrating the Roles for Cytokinin and Auxin in De Novo Shoot Organogenesis: From Hormone Uptake to Signaling Outputs

by Martin Raspor, Václav Motyka, Abdul Rasheed Kaleri, Slavica Ninković, Ljiljana Tubić, Aleksandar Cingel and Tatjana Ćosić

Int. J. Mol. Sci. 2021, 22(16), 8554; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22168554 - 09 Aug 2021

Cited by 27 | Viewed by 7366

Abstract

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. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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23 pages, 3189 KiB

Open AccessReview

Differential Subcellular Distribution of Cytokinins: How Does Membrane Transport Fit into the Big Picture?

by Daniel Nedvěd, Petr Hošek, Petr Klíma and Klára Hoyerová

Int. J. Mol. Sci. 2021, 22(7), 3428; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22073428 - 26 Mar 2021

Cited by 13 | Viewed by 3222

Abstract

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. Full article

(This article belongs to the Special Issue Perception, Transduction and Crosstalk of Auxin and Cytokinin Signals)

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