The Plant Two-Component System

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Physiology and Metabolism".

Deadline for manuscript submissions: closed (31 December 2019) | Viewed by 23981

Special Issue Editors


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Guest Editor
Center for Plant Molecular Biology (ZMBP)/Plant Physiology, 72076 Tübingen, Germany
Interests: abiotic stress physiology; signal perception by histidine kinases; activity/regulation of transcription factors; composition and dynamics of membrane-bound protein complexes; spectro- and super-resolution microscopy; focusing on Arabidopsis and tobacco

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Guest Editor
Center for Plant Molecular Biology (ZMBP)/Plant Physiology, 72076 Tübingen, Germany
Interests: fluorescence-correlation spectroscopy; microscale thermophoresis; photobiology; two-component system regulation and cross-talk; response regulators; focusing on Arabidopsis

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Guest Editor
Center for Plant Molecular Biology (ZMBP)/Cytometry & FACS, 72076 Tübingen, Germany
Interests: phosphorelay signal transduction; activity/regulation of response regulators; protein-protein interaction networks and methods; combinatorial regulation of promoters; flow cytometry

Special Issue Information

Dear Colleagues,

The plant two-component system (TCS) is a perception-response system that was derived from the ancestral cyanobacterial endosymbiotic plastid. In comparison with the majority of bacterial TCS, the canonical TCS of plants consists of three components: the histidine kinases (HKs), the histidine phosphotransfer proteins (HPs) and the response regulators (RRs). Upon the binding of a specific ligand by the N-terminal input domain, the HK autophosphorylates and the phosphoryl residue is then relayed in multiple steps to the downstream RRs via the HPs. Although many facets of TCS signaling have been elucidated in the past years—especially in the case of cytokinin perception and signaling—many aspects of the TCS remain to be discovered or explained. For instance, what are the input signals and defined functions of those HKs that are not involved in hormonal perception, what determines the speed and direction of the phosphoryl flow through the TCS, how and at which level (HK, HP or RR) are signal integration and specificity achieved, are there discernible sub-TCS networks, as well as how and to which extent does TCS cross-talk into other signal transduction pathways?

This Special Issue of Plants aims to address these questions and will thereby help to clarify the role of the TCS in the control of plant development and interaction with the environment.

Prof. Dr. Klaus Harter
Dr. Virtudes Mira-Rodado
Dr. Kenneth Wayne Berendzen
Guest Editors

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Keywords

  • Two-component system (TCS)
  • histidine kinase
  • phosphotransfer protein
  • response regulator
  • multistep phosphorelay
  • TCS signal perception, transduction, integration and cross-talk
  • TCS physiological output

Published Papers (6 papers)

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Research

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17 pages, 3839 KiB  
Article
High-Level Expression, Purification and Initial Characterization of Recombinant Arabidopsis Histidine Kinase AHK1
by Alexander Hofmann, Sophia Müller, Thomas Drechsler, Mareike Berleth, Katharina Caesar, Leander Rohr, Klaus Harter and Georg Groth
Plants 2020, 9(3), 304; https://doi.org/10.3390/plants9030304 - 01 Mar 2020
Cited by 4 | Viewed by 3470
Abstract
Plants employ a number of phosphorylation cascades in response to a wide range of environmental stimuli. Previous studies in Arabidopsis and yeast indicate that histidine kinase AHK1 is a positive regulator of drought and osmotic stress responses. Based on these studies AHK1 was [...] Read more.
Plants employ a number of phosphorylation cascades in response to a wide range of environmental stimuli. Previous studies in Arabidopsis and yeast indicate that histidine kinase AHK1 is a positive regulator of drought and osmotic stress responses. Based on these studies AHK1 was proposed a plant osmosensor, although the molecular basis of plant osmosensing still remains unknown. To understand the molecular role and signaling mechanism of AHK1 in osmotic stress, we have expressed and purified full-length AHK1 from Arabidopsis in a bacterial host to allow for studies on the isolated transmembrane receptor. Purification of the recombinant protein solubilized from the host membranes was achieved in a single step by metal-affinity chromatography. Analysis of the purified AHK1 by SDS-polyacrylamide gel electrophoresis (SDS-PAGE) and immunoblotting show a single band indicating that the preparation is highly pure and devoid of contaminants or degradation products. In addition, gel filtration experiments indicate that the preparation is homogenous and monodisperse. Finally, CD-spectroscopy, phosphorylation activity, dimerization studies, and protein–protein interaction with plant phosphorylation targeting AHP2 demonstrate that the purified protein is functionally folded and acts as phospho-His or phospho-Asp phosphatase. Hence, the expression and purification of recombinant AHK1 reported here provide a basis for further detailed functional and structural studies of the receptor, which might help to understand plant osmosensing and osmosignaling on the molecular level. Full article
(This article belongs to the Special Issue The Plant Two-Component System)
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17 pages, 1822 KiB  
Article
Steady-State Levels of Cytokinins and Their Derivatives May Serve as a Unique Classifier of Arabidopsis Ecotypes
by Zuzana Samsonová, Nagavalli S. Kiran, Ondřej Novák, Ioannis Spyroglou, Jan Skalák, Jan Hejátko and Vít Gloser
Plants 2020, 9(1), 116; https://doi.org/10.3390/plants9010116 - 17 Jan 2020
Cited by 4 | Viewed by 2915
Abstract
We determined steady-state (basal) endogenous levels of three plant hormones (abscisic acid, cytokinins and indole-3-acetic acid) in a collection of thirty different ecotypes of Arabidopsis that represent a broad genetic variability within this species. Hormone contents were analysed separately in plant shoots and [...] Read more.
We determined steady-state (basal) endogenous levels of three plant hormones (abscisic acid, cytokinins and indole-3-acetic acid) in a collection of thirty different ecotypes of Arabidopsis that represent a broad genetic variability within this species. Hormone contents were analysed separately in plant shoots and roots after 21 days of cultivation on agar plates in a climate-controlled chamber. Using advanced statistical and machine learning methods, we tested if basal hormonal levels can be considered a unique ecotype-specific classifier. We also explored possible relationships between hormone levels and the prevalent environmental conditions in the site of origin for each ecotype. We found significant variations in basal hormonal levels and their ratios in both root and shoot among the ecotypes. We showed the prominent position of cytokinins (CK) among the other hormones. We found the content of CK and CK metabolites to be a reliable ecotype-specific identifier. Correlation with the mean temperature at the site of origin and the large variation in basal hormonal levels suggest that the high variability may potentially be in response to environmental factors. This study provides a starting point for ecotype-specific genetic maps of the CK metabolic and signalling network to explore its contribution to the adaptation of plants to local environmental conditions. Full article
(This article belongs to the Special Issue The Plant Two-Component System)
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17 pages, 3133 KiB  
Article
New Insight into HPts as Hubs in Poplar Cytokinin and Osmosensing Multistep Phosphorelays: Cytokinin Pathway Uses Specific HPts
by François Héricourt, Mélanie Larcher, Françoise Chefdor, Konstantinos Koudounas, Inês Carqueijeiro, Pamela Lemos Cruz, Vincent Courdavault, Mirai Tanigawa, Tatsuya Maeda, Christiane Depierreux, Frédéric Lamblin, Gaëlle Glévarec and Sabine Carpin
Plants 2019, 8(12), 591; https://doi.org/10.3390/plants8120591 - 11 Dec 2019
Cited by 11 | Viewed by 3229
Abstract
We have previously identified proteins in poplar which belong to an osmosensing (OS) signaling pathway, called a multistep phosphorelay (MSP). The MSP comprises histidine-aspartate kinases (HK), which act as membrane receptors; histidine phosphotransfer (HPt) proteins, which act as phosphorelay proteins; and response regulators [...] Read more.
We have previously identified proteins in poplar which belong to an osmosensing (OS) signaling pathway, called a multistep phosphorelay (MSP). The MSP comprises histidine-aspartate kinases (HK), which act as membrane receptors; histidine phosphotransfer (HPt) proteins, which act as phosphorelay proteins; and response regulators (RR), some of which act as transcription factors. In this study, we identified the HK proteins homologous to the Arabidopsis cytokinin (CK) receptors, which are first partners in the poplar cytokinin MSP, and focused on specificity of these two MSPs (CK and OS), which seem to share the same pool of HPt proteins. Firstly, we isolated five CK HKs from poplar which are homologous to Arabidopsis AHK2, AHK3, and AHK4, namely, HK2, HK3a, HK3b, HK4a, HK4b. These HKs were shown to be functional kinases, as observed in a functional complementation of a yeast HK deleted strain. Moreover, one of these HKs, HK4a, was shown to have kinase activity dependent on the presence of CK. Exhaustive interaction tests between these five CK HKs and the 10 HPts characterized in poplar were performed using two-hybrid and BiFC experiments. The resulting partnership was compared to that previously identified between putative osmosensors HK1a/1b and HPt proteins. Finally, in planta coexpression analysis of genes encoding these potential partners revealed that almost all HPts are coexpressed with CK HKs in four different poplar organs. Overall, these results allowed us to unravel the common and specific partnerships existing between OS and CK MSP in Populus. Full article
(This article belongs to the Special Issue The Plant Two-Component System)
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16 pages, 709 KiB  
Review
Meeting at the DNA: Specifying Cytokinin Responses through Transcription Factor Complex Formation
by Jan Erik Leuendorf and Thomas Schmülling
Plants 2021, 10(7), 1458; https://doi.org/10.3390/plants10071458 - 16 Jul 2021
Cited by 7 | Viewed by 2654
Abstract
Cytokinin is a plant hormone regulating numerous biological processes. Its diverse functions are realized through the expression control of specific target genes. The transcription of the immediate early cytokinin target genes is regulated by type-B response regulator proteins (RRBs), which are transcription factors [...] Read more.
Cytokinin is a plant hormone regulating numerous biological processes. Its diverse functions are realized through the expression control of specific target genes. The transcription of the immediate early cytokinin target genes is regulated by type-B response regulator proteins (RRBs), which are transcription factors (TFs) of the Myb family. RRB activity is controlled by phosphorylation and protein degradation. Here, we focus on another step of regulation, the interaction of RRBs among each other or with other TFs to form active or repressive TF complexes. Several examples in Arabidopsis thaliana illustrate that RRBs form homodimers or complexes with other TFs to specify the cytokinin response. This increases the variability of the output response and provides opportunities of crosstalk between the cytokinin signaling pathway and other cellular signaling pathways. We propose that a targeted approach is required to uncover the full extent and impact of RRB interaction with other TFs. Full article
(This article belongs to the Special Issue The Plant Two-Component System)
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18 pages, 2427 KiB  
Review
Role of the Cytokinin-Activated Type-B Response Regulators in Hormone Crosstalk
by Yan O. Zubo and G. Eric Schaller
Plants 2020, 9(2), 166; https://doi.org/10.3390/plants9020166 - 30 Jan 2020
Cited by 36 | Viewed by 6283
Abstract
Cytokinin is an important phytohormone that employs a multistep phosphorelay to transduce the signal from receptors to the nucleus, culminating in activation of type-B response regulators which function as transcription factors. Recent chromatin immunoprecipitation-sequencing (ChIP-seq) studies have identified targets of type-B ARABIDOPSIS RESPONSE [...] Read more.
Cytokinin is an important phytohormone that employs a multistep phosphorelay to transduce the signal from receptors to the nucleus, culminating in activation of type-B response regulators which function as transcription factors. Recent chromatin immunoprecipitation-sequencing (ChIP-seq) studies have identified targets of type-B ARABIDOPSIS RESPONSE REGULATORs (ARRs) and integrated these into the cytokinin-activated transcriptional network. Primary targets of the type-B ARRs are enriched for genes involved in hormonal regulation, emphasizing the extensive crosstalk that can occur between cytokinin, auxin, abscisic acid, brassinosteroids, gibberellic acid, ethylene, jasmonic acid, and salicylic acid. Examination of hormone-related targets reveals multiple regulatory points including biosynthesis, degradation/inactivation, transport, and signal transduction. Here, we consider this early response to cytokinin in terms of the hormones involved, points of regulatory crosstalk, and physiological significance. Full article
(This article belongs to the Special Issue The Plant Two-Component System)
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21 pages, 795 KiB  
Review
New Insights into Multistep-Phosphorelay (MSP)/Two-Component System (TCS) Regulation: Are Plants and Bacteria That Different?
by Virtudes Mira-Rodado
Plants 2019, 8(12), 590; https://doi.org/10.3390/plants8120590 - 11 Dec 2019
Cited by 20 | Viewed by 4457
Abstract
The Arabidopsis multistep-phosphorelay (MSP) is a signaling mechanism based on a phosphorelay that involves three different types of proteins: Histidine kinases, phosphotransfer proteins, and response regulators. Its bacterial equivalent, the two-component system (TCS), is the most predominant device for signal transduction in prokaryotes. [...] Read more.
The Arabidopsis multistep-phosphorelay (MSP) is a signaling mechanism based on a phosphorelay that involves three different types of proteins: Histidine kinases, phosphotransfer proteins, and response regulators. Its bacterial equivalent, the two-component system (TCS), is the most predominant device for signal transduction in prokaryotes. The TCS has been extensively studied and is thus generally well-understood. In contrast, the MSP in plants was first described in 1993. Although great advances have been made, MSP is far from being completely comprehended. Focusing on the model organism Arabidopsis thaliana, this review summarized recent studies that have revealed many similarities with bacterial TCSs regarding how TCS/MSP signaling is regulated by protein phosphorylation and dephosphorylation, protein degradation, and dimerization. Thus, comparison with better-understood bacterial systems might be relevant for an improved study of the Arabidopsis MSP. Full article
(This article belongs to the Special Issue The Plant Two-Component System)
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