Most cited article - PubMed ID 27322763
Cytokinins influence root gravitropism via differential regulation of auxin transporter expression and localization in Arabidopsis
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.
- Keywords
- Arabidopsis thaliana, abiotic stress, auxin, crosstalk, cytokinin, photoperiod stress,
- MeSH
- Arabidopsis * metabolism MeSH
- Cytokinins metabolism pharmacology MeSH
- Photoperiod MeSH
- Plant Roots metabolism MeSH
- Indoleacetic Acids metabolism pharmacology MeSH
- Arabidopsis Proteins * genetics metabolism MeSH
- Gene Expression Regulation, Plant MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Cytokinins MeSH
- Indoleacetic Acids MeSH
- Arabidopsis Proteins * MeSH
Cytokinins and ethylene control plant development via sensors from the histidine kinase (HK) family. However, downstream signaling pathways for the key phytohormones are distinct. Here we report that not only cytokinin but also ethylene is able to control root apical meristem (RAM) size through activation of the multistep phosphorelay (MSP) pathway. We found that both cytokinin and ethylene-dependent RAM shortening requires ethylene binding to ETR1 and the HK activity of ETR1. The receiver domain of ETR1 interacts with MSP signaling intermediates acting downstream of cytokinin receptors, further substantiating the role of ETR1 in MSP signaling. We revealed that both cytokinin and ethylene induce the MSP in similar and distinct cell types with ETR1-mediated ethylene signaling controlling MSP output specifically in the root transition zone. We identified members of the MSP pathway specific and common to both hormones and showed that ETR1-regulated ARR3 controls RAM size. ETR1-mediated MSP spatially differs from canonical CTR1/EIN2/EIN3 ethylene signaling and is independent of EIN2, indicating that both pathways can be spatially and functionally separated. Furthermore, we demonstrated that canonical ethylene signaling controls MSP responsiveness to cytokinin specifically in the root transition zone, presumably via regulation of ARR10, one of the positive regulators of MSP signaling in Arabidopsis.
- Keywords
- crosstalk, cytokinin, ethylene, root development, signaling,
- MeSH
- Arabidopsis cytology drug effects growth & development metabolism MeSH
- Cytokinins metabolism pharmacology MeSH
- Ethylenes metabolism pharmacology MeSH
- Phosphorylation drug effects MeSH
- Plant Roots drug effects growth & development MeSH
- Arabidopsis Proteins metabolism MeSH
- Receptors, Cell Surface metabolism MeSH
- Signal Transduction drug effects MeSH
- Dose-Response Relationship, Drug MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Extramural MeSH
- Names of Substances
- Cytokinins MeSH
- ethylene MeSH Browser
- Ethylenes MeSH
- ETR1 protein, Arabidopsis MeSH Browser
- Arabidopsis Proteins MeSH
- Receptors, Cell Surface MeSH
Directional organ growth allows the plant root system to strategically cover its surroundings. Intercellular auxin transport is aligned with the gravity vector in the primary root tips, facilitating downward organ bending at the lower root flank. Here we show that cytokinin signaling functions as a lateral root specific anti-gravitropic component, promoting the radial distribution of the root system. We performed a genome-wide association study and reveal that signal peptide processing of Cytokinin Oxidase 2 (CKX2) affects its enzymatic activity and, thereby, determines the degradation of cytokinins in natural Arabidopsis thaliana accessions. Cytokinin signaling interferes with growth at the upper lateral root flank and thereby prevents downward bending. Our interdisciplinary approach proposes that two phytohormonal cues at opposite organ flanks counterbalance each other's negative impact on growth, suppressing organ growth towards gravity and allow for radial expansion of the root system.
- MeSH
- Arabidopsis physiology MeSH
- Genome-Wide Association Study MeSH
- Cytokinins metabolism MeSH
- Plants, Genetically Modified physiology MeSH
- Genome, Plant genetics MeSH
- Gravitropism MeSH
- Plant Roots metabolism MeSH
- Oxidoreductases genetics metabolism MeSH
- Arabidopsis Proteins metabolism MeSH
- Proteolysis MeSH
- Plant Growth Regulators metabolism MeSH
- Systems Biology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- cytokinin oxidase MeSH Browser
- Cytokinins MeSH
- Oxidoreductases MeSH
- Arabidopsis Proteins MeSH
- Plant Growth Regulators MeSH
Intercellular distribution of the plant hormone auxin largely depends on the polar subcellular distribution of the plasma membrane PIN-FORMED (PIN) auxin transporters. PIN polarity switches in response to different developmental and environmental signals have been shown to redirect auxin fluxes mediating certain developmental responses. PIN phosphorylation at different sites and by different kinases is crucial for PIN function. Here we investigate the role of PIN phosphorylation during gravitropic response. Loss- and gain-of-function mutants in PINOID and related kinases but not in D6PK kinase as well as mutations mimicking constitutive dephosphorylated or phosphorylated status of two clusters of predicted phosphorylation sites partially disrupted PIN3 phosphorylation and caused defects in gravitropic bending in roots and hypocotyls. In particular, they impacted PIN3 polarity rearrangements in response to gravity and during feed-back regulation by auxin itself. Thus PIN phosphorylation, besides regulating transport activity and apical-basal targeting, is also important for the rapid polarity switches in response to environmental and endogenous signals.
- MeSH
- Arabidopsis drug effects physiology MeSH
- Phosphorylation MeSH
- Gravitropism * MeSH
- Plant Roots drug effects physiology MeSH
- Indoleacetic Acids pharmacology MeSH
- Gravity Sensing MeSH
- Cell Polarity * MeSH
- Arabidopsis Proteins genetics metabolism MeSH
- Plant Growth Regulators pharmacology MeSH
- Amino Acid Sequence MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Indoleacetic Acids MeSH
- PIN3 protein, Arabidopsis MeSH Browser
- Arabidopsis Proteins MeSH
- Plant Growth Regulators MeSH
Auxins mediate various processes that are involved in plant growth and development in response to specific environmental conditions. Its proper spatio-temporal distribution that is driven by polar auxin transport machinery plays a crucial role in the wide range of auxins physiological effects. Numbers of approaches have been developed to either directly or indirectly monitor auxin distribution in vivo in order to elucidate the basis of its precise regulation. Herein, we provide an updated list of valuable techniques used for monitoring auxins in plants, with their utilities and limitations. Because the spatial and temporal resolutions of the presented approaches are different, their combination may provide a comprehensive outcome of auxin distribution in diverse developmental processes.
- Keywords
- auxin, auxin distribution, auxin signalling, auxin transport, direct visualization, indirect visualization, receptor, sensor,
- MeSH
- Arabidopsis metabolism MeSH
- Indoleacetic Acids metabolism MeSH
- Gene Expression Regulation, Plant MeSH
- Plant Development physiology MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Indoleacetic Acids MeSH