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Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and up-regulation.

ABSTRACT: In plants, numerous developmental processes are controlled by cytokinin (CK) levels and their ratios to levels of other hormones. While molecular mechanisms underlying the regulatory roles of CKs have been intensely researched, proteomic and metabolomic responses to CK deficiency are unknown. Transgenic Arabidopsis seedlings carrying inducible barley cytokinin oxidase/dehydrogenase (CaMV35S>GR>HvCKX2) and agrobacterial isopentenyl transferase (CaMV35S>GR>ipt) constructs were profiled to elucidate proteome- and metabolome-wide responses to down- and up-regulation of CK levels, respectively. Proteome profiling identified >1100 proteins, 155 of which responded to HvCKX2 and/or ipt activation, mostly involved in growth, development, and/or hormone and light signalling. The metabolome profiling covered 79 metabolites, 33 of which responded to HvCKX2 and/or ipt activation, mostly amino acids, carbohydrates, and organic acids. Comparison of the data sets obtained from activated CaMV35S>GR>HvCKX2 and CaMV35S>GR>ipt plants revealed unexpectedly extensive overlaps. Integration of the proteomic and metabolomic data sets revealed: (i) novel components of molecular circuits involved in CK action (e.g. ribosomal proteins); (ii) previously unrecognized links to redox regulation and stress hormone signalling networks; and (iii) CK content markers. The striking overlaps in profiles observed in CK-deficient and CK-overproducing seedlings might explain surprising previously reported similarities between plants with down- and up-regulated CK levels.

SUBMITTER: Cerny M

PROVIDER: S-EPMC3808309 | biostudies-literature | 2013 Nov

REPOSITORIES: biostudies-literature

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Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and up-regulation.

Černý Martin M Kuklová Alena A Hoehenwarter Wolfgang W Fragner Lena L Novák Ondrej O Rotková Gabriela G Jedelsky Petr L PL Žáková Katerina K Šmehilová Mária M Strnad Miroslav M Weckwerth Wolfram W Brzobohaty Bretislav B

Journal of experimental botany 20130924 14

In plants, numerous developmental processes are controlled by cytokinin (CK) levels and their ratios to levels of other hormones. While molecular mechanisms underlying the regulatory roles of CKs have been intensely researched, proteomic and metabolomic responses to CK deficiency are unknown. Transgenic Arabidopsis seedlings carrying inducible barley cytokinin oxidase/dehydrogenase (CaMV35S>GR>HvCKX2) and agrobacterial isopentenyl transferase (CaMV35S>GR>ipt) constructs were profiled to elucidat ...[more]

PMID: 24064926

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Project description:BackgroundThe plant hormone cytokinin regulates growth and development of roots and shoots in opposite ways. In shoots it is a positive growth regulator whereas it inhibits growth in roots. It may be assumed that organ-specific regulation of gene expression is involved in these differential activities, but little is known about it. To get more insight into the transcriptional events triggered by cytokinin in roots and shoots, we studied genome-wide gene expression in cytokinin-treated and cytokinin-deficient roots and shoots.ResultsIt was found by principal component analysis of the transcriptomic data that the immediate-early response to a cytokinin stimulus differs from the later response, and that the transcriptome of cytokinin-deficient plants is different from both the early and the late cytokinin induction response. A higher cytokinin status in the roots activated the expression of numerous genes normally expressed predominantly in the shoot, while a lower cytokinin status in the shoot reduced the expression of genes normally more active in the shoot to a more root-like level. This shift predominantly affected nuclear genes encoding plastid proteins. An organ-specific regulation was assigned to a number of genes previously known to react to a cytokinin signal, including root-specificity for the cytokinin hydroxylase gene CYP735A2 and shoot specificity for the cell cycle regulator gene CDKA;1. Numerous cytokinin-regulated genes were newly discovered or confirmed, including the meristem regulator genes SHEPHERD and CLAVATA1, auxin-related genes (IAA7, IAA13, AXR1, PIN2, PID), several genes involved in brassinosteroid (CYP710A1, CYP710A2, DIM/DWF) and flavonol (MYB12, CHS, FLS1) synthesis, various transporter genes (e.g. HKT1), numerous members of the AP2/ERF transcription factor gene family, genes involved in light signalling (PhyA, COP1, SPA1), and more than 80 ribosomal genes. However, contrasting with the fundamental difference of the growth response of roots and shoots to the hormone, the vast majority of the cytokinin-regulated transcriptome showed similar response patterns in roots and shoots.ConclusionsThe shift of the root and shoot transcriptomes towards the respective other organ depending on the cytokinin status indicated that the hormone determines part of the organ-specific transcriptome pattern independent of morphological organ identity. Numerous novel cytokinin-regulated genes were discovered which had escaped earlier discovery, most probably due to unspecific sampling. These offer novel insights into the diverse activities of cytokinin, including crosstalk with other hormones and different environmental cues, identify the AP2/ERF class of transcriptions factors as particularly cytokinin sensitive, and also suggest translational control of cytokinin-induced changes.

Project description:The plant hormone cytokinin realizes at least part of its signaling output through the regulation of gene expression. A great part of the early transcriptional regulation is mediated by type-B response regulators, which are transcription factors of the MYB family. Other transcription factors, such as the cytokinin response factors of the AP2/ERF family, have also been shown to be involved in this process. Additional transcription factors mediate distinct parts of the cytokinin response through tissue- and cell-specific downstream transcriptional cascades. In Arabidopsis, only a single cytokinin response element, to which type-B response regulators bind, has been clearly proven so far, which has 5'-GAT(T/C)-3' as a core sequence. This motif has served to construct a synthetic cytokinin-sensitive two-component system response element, which is useful for monitoring the cellular cytokinin status. Insight into the extent of transcriptional regulation has been gained by genome-wide gene expression analyses following cytokinin treatment and from plants having an altered cytokinin content or signaling. This review presents a meta analysis of such microarray data resulting in a core list of cytokinin response genes. Genes encoding type-A response regulators displayed the most stable response to cytokinin, but a number of cytokinin metabolism genes (CKX4, CKX5, CYP735A2, UGT76C2) also belong to them, indicating homeostatic mechanisms operating at the transcriptional level. The cytokinin core response genes are also the target of other hormones as well as biotic and abiotic stresses, documenting crosstalk of the cytokinin system with other hormonal and environmental signaling pathways. The multiple links of cytokinin to diverse functions, ranging from control of meristem activity, hormonal crosstalk, nutrient acquisition, and various stress responses, are also corroborated by a compilation of genes that have been repeatedly found by independent gene expression profiling studies. Such functions are, at least in part, supported by genetic studies.

Project description:The relative importance of bottom-up versus top-down control of population dynamics has been the focus of much debate. In infectious disease biology, research is typically focused on the bottom-up process of host resistance, wherein the direction of control flows from the lower to the higher trophic level to impact on pathogen population size and epidemiology. However, the importance of top-down control by a pathogen's natural enemies has been mostly overlooked.Here, we explore the effects of, and interaction between, host genotype (i.e., genetic susceptibility to pathogen infection) and infection by a hyperparasitic fungus, Ampelomyces spp., on the establishment and early epidemic growth and transmission of a powdery mildew plant pathogen (Podosphaera plantaginis). We used a semi-natural field experiment to contrast the impacts of hyperparasite infection, host-plant resistance and spatial structure to reveal the key factors that determine pathogen spread. We then used a laboratory-based inoculation approach to test whether the field experiment results hold across multiple pathogen-host genetic combinations and to explore hyperparasite effects on the pathogen's later life-history stages.We found that hyperparasite infection had a negligible effect on within-host infection development and between-host spread of the pathogen during the onset of epidemics. In contrast, host-plant resistance was the major determinant of whether plants became infected, and host genotype and proximity to an infection source determined infection severity.Our laboratory study showed that, while the interaction between host and pathogen genotypes was the key determinant of infection outcome, hyperparasitism did, on average, reduce the severity of infection. Moreover, hyperparasite infection negatively influenced the production of the pathogen's overwintering structures. Synthesis and applications. Our results suggest that bottom-up host resistance affects pathogen spread, but top-down control of powdery mildew pathogens is likely more effective against later life-history stages. Further, while hyperparasitism in this system can reduce early pathogen growth under stable laboratory conditions, this effect is not detectable in a semi-natural environment. Considering the effects of hyperparasites at multiple points in pathogen's life history will be important when considering hyperparasite-derived biocontrol measures in other natural and agricultural systems.

Dataset Information

Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and up-regulation.

Publications

Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and up-regulation.

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