Cytokinin Regulates the Etioplast-Chloroplast Transition through the Two-Component Signaling System and Activation of Chloroplast-Related Genes

• Published in: Plant physiology (Bethesda) Vol. 172; no. 1; pp. 464 - 478
• Main Authors: Cortleven, Anne, Marg, Ingke, Yamburenko, Maria V, Schlicke, Hagen, Hill, Kristine, Grimm, Bernhard, Schaller, G. Eric, Schmülling, Thomas
• Format: Journal Article
• Language: English
• Published: United States American Society of Plant Biologists 01-09-2016
• Subjects: Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Benzyl Compounds - pharmacology; Chloroplasts - genetics; Chloroplasts - metabolism; Chloroplasts - ultrastructure; Cytokinins - pharmacology; Gene Expression Regulation, Plant - drug effects; Gene Expression Regulation, Plant - genetics; Gene Expression Regulation, Plant - radiation effects; Genes, Chloroplast - genetics; Immunoblotting; Light; Microscopy, Electron, Transmission; Mutation; Plant Growth Regulators - pharmacology; Plant Leaves - genetics; Plant Leaves - metabolism; Purines - pharmacology; Reverse Transcriptase Polymerase Chain Reaction; Signal Transduction - drug effects; Signal Transduction - genetics; Signal Transduction - radiation effects; SIGNALING AND RESPONSE
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.16.00640

One of the classical functions of the plant hormone cytokinin is the regulation of plastid development, but the underlying molecular mechanisms remain elusive. In this study, we employed a genetic approach to evaluate the role of cytokinin and its signaling pathway in the light-induced development of chloroplasts from etioplasts in Arabidopsis (Arabidopsis thaliana). Cytokinin increases the rate of greening and stimulates ultrastructural changes characteristic for the etioplast-to-chloroplast transition. The steady-state levels of metabolites of the tetrapyrrole biosynthesis pathway leadingto the production of chlorophyll are enhanced by cytokinin. This effect of cytokinin on metabolite levels arises due to the modulation of expression for chlorophyll biosynthesis genes such as HEMA1, GUN4, GUN5, and CHLM. Increased expression of HEMA1 is reflected in an enhanced level of the encoded glutamyl-tRNA reductase, which catalyzes one of the rate-limiting steps of chlorophyll biosynthesis. Mutant analysis indicates that the cytokinin receptors ARABIDOPSIS HIS KINASE2 (AHK2) and AHK3 play a central role in this process. Furthermore, the B-type ARABIDOPSIS RESPONSE REGULATOR1 (ARR1), ARR10, and ARR12 play an important role in mediating the transcriptional output during etioplast-chloroplast transition. B-type ARRs bind to the promotors of HEMA1 and LHCB6 genes, indicating that cytokinin-dependent transcription factors directly regulate genes of chlorophyll biosynthesis and the light harvesting complex. Together, these results demonstrate an important role for the cytokinin signaling pathway in chloroplast development, with the direct transcriptional regulation of chlorophyll biosynthesis genes as a key aspect for this hormonal control.