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Meeting at the DNA: Specifying Cytokinin Responses Through Transcription Factor Complex Formation

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Meeting at the DNA: Specifying Cytokinin Responses Through Transcription Factor Complex Formation plants Review Meeting at the DNA: Specifying Cytokinin Responses through Transcription Factor Complex Formation Jan Erik Leuendorf and Thomas Schmülling * Dahlem Centre of Plant Sciences, Institute of Biology/Applied Genetics, Freie Universität Berlin, Albrecht-Thaer-Weg 6, D-14195 Berlin, Germany; [email protected] * Correspondence: [email protected] 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 (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. Citation: Leuendorf, J.E.; Keywords: Arabidopsis thaliana; cytokinin; type-B response regulator; phytohormone; two-component Schmülling, T. Meeting at the DNA: system; crosstalk; transcription; transcription factor complex Specifying Cytokinin Responses through Transcription Factor Complex Formation. Plants 2021, 10, 1458. https://doi.org/10.3390/ 1. Introduction plants10071458 The plant hormone cytokinin has numerous biological activities in regulating plant development and biotic and abiotic stress responses [1–3]. Amongst others, cytokinin Academic Editors: Klaus Harter, regulates shoot meristem size and activity [4], leaf size through control of cell division Virtudes Mira-Rodado and Kenneth and termination of leaf growth [5,6], leaf senescence [7,8], shoot branching [9], flowering Wayne Berendzen time [10], sex determination [11], root meristem size [12,13] and lateral root formation [14], the response to the availability of various nutrients [15,16], the response to highlight and Received: 18 June 2021 photoperiod stress [17,18], and the defense against certain pathogens [19,20]. The large Accepted: 14 July 2021 Published: 16 July 2021 variety and versatility of different functions that cytokinin fulfills raises the question of how a single phytohormone can regulate so many different aspects of plant life. At least Publisher’s Note: MDPI stays neutral part of the answer lies in the complex and specific transcriptional responses that are a with regard to jurisdictional claims in primary result of cytokinin signaling [21–26]. published maps and institutional affil- Cytokinin signals through a plant two-component signal transduction system (TCS). iations. This consists of membrane-bound HISTIDINE KINASES (HK), which sense the cytokinin free bases [27] and transmit the signal through a multistep phosphorylation cascade via HISTIDINE PHOSPHOTRANSFER (HP) proteins to nuclear-localized type-B RESPONSE REGULATOR (RRB) proteins, which are the primary CK output TFs. Arabidopsis thaliana encodes three cytokinin receptors (AHK2, AHK3 and CRE1/AHK4), five AHPs and eleven Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. ARABIDOPSIS RRB (B-type ARR) proteins. Transcriptomic studies have shown that some This article is an open access article of the RRBs convey a very large part of the transcriptional response to CK, which is the distributed under the terms and basis to realize at the end the various biological functions of the hormone. In this review, conditions of the Creative Commons we will therefore first summarize current knowledge about RRBs and their CK-dependent Attribution (CC BY) license (https:// gene regulatory activity. However, despite genome-wide coverage of gene expression data creativecommons.org/licenses/by/ it is largely unknown how the context-dependent specificity of the transcriptional response 4.0/). to CK is achieved. Comparison of transcriptomic data, the occurrence of RRB DNA-binding Plants 2021, 10, 1458. https://doi.org/10.3390/plants10071458 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 17 Plants 2021, 10, 1458 2 of 16 (http://creativecommons.org/licenses transcriptional response to CK is achieved. Comparison of transcriptomic data, the /by/4.0/). occurrence of RRB DNA-binding sites and target genes identified by chromatin immunoprecipitationsites and target genes (ChIP) identified suggested by chromatin that RR immunoprecipitationBs may often not alone (ChIP) be responsible suggested thatfor theRRBs transcriptional may often not CK alone output. be responsible In its second for part, the transcriptional this review reports CK output. on the In increasing its second evidencepart, this that review RRBs reports may act on theas dimers increasing or te evidenceam up with that other RRBs TFs may belonging act as dimers to different or team TFup families. with other Several TFs belonging examples to from different Arabidop TF families.sis illustrate Several that examples TF complex from Arabidopsis formation contributesillustrate that to modulate TF complex the formation CK signaling contributes output and to modulate provides the opportunities CK signaling for output crosstalk and withprovides other opportunitiespathways. for crosstalk with other pathways. 2.2. B-Type B-Type Response Response Regulators Regulators TheThe structure structure of of plant plant RRBs RRBs resembles resembles that that of ofprokaryotic prokaryotic RRs. RRs. They They have have at the at N- the terminalN-terminal end enda phosphate-accepting a phosphate-accepting receiver receiver domain domain with with a conserved a conserved Asp Aspresidue residue as the as sitethe for site regulatory for regulatory phosphorylation. phosphorylation. There There is at least is at leastone nuclear one nuclear localization localization signal signal and towardsand towards the C-terminal the C-terminal end endis located is located a Myb-like a Myb-like DNA-binding DNA-binding domain domain followed followed by by a a putativeputative Gln-/Pro-rich Gln-/Pro-rich activation activation domain domain (Fig (Figureure 1)1)[ [28,29].28,29]. Several Several RRBs RRBs of of Arabidopsis Arabidopsis havehave been been shown shown to to bind bind to to a ashort short DNA DNA sequ sequenceence containing containing the the core core cytokinin cytokinin response response motifmotif (CRM) (CRM) A/GGATC A/GGATC [28,30,31]. [28,30,31]. The The best best characterized characterized extension extension motif motif (ECRM) (ECRM) bound bound byby ARR1 ARR1 is is AAGAT(T/C)TT AAGAT(T/C)TT [32] [32 but] but variants variants of of this this exist exist [33,34,35]. [33–35]. N D D K Myb-like Pro/Gln C receiver domain output domain Figure 1. Schematic structure of plant RRB proteins. The N-terminal signal receiver domain contains Figure 1. Schematic structure of plant RRB proteins. The N-terminal signal receiver domain contains a DDK motif as the phosphoacceptor site. The C-terminal extension (output domain) contains a a DDK motif as the phosphoacceptor site. The C-terminal extension (output domain) contains a Myb-related GARP DNA binding domain (B-motif) and the proline-/glutamine-rich transactivation Myb-related GARP DNA binding domain (B-motif) and the proline-/glutamine-rich transactivation domain.domain. In In addition, addition, RRBs RRBs contain contain at at least least one one nuclear nuclear localization localization signal. signal. Based on the evolutionary relationship of their DNA-binding domains the Ara- Based on the evolutionary relationship of their DNA-binding domains the bidopsis RRBs have been subdivided into three subfamilies, subfamily B-I (ARR1, ARR2, Arabidopsis RRBs have been subdivided into three subfamilies, subfamily B-I (ARR1, ARR10, ARR11, ARR12, ARR14 and ARR18), B-II (ARR13, ARR21) and B-III (ARR19, ARR2, ARR10, ARR11, ARR12, ARR14 and ARR18), B-II (ARR13, ARR21) and B-III ARR20) [36,37]. A core set of subfamily B-I RRBs, ARR1, ARR10 and ARR12, regulate (ARR19, ARR20) [36,37]. A core set of subfamily B-I RRBs, ARR1, ARR10 and ARR12, redundantly a number of important aspects of cytokinin functions, like regulation of regulate redundantly a number of important aspects of cytokinin functions, like growth and development during the vegetative phase [38,39] and responses to high light regulation of growth and development during the vegetative phase [38,39] and responses and photoperiod stress [1,18,40]. Consistently, the transcriptional response to cytokinin towas high strongly light and reduced photoperiod in the arr1 stress arr10 [1,18,40 arr12].mutant, Consistently, but it was the nottranscriptional completely abolishedresponse toand cytokinin the expression was strongly of some reduced cytokinin in response the arr1 genes arr10 was arr12 hardly mutant, affected but [38 ].it ARR2was not has completelyspecific functions abolished during and the leaf expression senescence of [8 ,some41] and cytokinin contributes response to Pseudomonas genes was syringaehardly affectedresistance [38]. [19 ARR2,42]. Whilehas specific there isfunctions convincing duri evidenceng leaf senescence for these four[8,41] RRBs and ofcontributes Arabidopsis to Pseudomonasthat
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