The vegetative juvenile-to-adult transition (vegetative phase change) is a critical phase in plant development, the timing of which is controlled by the highly conserved age pathway, comprising the miR156/miR157-SPL module and the downstream miR172-AP2-like module, and is modulated by exogenous and endogenous cues. The phytohormones cytokinin (CK) and gibberellin (GA) have been described to both alter miR172 levels, most probably by regulating SPL activity. In this study, we establish an epistatic relation between CK and GA, in which CK action depends on GA, contrasting with the antagonistic nature described previously for CK-GA crosstalk. We show that CK positively affects GA biosynthesis during Arabidopsis vegetative development and depends on the GA biosynthetic enzymes GA3ox1 and GA3ox2 to modify the appearance of abaxial trichomes as well as leaf shape, both hallmarks of vegetative phase change. Downstream of CK, epidermal identity is regulated in dependence of SPL transcription factors, the GA signaling repressors GAI and RGA and the miR172-targets TOE1 and TOE2. Notably, genetic analysis revealed that GA regulates this process also CK-independently. Furthermore, our data from genetic analyses suggests that CK affects leaf shape through other GA signaling components and AP2-like transcription factors rather than SPLs. Hence, CK differentially regulates several aspects of vegetative phase change. The work contributes to the understanding of vegetative phase change regulation as well as phytohormone crosstalk in general.

Institute of Biology Applied Genetics Dahlem Centre of Plant Sciences Freie Universität Berlin Albrecht Thaer Weg 6 Berlin Germany

Laboratory of Growth Regulators Institute of Experimental Botany Czech Academy of Sciences and Faculty of Sciences Palacký University Šlechtitelů 27 Olomouc Czech Republic

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Huijser, P. & Schmid, M. The control of developmental phase transitions in plants. PubMed

Poethig, R. S. & Fouracre, J. Temporal regulation of vegetative phase change in plants. PubMed PMC

Zhao, J., Doody, E. & Poethig, R. S. Reproductive competence is regulated independently of vegetative phase change in PubMed PMC

Fouracre, J. P. & Poethig, R. S. Role for the shoot apical meristem in the specification of juvenile leaf identity in PubMed PMC

Wu, G. et al. The sequential action of miR156 and miR172 regulates developmental timing in PubMed PMC

Wang, J. W., Czech, B. & Weigel, D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in PubMed

He, J. et al. Threshold-dependent repression of PubMed PMC

Cheng, Y.-J. et al. Cell division in the shoot apical meristem is a trigger for miR156 decline and vegetative phase transition in PubMed PMC

Xu, M. et al. Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes in PubMed PMC

Telfer, A., Bollman, K. M. & Poethig, R. S. Phase change and the regulation of trichome distribution in PubMed

Tsukaya, H., Shoda, K., Kim, G. T. & Uchimiya, H. Heteroblasty in PubMed

Usami, T., Horiguchi, G., Yano, S. & Tsukaya, H. The more and smaller cells mutants of PubMed

Rubio-Somoza, I. et al. Temporal control of leaf complexity by miRNA-regulated licensing of protein complexes. PubMed

Aukerman, M. J. & Sakai, H. Regulation of flowering time and floral organ identity by a microRNA and its PubMed PMC

Mathieu, J., Yant, L. J., Mürdter, F., Küttner, F. & Schmid, M. Repression of flowering by the miR172 target PubMed PMC

Chen, X. M. A microRNA as a translational repressor of PubMed PMC

Jung, J. H. et al. The PubMed PMC

Jung, J. H., Seo, P. J., Kang, S. K. & Park, C. M. miR172 signals are incorporated into the miR156 signaling pathway at the PubMed

Wu, G. & Poethig, R. S. Temporal regulation of shoot development in PubMed PMC

Werner, S., Bartrina, I. & Schmülling, T. Cytokinin regulates vegetative phase change in PubMed PMC

Hu, H. et al. TEM1 combinatorially binds to PubMed PMC

Aguilar-Jaramillo, A. E. et al. TEMPRANILLO is a direct repressor of the microRNA miR172. PubMed

Cho, H. J. et al. SHORT VEGETATIVE PHASE (SVP) protein negatively regulates miR172 transcription via direct binding to the PubMed

Tao, Z. et al. Genome-wide identification of SOC1 and SVP targets during the floral transition in PubMed

Hyun, Y. et al. Multi-layered regulation of SPL15 and cooperation with SOC1 integrate endogenous flowering pathways at the PubMed

Wang, L. et al. A spatiotemporally regulated transcriptional complex underlies heteroblastic development of leaf hairs in PubMed PMC

Xu, Y., Qian, Z., Zhou, B. & Wu, G. Age-dependent heteroblastic development of leaf hairs in PubMed

Herman, P. L. & Marks, M. D. Trichome development in PubMed PMC

Zhou, B. et al. Coordinated regulation of vegetative phase change by brassinosteroids and the age pathway in PubMed PMC

Guo, C., Jiang, Y., Shi, M., Wu, X. & Wu, G. ABI5 acts downstream of miR159 to delay vegetative phase change in PubMed

Hu, T., Manuela, D. & Xu, M. SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9 and 13 repress PubMed PMC

Tang, H.-B. et al. Anisotropic cell growth at the leaf base promotes age-related changes in leaf shape in PubMed PMC

Li, X.-M. et al. Cell-cycle-linked growth reprogramming encodes developmental time into leaf morphogenesis. PubMed

Lian, H. et al. Redundant and specific roles of individual PubMed PMC

Inoue, T. et al. Identification of CRE1 as a cytokinin receptor from PubMed

Ueguchi, C., Koizumi, H., Suzuki, T. & Mizuno, T. Novel family of sensor histidine kinase genes in PubMed

Kieber, J. J. & Schaller, G. E. Cytokinin signaling in plant development. PubMed

Hackett, W. P. Juvenility, maturation, and rejuvenation in woody plants.

Zimmerman, R. H., Hackett, W. P. & Pharis, R. P. Hormonal aspects of phase change and precocious flowering. In:

Evans, M. M. & Poethig, R. S. Gibberellins promote vegetative phase change and reproductive maturity in maize. PubMed PMC

Dill, A. & Sun, T. Synergistic derepression of gibberellin signaling by removing RGA and GAI function in PubMed PMC

Chien, J. C. & Sussex, I. M. Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in PubMed PMC

Silverstone, A. L. et al. Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in PubMed PMC

Griffiths, J. et al. Genetic characterization and functional analysis of the GID1 gibberellin receptors in PubMed PMC

Willige, B. C. et al. The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of PubMed PMC

Murase, K., Hirano, Y., Sun, T.-P. & Hakoshima, T. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. PubMed

McGinnis, K. M. et al. The PubMed PMC

Fu, X. et al. The Arabidopsis mutant sleepy1 PubMed PMC

Peng, J. R. et al. The PubMed PMC

Silverstone, A. L., Ciampaglio, C. N. & Sun, T. The PubMed PMC

Tyler, L. et al. DELLA proteins and gibberellin-regulated seed germination and floral development in PubMed PMC

Lee, S. et al. Gibberellin regulates PubMed PMC

Cheng, H. et al. Gibberellin regulates PubMed

Yu, S. et al. Gibberellin regulates the PubMed PMC

Galvão, V. C., Horrer, D., Kuttner, F. & Schmid, M. Spatial control of flowering by DELLA proteins in PubMed

Zhang, T. Q. et al. An intrinsic microRNA timer regulates progressive decline in shoot regenerative capacity in plants. PubMed PMC

Greenboim-Wainberg, Y. et al. Cross talk between gibberellin and cytokinin: the PubMed PMC

Jasinski, S. et al. KNOX action in PubMed

Cai, H. et al. Gibberellin and cytokinin signaling antagonistically control female-germline cell specification in PubMed

Werner, S. et al. The cytokinin status of the epidermis regulates aspects of vegetative and reproductive development in PubMed PMC

Bartrina, I. et al. Gain-of-function mutants of the cytokinin receptors AHK2 and AHK3 regulate plant organ size, flowering time and plant longevity. PubMed PMC

Sun, T.-P. & Kamiya, Y. The PubMed PMC

Mitchum, M. G. et al. Distinct and overlapping roles of two gibberellin 3-oxidases in PubMed

Sun, T.-P. & Kamiya, Y. Regulation and cellular localization of

Yamaguchi, S. Gibberellin metabolism and its regulation. PubMed

Urbanová, T., Tarkowská, D., Strnad, M. & Hedden, P. Gibberellins - terpenoid plant hormones: biological importance and chemical analysis.

Gandikota, M. et al. The miRNA156/157 recognition element in the 3’ UTR of the Arabidopsis SBP box gene PubMed

Kim, J. J. et al. The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via PubMed PMC

Zubo, Y. O. et al. Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in PubMed PMC

Xie, M. et al. A B-ARR-mediated cytokinin transcriptional network directs hormone cross-regulation and shoot development. PubMed PMC

Bhargava, A. et al. Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-seq in PubMed PMC

Talón, M., Koornneef, M. & Zeevaart, J. A. D. Endogenous gibberellins in PubMed PMC

Rieu, I. et al. The gibberellin biosynthetic genes PubMed

Yanai, O. et al. PubMed

Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S. & Matsuoka, M. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. PubMed PMC

Hay, A. et al. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. PubMed

Chen, H., Banerjee, A. K. & Hannapel, D. J. The tandem complex of BEL and KNOX partners is required for transcriptional repression of PubMed

Marash, I. et al. TOR coordinates cytokinin and gibberellin signals mediating development and defense. PubMed

Zentella, R. et al. PubMed PMC

Zentella, R. et al. The PubMed PMC

Xu, S.-L. et al. Proteomic analysis reveals PubMed PMC

Bi, Y. et al. SPINDLY mediates PubMed PMC

Silverstone, A. L. et al. Functional analysis of SPINDLY in gibberellin signaling in PubMed PMC

Swain, S. M., Tseng, T.-S. & Olszewski, N. E. Altered expression of PubMed PMC

Tseng, T.-S., Swain, S. M. & Olszewski, N. E. Ectopic expression of the tetratricopeptide repeat domain of SPINDLY causes defects in gibberellin response. PubMed PMC

Mutanwad, K. V., et al.

Mutanwad, K. V., Neumayer, N., Freitag, C., Zangl, I. & Lucyshyn, D.

Guo, C. et al. Repression of miR156 by miR159 regulates the timing of the juvenile-to-adult transition in PubMed PMC

Díaz-Manzano, F. E. et al. A role for the gene regulatory module microRNA172/TARGET OF EARLY ACTIVATION TAGGED 1/FLOWERING LOCUS T (miRNA172/TOE1/FT) in the feeding sites induced by PubMed PMC

Hunter, C. et al. Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. PubMed PMC

Wang, L. et al. BZR1 physically interacts with SPL9 to regulate the vegetative phase change and cell elongation in PubMed PMC

Beydler, B., Osadchuk, K., Cheng, C.-L., Manak, J. R. & Irish, E. E. The juvenile phase of maize sees upregulation of stress-response genes and is extended by exogenous jasmonic acid. PubMed PMC

Osadchuk, K., Cheng, C.-L. & Irish, E. E. Jasmonic acid levels decline in advance of the transition to the adult phase in maize. PubMed PMC

Mao, Y. B. et al. Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance. PubMed PMC

Marín-de la Rosa, N. et al. Genome wide binding site analysis reveals transcriptional coactivation of cytokinin-responsive genes by DELLA proteins. PubMed PMC

Doody, E., Zha, Y., He, J. & Poethig, R. S. The genetic basis of natural variation in the timing of vegetative phase change in PubMed PMC

Matschi, S., Hake, K., Herde, M., Hause, B. & Romeis, T. The calcium-dependent protein kinase CPK28 regulates development by inducing growth phase-specific, spatially restricted alterations in jasmonic acid levels independent of defense responses in PubMed PMC

Taniguchi, M. et al. Expression of PubMed

Vandesompele, J., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. PubMed PMC

Urbanová, T., Tarkowská, D., Novák, O., Hedden, P. & Strnad, M. Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. PubMed

Rittenberg, D. & Foster, G. L. A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids.