The Cytokinin Status of the Epidermis Regulates Aspects of Vegetative and Reproductive Development in Arabidopsis thaliana
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
33732273
PubMed Central
PMC7959818
DOI
10.3389/fpls.2021.613488
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, cytokinin, developmental transitions, epidermis, seed yield, shoot growth,
- Publikační typ
- časopisecké články MeSH
The epidermal cell layer of plants has important functions in regulating plant growth and development. We have studied the impact of an altered epidermal cytokinin metabolism on Arabidopsis shoot development. Increased epidermal cytokinin synthesis or breakdown was achieved through expression of the cytokinin synthesis gene LOG4 and the cytokinin-degrading CKX1 gene, respectively, under the control of the epidermis-specific AtML1 promoter. During vegetative growth, increased epidermal cytokinin production caused an increased size of the shoot apical meristem and promoted earlier flowering. Leaves became larger and the shoots showed an earlier juvenile-to-adult transition. An increased cytokinin breakdown had the opposite effect on these phenotypic traits indicating that epidermal cytokinin metabolism can be a factor regulating these aspects of shoot development. The phenotypic consequences of abbreviated cytokinin signaling in the epidermis achieved through expression of the ARR1-SRDX repressor were generally milder or even absent indicating that the epidermal cytokinin acts, at least in part, cell non-autonomously. Enhanced epidermal cytokinin synthesis delayed cell differentiation during leaf development leading to an increased cell proliferation and leaf growth. Genetic analysis showed that this cytokinin activity was mediated mainly by the AHK3 receptor and the transcription factor ARR1. We also demonstrate that epidermal cytokinin promotes leaf growth in a largely cell-autonomous fashion. Increased cytokinin synthesis in the outer layer of reproductive tissues and in the placenta enhanced ovule formation by the placenta and caused the formation of larger siliques. This led to a higher number of seeds in larger pods resulting in an increased seed yield per plant. Collectively, the results provide evidence that the cytokinin metabolism in the epidermis is a relevant parameter determining vegetative and reproductive plant growth and development.
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Abràmoff M. D., Magalhães P. J., Ram S. J. (2004). Image processing with ImageJ. Biophoton. Int. 11 36–42.
Antoniadi I., Novák O., Gelova Z., Johnson A., Plíhal O., Simerský R., et al. (2020). Cell-surface receptors enable perception of extracellular cytokinins. Nat. Commun. 11:4284. 10.1038/s41467-020-17700-9 PubMed DOI PMC
Argyros R. D., Mathews D. E., Chiang Y. H., Palmer C. M., Thibault D. M., Etheridge N., et al. (2008). Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20 2102–2116. 10.1105/tpc.108.059584 PubMed DOI PMC
Arnaud D., Lee S., Takebayashi Y., Choi D., Choi J., Sakakibara H., et al. (2017). Cytokinin-mediated regulation of reactive oxygen species homeostasis modulates stomatal immunity in Arabidopsis. Plant Cell 29 543–559. 10.1105/tpc.16.00583 PubMed DOI PMC
Bartrina I., Jensen H., Novák O., Strnad M., Werner T., Schmülling T. (2017). Gain-of-function mutants of the cytokinin receptors AHK2 and AHK3 regulate plant organ size, flowering time and plant longevity. Plant Physiol. 173 1783–1797. 10.1104/pp.16.01903 PubMed DOI PMC
Bartrina I., Otto E., Strnad M., Werner T., Schmülling T. (2011). Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23 69–80. 10.1105/tpc.110.079079 PubMed DOI PMC
Bencivenga S., Simonini S., Benkova E., Colombo L. (2012). The transcription factors BEL1 and SPL are required for cytokinin and auxin signaling during ovule development in Arabidopsis. Plant Cell 24 2886–2897. 10.1105/tpc.112.100164 PubMed DOI PMC
Bhargava A., Clabaugh I., To J. P., Maxwell B. B., Chiang Y. H., Schaller G. E., et al. (2013). Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-seq in Arabidopsis. Plant Physiol. 162 272–294. 10.1104/pp.113.217026 PubMed DOI PMC
Brenner W. G., Ramireddy E., Heyl A., Schmülling T. (2012). Gene regulation by cytokinin in Arabidopsis. Front. Plant Sci. 3:8. 10.3389/fpls.2012.00008 PubMed DOI PMC
Cerbantez-Bueno V. E., Zúñiga-Mayo V. M., Reyes-Olalde J. I., Lozano-Sotomayor P., Herrera-Ubaldo H., Marsch-Martínez N., et al. (2020). Redundant and non-redundant functions of the AHK cytokinin receptors during gynoecium development. Front. Plant Sci. 11:568277. 10.3389/fpls.2020.568277 PubMed DOI PMC
Chickarmane V. S., Gordon S. P., Tarr P. T., Heisler M. G., Meyerowitz E. M. (2012). Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. U.S.A. 109 4002–4007. 10.1073/pnas.1200636109 PubMed DOI PMC
Clough S. J., Bent A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16 735–743. 10.1046/j.1365-313x.1998.00343.x PubMed DOI
Cortleven A., Nitschke S., Klaumünzer M., Abdelgawad H., Asard H., Grimm B., et al. (2014). A novel protective function for cytokinin in the light stress response is mediated by the ARABIDOPSIS HISTIDINE KINASE2 and ARABIDOPSIS HISTIDINE KINASE3 receptors. Plant Physiol. 164 1470–1483. 10.1104/pp.113.224667 PubMed DOI PMC
Czesnick H., Lenhard M. (2015). Size control in plants – lessons from leaves and flowers. Cold Spring Harb. Perspect. Biol. 7:a019190. 10.1101/cshperspect.a019190 PubMed DOI PMC
Efroni I., Han S. K., Kim H. J., Wu M. F., Steiner E., Birnbaum K. D., et al. (2013). Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev. Cell 24 438–445. 10.1016/j.devcel.2013.01.019 PubMed DOI PMC
Grandjean O., Vernoux T., Laufs P., Belcram K., Mizukami Y., Traas J. (2004). In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis. Plant Cell 16 74–87. 10.1105/tpc.017962 PubMed DOI PMC
Gruel J., Landrein B., Tarr P., Schuster C., Refahi Y., Sampathkumar A., et al. (2016). An epidermis-driven mechanism positions and scales stem cell niches in plants. Sci. Adv. 2:e1500989. 10.1126/sciadv.1500989 PubMed DOI PMC
Ha C. M., Jun J. H., Fletcher J. C. (2010). Shoot apical meristem form and function. Curr. Top. Dev. Biol. 91 103–140. 10.1016/S0070-2153(10)91004-1 PubMed DOI
Hemerly A. S., Ferreira P., Engler J. D., Van Montagu M., Engler G., Inzé D. (1993). Cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5 1711–1723. 10.1105/tpc.5.12.1711 PubMed DOI PMC
Heyl A., Ramireddy E., Brenner W. G., Riefler M., Allemeersch J., Schmülling T. (2008). The transcriptional repressor ARR1-SRDX suppresses pleiotropic cytokinin activities in Arabidopsis. Plant Physiol. 147 1380–1395. 10.1104/pp.107.115436 PubMed DOI PMC
Higuchi M., Pischke M. S., Mähönen A. P., Miyawaki K., Hashimoto Y., Seki M., et al. (2004). In planta functions of the Arabidopsis cytokinin receptor family. Proc. Natl. Acad. Sci. U.S.A. 101 8821–8826. 10.1073/pnas.0402887101 PubMed DOI PMC
Hiratsu K., Matsui K., Koyama T., Ohme-Takagi M. (2003). Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J. 34 733–739. 10.1046/j.1365-313X.2003.01759.x PubMed DOI
Holst K., Schmülling T., Werner T. (2011). Enhanced cytokinin degradation in leaf primordia of transgenic Arabidopsis plants reduces leaf size and shoot organ primordia formation. J. Plant Physiol. 168 1328–1334. 10.1016/j.jplph.2011.03.003 PubMed DOI
Horiguchi G., Tsukaya H. (2011). Organ size regulation in plants: insights from compensation. Front. Plant Sci. 2:24. 10.3389/fpls.2011.00024 PubMed DOI PMC
Hou B., Lim E. K., Higgins G. S., Bowles D. J. (2004). N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. J. Biol. Chem. 279 47822–47832. 10.1074/jbc.M409569200 PubMed DOI
Huijser P., Schmid M. (2011). The control of developmental phase transitions in plants. Development 138 4117–4129. 10.1242/dev.063511 PubMed DOI
Hwang I., Sheen J. (2001). Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413 383–389. 10.1038/35096500 PubMed DOI
Hwang I., Sheen J., Müller B. (2012). Cytokinin signaling networks. Annu. Rev. Plant Biol. 63 353–380. 10.1146/annurev-arplant-042811-105503 PubMed DOI
Ingram G. C. (2004). Between the sheets: inter-cell-layer communication in plant development. Philos. Trans. R. Soc. London [Biol.] 359 891–906. 10.1098/rstb.2003.1356 PubMed DOI PMC
Inoue T., Higuchi M., Hashimoto Y., Seki M., Kobayashi M., Kato T., et al. (2001). Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409 1060–1063. 10.1038/35059117 PubMed DOI
Ishida K., Yamashino T., Yokoyama A., Mizuno T. (2008). Three type-B response regulators, ARR1, ARR10 and ARR12, play essential but redundant roles in cytokinin signal transduction throughout the life cycle of Arabidopsis thaliana. Plant Cell Physiol. 49 47–57. 10.1093/pcp/pcm165 PubMed DOI
Kakimoto T. (2001). Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant Cell Physiol. 42 677–685. 10.1093/pcp/pce112 PubMed DOI
Karimi M., De Meyer B., Hilson P. (2005). Modular cloning in plant cells. Trends Plant Sci. 10 103–105. 10.1016/j.tplants.2005.01.008 PubMed DOI
Karimi M., Inzé D., Depicker A. (2002). GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7 193–195. 10.1016/s1360-1385(02)02251-3 PubMed DOI
Kiba T., Takei K., Kojima M., Sakakibara H. (2013). Side-chain modification of cytokinins controls shoot growth in Arabidopsis. Dev. Cell 27 452–461. 10.1016/j.devcel.2013.10.004 PubMed DOI
Kieber J. J., Schaller G. E. (2014). Cytokinins. Arabidopsis Book 12:e0168. 10.1199/tab.0168 PubMed DOI PMC
Kieber J. J., Schaller G. E. (2018). Cytokinin signaling in plant development. Development 145:dev149344. 10.1242/dev.149344 PubMed DOI
Kurakawa T., Ueda N., Maekawa M., Kobayashi K., Kojima M., Nagato Y., et al. (2007). Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445 652–655. 10.1038/nature05504 PubMed DOI
Kuroha T., Tokunaga H., Kojima M., Ueda N., Ishida T., Nagawa S., et al. (2009). Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21 3152–3169. 10.1105/tpc.109.068676 PubMed DOI PMC
Li J., Nie X., Tan J. L., Berger F. (2013). Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 110 15479–15484. 10.1073/pnas.1305175110 PubMed DOI PMC
Lu P. Z., Porat R., Nadeau J. A., Oneill S. D. (1996). Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8 2155–2168. 10.1105/tpc.8.12.2155 PubMed DOI PMC
Malamy J. E., Benfey P. N. (1997). Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124 33–44. PubMed
Maloof J. N., Nozue K., Mumbach M. R., Palmer C. M. (2013). LeafJ: an ImageJ plugin for semi-automated leaf shape measurement. J. Vis. Exp. 21:50028. 10.3791/50028 PubMed DOI PMC
Marcotrigiano M. (2010). A role for leaf epidermis in the control of leaf size and the rate and extent of mesophyll cell division. Am. J. Bot. 97 224–233. 10.3732/ajb.0900102 PubMed DOI
Marsch-Martínez N., Ramos-Cruz D., Reyes-Olalde J. I., Lozano-Sotomayor P., Zúñiga-Mayo V. M., de Folter S. (2012). The role of cytokinin during Arabidopsis gynoecia and fruit morphogenesis and patterning. Plant J. 72 222–234. 10.1111/j.1365-313X.2012.05062 PubMed DOI
Mason M. G., Li J., Mathews D. E., Kieber J. J., Schaller G. E. (2004). Type-B response regulators display overlapping expression patterns in Arabidopsis. Plant Physiol. 135 927–937. 10.1104/pp.103.038109 PubMed DOI PMC
Matías-Hernández L., Aguilar-Jaramillo A. E., Cigliano R. A., Sanseverino W., Pelaz S. (2016). Flowering and trichome development share hormonal and transcription factor regulation. J. Exp. Bot. 67 1209–1219. 10.1093/jxb/erv534 PubMed DOI
Michniewicz M., Kamieńska A. (1965). Flower formation induced by kinetin and vitamin E treatment in long-day plant (Arabidopsis thaliana) grown in short day. Naturwissenschaften 52:623.
Miyawaki K., Tarkowski P., Matsumoto-Kitano M., Kato T., Sato S., Tarkowska D., et al. (2006). Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 103 16598–16603. 10.1073/pnas.0603522103 PubMed DOI PMC
Morcuende R., Bari R., Gibon Y., Zheng W. M., Pant B. D., Bläsing O., et al. (2007). Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ. 30 85–112. 10.1111/j.1365-3040.2006.01608.x PubMed DOI
Niemann M. C., Bartrina I., Ashikov A., Weber H., Novák O., Spíchal L., et al. (2015). Arabidopsis ROCK1 transports UDP-GlcNAc/UDP-GalNAc and regulates ER protein quality control and cytokinin activity. Proc. Natl. Acad. Sci. U.S.A. 112 291–296. 10.1073/pnas.1419050112 PubMed DOI PMC
Nishimura C., Ohashi Y., Sato S., Kato T., Tabata S., Ueguchi C. (2004). Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16 1365–1377. 10.1105/tpc.021477 PubMed DOI PMC
Nobusawa T., Okushima Y., Nagata N., Kojima M., Sakakibara H., Umeda M. (2013). Synthesis of very-long-chain fatty acids in the epidermis controls plant organ growth by restricting cell proliferation. PLoS Biol. 11:e1001531. 10.1371/journal.pbio.1001531 PubMed DOI PMC
Novák O., Hauserová E., Amakorová P., Doležal K., Strnad M. (2008). Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69 2214–2224. 10.1016/j.phytochem.2008.04.022 PubMed DOI
Ohta M., Matsui K., Hiratsu K., Shinshi H., Ohme-Takagi M. (2001). Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13 1959–1968. 10.1105/TPC.010127 PubMed DOI PMC
Osugi A., Kojima M., Takebayashi Y., Ueda N., Kiba T., Sakakibara H. (2017). Systemic transport of trans-zeatin and its precursor have differing roles in Arabidopsis shoots. Nat. Plants 3:17112. 10.1038/nplants.2017.112 PubMed DOI
Poethig R. S. (2013). Vegetative phase change and shoot maturation in plants. Curr. Top. Dev. Biol. 105 125–152. 10.1016/B978-0-12-396968-2.00005-1 PubMed DOI PMC
Riefler M., Novak O., Strnad M., Schmülling T. (2006). Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18 40–54. 10.1105/tpc.105.037796 PubMed DOI PMC
Romanov G. A., Lomin S. N., Schmülling T. (2006). Biochemical characteristics and ligand-binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/A/AHK4 as revealed by a direct binding assay. J. Exp. Bot. 57 4051–4058. 10.1093/jxb/erl179 PubMed DOI
Sakai H., Aoyama T., Oka A. (2000). Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 24 703–711. 10.1046/j.1365-313x.2000.00909.x PubMed DOI
Sakai H., Honma T., Aoyama T., Sato S., Kato T., Tabata S., et al. (2001). ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294 1519–1521. 10.1126/science.1065201 PubMed DOI
Savaldi-Goldstein S., Chory J. (2008). Growth coordination and the shoot epidermis. Curr. Opin. Plant Biol. 11 42–48. 10.1016/j.pbi.2007.10.009 PubMed DOI PMC
Savaldi-Goldstein S., Peto C., Chory J. (2007). The epidermis both drives and restricts plant shoot growth. Nature 446 199–202. 10.1038/nature05618 PubMed DOI
Schnablovà R., Herben T., Klimešova J. (2017). Shoot apical meristem and plant body organization: a cross-species comparative study. Ann. Bot. 120 833–843. 10.1093/aob/mcx116 PubMed DOI PMC
Schwarz I., Scheirlinck M. T., Otto E., Bartrina I., Schmidt R. C., Schmülling T. (2020). Cytokinin regulates the activity of the inflorescence meristem and components of seed yield in oilseed rape. J. Exp. Bot. 71 7146–7159. 10.1093/jxb/eraa419 PubMed DOI
Sessions A., Weigel D., Yanofsky M. F. (1999). The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J. 20 259–263. 10.1046/j.1365-313x.1999.00594.x PubMed DOI
Skalák J., Vercruyssen L., Claeys H., Hradilová J., Cerny M., Novák O., et al. (2019). Multifaceted activity of cytokinin in leaf development shapes its size and structure in Arabidopsis. Plant J. 97 805–824. 10.1111/tpj.14285 PubMed DOI
Stolz A., Riefler M., Lomin S. N., Achazi K., Romanov G. A., Schmülling T. (2011). The specificity of cytokinin signalling in Arabidopsis thaliana is mediated by differing ligand affinities and expression profiles of the receptors. Plant J. 67 157–168. 10.1111/j.1365-313X.2011.04584.x PubMed DOI
Suzuki T., Miwa K., Ishikawa K., Yamada H., Aiba H., Mizuno T. (2001). The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol. 42 107–113. 10.1093/pcp/pce037 PubMed DOI
Tajima Y., Imamura A., Kiba T., Amano Y., Yamashino T., Mizuno T. (2004). Comparative studies on the type-B response regulators revealing their distinctive properties in the His-to-Asp phosphorelay signal transduction of Arabidopsis thaliana. Plant Cell Physiol. 45 28–39. 10.1093/pcp/pcg154 PubMed DOI
Takada S., Jürgens G. (2007). Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134 1141–1150. 10.1242/dev.02803 PubMed DOI
Takada S., Takada N., Yoshida A. (2013). ATML1 promotes epidermal cell differentiation in Arabidopsis shoots. Development 140 1919–1923. 10.1242/dev.094417 PubMed DOI
Takei K., Sakakibara H., Sugiyama T. (2001). Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J. Biol. Chem. 276 26405–26410. 10.1074/jbc.M102130200 PubMed DOI
Takei K., Yamaya T., Sakakibara H. (2004). Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J. Biol. Chem. 279 41866–41872. 10.1074/jbc.M406337200 PubMed DOI
Tanaka Y., Suzuki T., Yamashino T., Mizuno T. (2004). Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 68 462–465. 10.1271/bbb.68.462 PubMed DOI
Telfer A., Bollman K. M., Poethig R. S. (1997). Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124 645–654. PubMed
To J. P. C., Haberer G., Ferreira F. J., Deruere J., Mason M. G., Schaller G. E., et al. (2004). Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16 658–671. 10.1105/tpc.018978 PubMed DOI PMC
Tokunaga H., Kojima M., Kuroha T., Ishida T., Sugimoto K., Kiba T., et al. (2012). Arabidopsis LONELY GUY (LOG) multiple mutants reveal a central role of the LOG-dependent pathway in cytokinin activation. Plant J. 69 355–365. 10.1111/j.1365-313X.2011.04795.x PubMed DOI
Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., et al. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:research0034.1. 10.1186/gb-2002-3-7-research0034 PubMed DOI PMC
Vaseva I., Qudeimat E., Potuschak T., Du Y., Genschik P., Vandenbussche F., et al. (2018). The plant hormone ethylene restricts Arabidopsis growth via the epidermis. Proc. Natl. Acad. Sci. U.S.A. 115 E4130–E4139. 10.1073/pnas.1717649115 PubMed DOI PMC
Vatén A., Soyars C. L., Tarr P. T., Nimchuk Z. L., Bergmann D. C. (2018). Modulation of asymmetric division diversity through cytokinin and SPEECHLESS regulatory interactions in the Arabidopsis stomatal lineage. Dev. Cell 47:e55. 10.1016/j.devcel.2018.08.007 PubMed DOI PMC
Werner T., Köllmer I., Bartrina I., Holst K., Schmülling T. (2006). New insights into the biology of cytokinin degradation. Plant Biol. 8 371–381. 10.1055/s-2006-923928 PubMed DOI
Werner T., Motyka V., Laucou V., Smets R., Van Onckelen H., Schmülling T. (2003). Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15 2532–2550. 10.1105/tpc.014928 PubMed DOI PMC
Werner T., Motyka V., Strnad M., Schmülling T. (2001). Regulation of plant growth by cytokinin. Proc. Natl. Acad. Sci. U.S.A. 98 10487–10492. 10.1073/pnas.171304098 PubMed DOI PMC
Werner T., Schmülling T. (2009). Cytokinin action in plant development. Curr. Opin. Plant Biol. 12 527–538. 10.1016/j.pbi.2009.07.002 PubMed DOI
Wulfetange K., Lomin S. N., Romanov G. A., Stolz A., Heyl A., Schmülling T. (2011). The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol. 156 1808–1818. 10.1104/pp.111.180539 PubMed DOI PMC
Yadav R. K., Tavakkoli M., Xie M., Girke T., Reddy G. V. (2014). A high-resolution gene expression map of the Arabidopsis shoot meristem stem cell niche. Development 141 2735–2744. 10.1242/dev.106104 PubMed DOI
Yamada H., Suzuki T., Terada K., Takei K., Ishikawa K., Miwa K., et al. (2001). The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42 1017–1023. 10.1093/pcp/pce127 PubMed DOI
Yeats T. H., Rose J. K. (2013). The formation and function of plant cuticles. Plant Physiol. 163 5–20. 10.1104/pp.113.222737 PubMed DOI PMC
Yoshida S., Mandel T., Kuhlemeier C. (2011). Stem cell activation by light guides plant organogenesis. Genes Dev. 25 1439–1450. 10.1101/gad.631211 PubMed DOI PMC
Zubo Y. O., Blakley I. C., Yamburenko M. V., Worthen J. M., Street I. H., Franco-Zorrilla J. M., et al. (2017). Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 114 E5995–E6004. 10.1073/pnas.1620749114 PubMed DOI PMC
Zúñiga-Mayo V. M., Baños-Bayardo C. R., Díaz-Ramírez D., Marsch-Martínez N., De Folter S. (2018). Conserved and novel responses to cytokinin treatments during flower and fruit development in Brassica napus and Arabidopsis thaliana. Sci. Rep. 8:6836. 10.1038/s41598-018-25017-3 PubMed DOI PMC
Zúñiga-Mayo V. M., Gómez-Felipe A., Herrera-Ubaldo H., De Folter S. (2019). Gynoecium development: networks in Arabidopsis and beyond. J. Exp. Bot. 70 1447–1460. 10.1093/jxb/erz026 PubMed DOI