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Cytokinin Regulates Root Meristem Activity Via Modulation of the Polar Auxin Transport

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Cytokinin Regulates Root Meristem Activity Via Modulation of the Polar Auxin Transport Cytokinin regulates root meristem activity via modulation of the polar auxin transport Kamil Ru˚ zˇicˇkaa,1,Ma´ ria Simaˇ ´ sˇkova´ a, Jerome Duclercqa, Jan Petra´ sˇekb,c, Eva Zažímalova´ b, Sibu Simonb,d, Jirˇí Frimla,e, Marc C. E. Van Montagua,2, and Eva Benkova´ a,e,2 aDepartment of Plant Systems Biology, VIB, and Department of Plant Biotechnology and Genetics, Gent University, Technologiepark 927, 9052 Gent, Belgium; bInstitute of Experimental Botany, Rozvojova´263, 16502 Prague, Czech Republic; cDepartment of Plant Physiology, Faculty of Science, Charles University, Vinicˇna´ 5, 12844 Prague 2, Czech Republic; eLaboratory of Molecular Plant Physiology, Department of Functional Genomics and Proteomics, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic; and dDepartment of Biochemistry, Faculty of Science, Charles University, Hlavova 2030, 12840 Prague 2, Czech Republic Contributed by Marc C. E. Van Montagu, January 9, 2009 (sent for review November 26, 2008) Plant development is governed by signaling molecules called FERASE (IPT) gene (17, 18) inhibits the root growth and phytohormones. Typically, in certain developmental processes reduces the meristem size. Accordingly, decreased endogenous more than 1 hormone is implicated and, thus, coordination of their CK levels via overexpression of the CYTOKININ OXIDASE/ overlapping activities is crucial for correct plant development. DEHYDROGENASE (CKX) family genes have an opposite However, molecular mechanisms underlying the hormonal effect, i.e., enhanced meristem and root growth (19). crosstalk are only poorly understood. Multiple hormones including CK seems to play an important role already in the early events cytokinin and auxin have been implicated in the regulation of root of root specification, because lack of the ARR7, and ARR15 development. Here we dissect the roles of cytokinin in modulating components of the CK signaling pathway causes defects in the growth of the primary root. We show that cytokinin effect on root establishment of the root stem cell niche during embryogenesis elongation occurs through ethylene signaling whereas cytokinin (20). Postembryonically in the root meristem, CK does not seem effect on the root meristem size involves ethylene-independent to interfere with specification of the quiescent center (QC) and modulation of transport-dependent asymmetric auxin distribu- stem cell function, or with the overall division rate, but affects tion. Exogenous or endogenous modification of cytokinin levels mainly the meristematic cell differentiation rate, resulting in and cytokinin signaling lead to specific changes in transcription of shortening of the meristematic zone (4, 5). In addition, CK several auxin efflux carrier genes from the PIN family having a regulates elongation of cells leaving the root meristem (4). direct impact on auxin efflux from cultured cells and on auxin Although the interaction between auxin and CKs in control of distribution in the root apex. We propose a novel model for organogenesis has been known for years (the first information cytokinin action in regulating root growth: Cytokinin influences related to this phenomenon appeared decades ago) (21), the cell-to-cell auxin transport by modification of expression of several molecular mechanisms underlying the mutual coordination of auxin transport components and thus modulates auxin distribution the auxin and cytokinin action and the possible crosstalk of their important for regulation of activity and size of the root meristem. pathways in regulating root growth are so far not known. We reveal a unique mechanism of auxin–cytokinin interaction and auxin ͉ auxin transport ͉ cytokinin ͉ hormonal crosstalk ͉ root meristem show that CK regulates the cell-to-cell auxin transport by modulating transcription of several PIN auxin efflux carriers. lant hormones play a crucial role in regulating plant devel- We propose a model for regulation of the auxin–cytokinin Popment and the flexible shaping of the plant architecture in balance that is critical for root organogenesis. By modulating the response to variable environmental conditions. The final devel- auxin transport CK might control the auxin levels in root opmental and physiological output of the hormonal signaling in meristem cells and, thus, the ratio between auxin and CK. plants is the typical result of combined actions of several hormonal pathways. However, our knowledge of the mecha- Results and Discussion nisms involved in the hormonal crosstalk is still poor. The CK Effect on the Root Meristem Does Not Interfere with Ethylene- In the regulation of root development, several hormonal Mediated Processes. Root growth depends on the production of pathways are involved, with auxin and cytokinin being the new cells, their differentiation, and elongation. New cells are principal players. The whole process of root organogenesis, produced in the mitotically active meristem zone, whereas their starting with the initiation of the root pole in embryos (1), differentiation and elongation occur in the more proximal part positioning and formation of stem cell niche (2, 3), maintenance of the root tip. The plant hormone CK regulates the root of mitotic activity in proximal meristem (4–6), and rapid elon- meristem activity. Increase of CK levels either by exogenous gation and differentiation of cells leaving the root meristem (7) application of CK or overexpression of ISOPENTENYLTRANS- has been demonstrated to be controlled by auxin. In this context, FERASE (IPT), a gene involved in CK biosynthesis, reduces the the differential auxin distribution between cells is crucial (3, 8, size of root meristems and overall root growth (5) (supporting 9). The auxin gradients or local auxin maxima can be generated information (SI) Fig. S1C). On the contrary, plants overexpress- by auxin metabolic reactions, mainly by local auxin biosynthesis ing CYTOKININ OXIDASE/DEHYDROGENASE (CKX) caus- (6, 10, 11) and intercellular auxin transport dependent on the coordinated action of influx carriers of the AUX/LAX family (12), PIN efflux carriers (13, 14), and members of the multidrug- Author contributions: K.R., J.F., and E.B. designed research; K.R., M.S., J.D., J.P., E.Z., S.S., M.C.E.V.M., and E.B. performed research; K.R., M.S., J.D., J.P., E.Z., and E.B. analyzed data; resistant/P-glycoprotein (MDR/PGP) subfamily B of ATP- and J.F. and E.B. wrote the paper. binding cassette (ABCB) proteins (15, 16). Accordingly, inter- The authors declare no conflict of interest. ference with the polar auxin transport disrupts the auxin 1Present address: Institute of Biochemistry, University of Helsinki, FIN-00014, Helsinki, distribution and results in dramatic patterning defects in the root Finland. meristem (2, 3, 9). 2To whom correspondence may be addressed. E-mail: [email protected] or eva. Besides auxin, cytokinin (CK) is also involved in root orga- [email protected]. nogenesis. Increase in CK levels by exogenous application or This article contains supporting information online at www.pnas.org/cgi/content/full/ overexpression of the bacterial ISOPENTENYLTRANS- 0900060106/DCSupplemental. 4284–4289 ͉ PNAS ͉ March 17, 2009 ͉ vol. 106 ͉ no. 11 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0900060106 Downloaded by guest on September 30, 2021 -AVG +AVG 1,3 - -AVG +AVG col ein2 etr1-3 A B * C 120 1,2 1,6 * * * * 1,1 ** 100 * * * ** 1,4 * * * * 1 1,2 80 0,9 1 60 0,8 0,8 0,7 (cm) RL 0,6 40 0,6 0,4 20 RM reduction (%) 0,5 0,2 RM reduction (relative units) 0 0105010 50 100 0105010 50 100 0 50 100 nM BA nM BA nM BA D col ein2 etr1-3 E MS BA AVG BA AVG F 120 120 100 100 80 80 60 * 60 40 20 40 0 RL reduction (%) RL 20 * * * Relative fluorescence (%) BA MS 0 AVG 050100 AVG BA nM BA Fig. 1. Ethylene-independent root meristem size modulation by CK. (A) Reduction of ethylene biosynthesis by AVG without interference with CK effect on the root meristem size (no difference between CK-treated and CK ϩ AVG-treated root meristems; Student’s t test, P Ͼ 0.05). (B) CK-insensitive root growth at reduced ethylene biosynthesis conditions (*statistically significant difference in root length between CK and CK ϩ AVG-treated seedlings; Student’s t test P Ͻ 0.05). (C) Reduced root meristem in the ethylene signaling mutants etr1–3 and ein2 after CK treatment (*statistically significant difference in the root meristem size between CK-treated and -nontreated seedlings; Student’s t test, P Ͻ 0.05). (D) CK-resistant root growth of etr1–3 and ein2.(E) CK-induced ectopic expression of DR5::GFP reporter in outer layers of the root meristem (lateral root cap and epidermis; arrowheads). Reduction of ethylene biosynthesis by AVG diminishes the DR5 ectopic expression. CK-reduced DR5 expression in QC (asterisks). (F) Quantification of DR5::GFP expression by image analysis in QC of roots treated with CK and CK ϩ AVG; expression of DR5::GFP is significantly reduced after CK treatment under conditions of reduced ethylene biosynthesis (*statistically significant difference between AVG and CK ϩ AVG-treated roots, Student’s t test, P Ͻ 0.05). Six-day-old seedlings grown on media containing 100 nM BA, 200 nM AVG, (if not marked differently). RM, root meristem; RL, root length; MS, Murashige and Skoog medium only; CK represented by N6-benzyladenine (BA); col, control Columbia seedlings. Error bars represent standard deviation (SD). ing enhanced degradation of CK have longer root meristems (19) activity in the outer layers of the root meristem and the (Fig. S1C). elongation zone (Fig. 1E, data not shown). A similar change in Because CK stimulates ethylene biosynthesis (22) and ethyl- the pattern of the DR5 reporter expression has been demon- ene itself strongly affects root growth (23, 24), we first examined strated previously to be caused by ethylene (23, 24, 29). Indeed, which CK effects on the root growth are mediated by ethylene. reduced ethylene biosynthesis by AVG completely eliminated To address this issue, either CK-induced ethylene production this ectopic signal, indicating that CK upregulates DR5::GFP was eliminated with the ethylene biosynthesis inhibitor 2- expression in the elongation zone through ethylene (Fig.
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