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      Antagonistic activity of auxin and cytokinin in shoot and root organs

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          Abstract

          The hormones auxin and cytokinin are essential for plant growth and development. Because of the central importance of root and shoot apical meristems in plant growth, auxin/cytokinin interactions have been predominantly analyzed in relation to apical meristem formation and function. In contrast, the auxin/cytokinin interactions during organ growth have remained largely unexplored. Here, we show that a specific interaction between auxin and cytokinin operates in both the root and the shoot where it serves as an additional determinant of plant development. We found that auxin at low concentrations limits the action of cytokinin. An increase in cytokinin level counteracts this inhibitory effect and leads to an inhibition of auxin signaling. At higher concentrations of both hormones, these antagonistic interactions between cytokinin and auxin are absent. Thus, our results reveal a bidirectional and asymmetrical interaction of auxin and cytokinin beyond the bounds of apical meristems. The relation is bidirectional in that both hormones exert inhibitory effects on each other's signaling mechanisms. However, this relation is also asymmetrical because under controlled growth conditions, auxin present in nontreated plants suppresses cytokinin signaling, whereas the reverse is not the case.

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          Most cited references32

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          Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism.

          We used loss-of-function mutants to study three Arabidopsis thaliana sensor histidine kinases, AHK2, AHK3, and CRE1/AHK4, known to be cytokinin receptors. Mutant seeds had more rapid germination, reduced requirement for light, and decreased far-red light sensitivity, unraveling cytokinin functions in seed germination control. Triple mutant seeds were more than twice as large as wild-type seeds. Genetic analysis indicated a cytokinin-dependent endospermal and/or maternal control of embryo size. Unchanged red light sensitivity of mutant hypocotyl elongation suggests that previously reported modulation of red light signaling by A-type response regulators may not depend on cytokinin. Combined loss of AHK2 and AHK3 led to the most prominent changes during vegetative development. Leaves of ahk2 ahk3 mutants formed fewer cells, had reduced chlorophyll content, and lacked the cytokinin-dependent inhibition of dark-induced chlorophyll loss, indicating a prominent role of AHK2 and, particularly, AHK3 in the control of leaf development. ahk2 ahk3 double mutants developed a strongly enhanced root system through faster growth of the primary root and, more importantly, increased branching. This result supports a negative regulatory role for cytokinin in root growth regulation. Increased cytokinin content of receptor mutants indicates a homeostatic control of steady state cytokinin levels through signaling. Together, the analyses reveal partially redundant functions of the cytokinin receptors and prominent roles for the AHK2/AHK3 receptor combination in quantitative control of organ growth in plants, with opposite regulatory functions in roots and shoots.
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            Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling.

            Type-A Arabidopsis (Arabidopsis thaliana) response regulators (ARRs) are a family of 10 genes that are rapidly induced by cytokinin and are highly similar to bacterial two-component response regulators. We have isolated T-DNA insertions in six of the type-A ARRs and constructed multiple insertional mutants, including the arr3,4,5,6,8,9 hextuple mutant. Single arr mutants were indistinguishable from the wild type in various cytokinin assays; double and higher order arr mutants showed progressively increasing sensitivity to cytokinin, indicating functional overlap among type-A ARRs and that these genes act as negative regulators of cytokinin responses. The induction of cytokinin primary response genes was amplified in arr mutants, indicating that the primary response to cytokinin is affected. Spatial patterns of ARR gene expression were consistent with partially redundant function of these genes in cytokinin signaling. The arr mutants show altered red light sensitivity, suggesting a general involvement of type-A ARRs in light signal transduction. Further, morphological phenotypes of some arr mutants suggest complex regulatory interactions and gene-specific functions among family members.
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              Cytokinins act directly on lateral root founder cells to inhibit root initiation.

              In Arabidopsis thaliana, lateral roots are formed from root pericycle cells adjacent to the xylem poles. Lateral root development is regulated antagonistically by the plant hormones auxin and cytokinin. While a great deal is known about how auxin promotes lateral root development, the mechanism of cytokinin repression is still unclear. Elevating cytokinin levels was observed to disrupt lateral root initiation and the regular pattern of divisions that characterizes lateral root development in Arabidopsis. To identify the stage of lateral root development that is sensitive to cytokinins, we targeted the expression of the Agrobacterium tumefaciens cytokinin biosynthesis enzyme isopentenyltransferase to either xylem-pole pericycle cells or young lateral root primordia using GAL4-GFP enhancer trap lines. Transactivation experiments revealed that xylem-pole pericycle cells are sensitive to cytokinins, whereas young lateral root primordia are not. This effect is physiologically significant because transactivation of the Arabidopsis cytokinin degrading enzyme cytokinin oxidase 1 in lateral root founder cells results in increased lateral root formation. We observed that cytokinins perturb the expression of PIN genes in lateral root founder cells and prevent the formation of an auxin gradient that is required to pattern lateral root primordia.
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                Author and article information

                Contributors
                jsmalle@uky.edu
                Journal
                Plant Direct
                Plant Direct
                10.1002/(ISSN)2475-4455
                PLD3
                Plant Direct
                John Wiley and Sons Inc. (Hoboken )
                2475-4455
                25 February 2019
                February 2019
                : 3
                : 2 ( doiID: 10.1002/pld3.2019.3.issue-2 )
                : e00121
                Affiliations
                [ 1 ] Department of Plant and Soil Sciences University of Kentucky Lexington Kentucky
                Author notes
                [*] [* ] Correspondence

                Jan A. Smalle, Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY.

                Email: jsmalle@ 123456uky.edu

                Article
                PLD3121
                10.1002/pld3.121
                6508789
                31245764
                57887a21-d92b-4a5c-93b4-71cf91cc3ce0
                © 2019 The Authors. Plant Direct published by American Society of Plant Biologists, Society for Experimental Biology and John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 31 October 2018
                : 31 January 2019
                : 08 February 2019
                Page count
                Figures: 4, Tables: 0, Pages: 9, Words: 6380
                Funding
                Funded by: USDA National Institute of Food and Agriculture
                Award ID: 1009329
                Funded by: National Science Foundation
                Award ID: IOS‐0919991
                Funded by: Kentucky Tobacco Research and Development Center
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                pld3121
                February 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.1 mode:remove_FC converted:27.03.2019

                apical meristems,auxin,cytokinin,hormonal antagonism,roots,shoots

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