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      Changes in transcription of cytokinin metabolism and signalling genes in grape ( Vitis vinifera L.) berries are associated with the ripening-related increase in isopentenyladenine

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          Abstract

          Background

          Cytokinins are known to play an important role in fruit set and early fruit growth, but their involvement in later stages of fruit development is less well understood. Recent reports of greatly increased cytokinin concentrations in the flesh of ripening kiwifruit ( Actinidia deliciosa (A. Chev.) C.F. Liang & A.R. Ferguson) and grapes ( Vitis vinifera L.) have suggested that these hormones are implicated in the control of ripening-related processes.

          Results

          A similar pattern of isopentenyladenine (iP) accumulation was observed in the ripening fruit of several grapevine cultivars, strawberry ( Fragaria ananassa Duch.) and tomato ( Solanum lycopersicum Mill.), suggesting a common, ripening-related role for this cytokinin. Significant differences in maximal iP concentrations between grapevine cultivars and between fruit species might reflect varying degrees of relevance or functional adaptations of this hormone in the ripening process. Grapevine orthologues of five Arabidopsis ( Arabidopsis thaliana L.) gene families involved in cytokinin metabolism and signalling were identified and analysed for their expression in developing grape berries and a range of other grapevine tissues. Members of each gene family were characterised by distinct expression profiles during berry development and in different grapevine organs, suggesting a complex regulation of cellular cytokinin activities throughout the plant. The post-veraison-specific expression of a set of biosynthesis, activation, perception and signalling genes together with a lack of expression of degradation-related genes during the ripening phase were indicative of a local control of berry iP concentrations leading to the observed accumulation of iP in ripening grapes.

          Conclusions

          The transcriptional analysis of grapevine genes involved in cytokinin production, degradation and response has provided a possible explanation for the ripening-associated accumulation of iP in grapes and other fruit. The pre- and post-veraison-specific expression of different members from each of five gene families suggests a highly complex and finely-tuned regulation of cytokinin concentrations and response to different cytokinin species at particular stages of fruit development. The same complexity and specialisation is also reflected in the distinct expression profiles of cytokinin-related genes in other grapevine organs.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12870-015-0611-5) contains supplementary material, which is available to authorized users.

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          Most cited references124

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          Cytokinin oxidase regulates rice grain production.

          Most agriculturally important traits are regulated by genes known as quantitative trait loci (QTLs) derived from natural allelic variations. We here show that a QTL that increases grain productivity in rice, Gn1a, is a gene for cytokinin oxidase/dehydrogenase (OsCKX2), an enzyme that degrades the phytohormone cytokinin. Reduced expression of OsCKX2 causes cytokinin accumulation in inflorescence meristems and increases the number of reproductive organs, resulting in enhanced grain yield. QTL pyramiding to combine loci for grain number and plant height in the same genetic background generated lines exhibiting both beneficial traits. These results provide a strategy for tailormade crop improvement.
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            Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.

            Cytokinins are hormones that regulate cell division and development. As a result of a lack of specific mutants and biochemical tools, it has not been possible to study the consequences of cytokinin deficiency. Cytokinin-deficient plants are expected to yield information about processes in which cytokinins are limiting and that, therefore, they might regulate. We have engineered transgenic Arabidopsis plants that overexpress individually six different members of the cytokinin oxidase/dehydrogenase (AtCKX) gene family and have undertaken a detailed phenotypic analysis. Transgenic plants had increased cytokinin breakdown (30 to 45% of wild-type cytokinin content) and reduced expression of the cytokinin reporter gene ARR5:GUS (beta-glucuronidase). Cytokinin deficiency resulted in diminished activity of the vegetative and floral shoot apical meristems and leaf primordia, indicating an absolute requirement for the hormone. By contrast, cytokinins are negative regulators of root growth and lateral root formation. We show that the increased growth of the primary root is linked to an enhanced meristematic cell number, suggesting that cytokinins control the exit of cells from the root meristem. Different AtCKX-green fluorescent protein fusion proteins were localized to the vacuoles or the endoplasmic reticulum and possibly to the extracellular space, indicating that subcellular compartmentation plays an important role in cytokinin biology. Analyses of promoter:GUS fusion genes showed differential expression of AtCKX genes during plant development, the activity being confined predominantly to zones of active growth. Our results are consistent with the hypothesis that cytokinins have central, but opposite, regulatory functions in root and shoot meristems and indicate that a fine-tuned control of catabolism plays an important role in ensuring the proper regulation of cytokinin functions.
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              Cytokinins: activity, biosynthesis, and translocation.

              Cytokinins (CKs) play a crucial role in various phases of plant growth and development, but the basic molecular mechanisms of their biosynthesis and signal transduction only recently became clear. The progress was achieved by identifying a series of key genes encoding enzymes and proteins controlling critical steps in biosynthesis, translocation, and signaling. Basic schemes for CK homeostasis and root/shoot communication at the whole-plant level can now be devised. This review summarizes recent findings on the relationship between CK structural variation and activity, distinct features in CK biosynthesis between higher plants and Agrobacterium infected plants, CK translocation at whole-plant and cellular levels, and CKs as signaling molecules for nutrient status via root-shoot communication.
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                Author and article information

                Contributors
                christine.bottcher@csiro.au
                crista.burbidge@csiro.au
                paul.boss@csiro.au
                christopher.davies@csiro.au
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                16 September 2015
                16 September 2015
                2015
                : 15
                : 223
                Affiliations
                CSIRO Agriculture Flagship, Waite Campus, WIC West Building, PMB2, Glen Osmond, South Australia 5064 Australia
                Article
                611
                10.1186/s12870-015-0611-5
                4573921
                26377914
                a3870566-dcb4-4c64-911b-d6bd8f2902e3
                © Böttcher et al. 2015

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 18 June 2015
                : 10 September 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Plant science & Botany
                cytokinins,isopentenyladenine,vitis vinifera,ripening
                Plant science & Botany
                cytokinins, isopentenyladenine, vitis vinifera, ripening

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