Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the <it>Schizosaccharomyces pombe </it>mitotic inducer, <it>cdc25</it>

<p>Abstract</p> <p>Background</p> <p>Entry into mitosis is regulated by cyclin dependent kinases that in turn are phosphoregulated. In most eukaryotes, phosphoregulation is through WEE1 kinase and CDC25 phosphatase. In higher plants a homologous CDC25 gene is unconfirme...

Full description

Bibliographic Details
Main Authors: Spadafora Natasha D, Parfitt David, Marchbank Angela, Li Sherong, Bruno Leonardo, Vaughan Rhys, Nieuwland Jeroen, Buchanan-Wollaston Vicky, Herbert Robert J, Bitonti Maria, Doonan John, Albani Diego, Prinsen Els, Francis Dennis, Rogers Hilary J
Format: Article
Language:English
Published: BMC 2012-03-01
Series:BMC Plant Biology
Online Access:http://www.biomedcentral.com/1471-2229/12/45
_version_ 1818664290132951040
author Spadafora Natasha D
Parfitt David
Marchbank Angela
Li Sherong
Bruno Leonardo
Vaughan Rhys
Nieuwland Jeroen
Buchanan-Wollaston Vicky
Herbert Robert J
Bitonti Maria
Doonan John
Albani Diego
Prinsen Els
Francis Dennis
Rogers Hilary J
author_facet Spadafora Natasha D
Parfitt David
Marchbank Angela
Li Sherong
Bruno Leonardo
Vaughan Rhys
Nieuwland Jeroen
Buchanan-Wollaston Vicky
Herbert Robert J
Bitonti Maria
Doonan John
Albani Diego
Prinsen Els
Francis Dennis
Rogers Hilary J
author_sort Spadafora Natasha D
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>Entry into mitosis is regulated by cyclin dependent kinases that in turn are phosphoregulated. In most eukaryotes, phosphoregulation is through WEE1 kinase and CDC25 phosphatase. In higher plants a homologous CDC25 gene is unconfirmed and hence the mitotic inducer <it>Schizosaccharomyces pombe </it>(<it>Sp</it>) <it>cdc25 </it>has been used as a tool in transgenic plants to probe cell cycle function. Expression of <it>Spcdc25 </it>in tobacco BY-2 cells accelerates entry into mitosis and depletes cytokinins; in whole plants it stimulates lateral root production. Here we show, for the first time, that alterations to cytokinin and ethylene signaling explain the rooting phenotype elicited by <it>Spcdc25 </it>expression in Arabidopsis.</p> <p>Results</p> <p>Expressing <it>Spcdc25 </it>in Arabidopsis results in increased formation of lateral and adventitious roots, a reduction of primary root width and more isodiametric cells in the root apical meristem (RAM) compared with wild type. Furthermore it stimulates root morphogenesis from hypocotyls when cultured on two way grids of increasing auxin and cytokinin concentrations. Microarray analysis of seedling roots expressing <it>Spcdc25 </it>reveals that expression of 167 genes is changed by > 2-fold. As well as genes related to stress responses and defence, these include 19 genes related to transcriptional regulation and signaling. Amongst these was the up-regulation of genes associated with ethylene synthesis and signaling. Seedlings expressing <it>Spcdc25 </it>produced 2-fold more ethylene than WT and exhibited a significant reduction in hypocotyl length both in darkness or when exposed to 10 ppm ethylene. Furthermore in <it>Spcdc25 </it>expressing plants, the cytokinin receptor <it>AHK3 </it>was down-regulated, and endogenous levels of iPA were reduced whereas endogeous IAA concentrations in the roots increased.</p> <p>Conclusions</p> <p>We suggest that the reduction in root width and change to a more isodiametric cell phenotype in the RAM in <it>Spcdc25 </it>expressing plants is a response to ethylene over-production. The increased rooting phenotype in <it>Spcdc25 </it>expressing plants is due to an increase in the ratio of endogenous auxin to cytokinin that is known to stimulate an increased rate of lateral root production. Overall, our data reveal important cross talk between cell division and plant growth regulators leading to developmental changes.</p>
first_indexed 2024-12-17T05:30:23Z
format Article
id doaj.art-943615e4ec4d402baf23cb8270101565
institution Directory Open Access Journal
issn 1471-2229
language English
last_indexed 2024-12-17T05:30:23Z
publishDate 2012-03-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj.art-943615e4ec4d402baf23cb82701015652022-12-21T22:01:45ZengBMCBMC Plant Biology1471-22292012-03-011214510.1186/1471-2229-12-45Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the <it>Schizosaccharomyces pombe </it>mitotic inducer, <it>cdc25</it>Spadafora Natasha DParfitt DavidMarchbank AngelaLi SherongBruno LeonardoVaughan RhysNieuwland JeroenBuchanan-Wollaston VickyHerbert Robert JBitonti MariaDoonan JohnAlbani DiegoPrinsen ElsFrancis DennisRogers Hilary J<p>Abstract</p> <p>Background</p> <p>Entry into mitosis is regulated by cyclin dependent kinases that in turn are phosphoregulated. In most eukaryotes, phosphoregulation is through WEE1 kinase and CDC25 phosphatase. In higher plants a homologous CDC25 gene is unconfirmed and hence the mitotic inducer <it>Schizosaccharomyces pombe </it>(<it>Sp</it>) <it>cdc25 </it>has been used as a tool in transgenic plants to probe cell cycle function. Expression of <it>Spcdc25 </it>in tobacco BY-2 cells accelerates entry into mitosis and depletes cytokinins; in whole plants it stimulates lateral root production. Here we show, for the first time, that alterations to cytokinin and ethylene signaling explain the rooting phenotype elicited by <it>Spcdc25 </it>expression in Arabidopsis.</p> <p>Results</p> <p>Expressing <it>Spcdc25 </it>in Arabidopsis results in increased formation of lateral and adventitious roots, a reduction of primary root width and more isodiametric cells in the root apical meristem (RAM) compared with wild type. Furthermore it stimulates root morphogenesis from hypocotyls when cultured on two way grids of increasing auxin and cytokinin concentrations. Microarray analysis of seedling roots expressing <it>Spcdc25 </it>reveals that expression of 167 genes is changed by > 2-fold. As well as genes related to stress responses and defence, these include 19 genes related to transcriptional regulation and signaling. Amongst these was the up-regulation of genes associated with ethylene synthesis and signaling. Seedlings expressing <it>Spcdc25 </it>produced 2-fold more ethylene than WT and exhibited a significant reduction in hypocotyl length both in darkness or when exposed to 10 ppm ethylene. Furthermore in <it>Spcdc25 </it>expressing plants, the cytokinin receptor <it>AHK3 </it>was down-regulated, and endogenous levels of iPA were reduced whereas endogeous IAA concentrations in the roots increased.</p> <p>Conclusions</p> <p>We suggest that the reduction in root width and change to a more isodiametric cell phenotype in the RAM in <it>Spcdc25 </it>expressing plants is a response to ethylene over-production. The increased rooting phenotype in <it>Spcdc25 </it>expressing plants is due to an increase in the ratio of endogenous auxin to cytokinin that is known to stimulate an increased rate of lateral root production. Overall, our data reveal important cross talk between cell division and plant growth regulators leading to developmental changes.</p>http://www.biomedcentral.com/1471-2229/12/45
spellingShingle Spadafora Natasha D
Parfitt David
Marchbank Angela
Li Sherong
Bruno Leonardo
Vaughan Rhys
Nieuwland Jeroen
Buchanan-Wollaston Vicky
Herbert Robert J
Bitonti Maria
Doonan John
Albani Diego
Prinsen Els
Francis Dennis
Rogers Hilary J
Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the <it>Schizosaccharomyces pombe </it>mitotic inducer, <it>cdc25</it>
BMC Plant Biology
title Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the <it>Schizosaccharomyces pombe </it>mitotic inducer, <it>cdc25</it>
title_full Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the <it>Schizosaccharomyces pombe </it>mitotic inducer, <it>cdc25</it>
title_fullStr Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the <it>Schizosaccharomyces pombe </it>mitotic inducer, <it>cdc25</it>
title_full_unstemmed Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the <it>Schizosaccharomyces pombe </it>mitotic inducer, <it>cdc25</it>
title_short Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the <it>Schizosaccharomyces pombe </it>mitotic inducer, <it>cdc25</it>
title_sort perturbation of cytokinin and ethylene signalling pathways explain the strong rooting phenotype exhibited by arabidopsis expressing the it schizosaccharomyces pombe it mitotic inducer it cdc25 it
url http://www.biomedcentral.com/1471-2229/12/45
work_keys_str_mv AT spadaforanatashad perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT parfittdavid perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT marchbankangela perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT lisherong perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT brunoleonardo perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT vaughanrhys perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT nieuwlandjeroen perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT buchananwollastonvicky perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT herbertrobertj perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT bitontimaria perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT doonanjohn perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT albanidiego perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT prinsenels perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT francisdennis perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it
AT rogershilaryj perturbationofcytokininandethylenesignallingpathwaysexplainthestrongrootingphenotypeexhibitedbyarabidopsisexpressingtheitschizosaccharomycespombeitmitoticinduceritcdc25it