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The E3 ubiquitin ligase HOS1 is involved in ethylene regulation of leaf expansion in Arabidopsis a
ab
Kyounghee Lee & Pil Joon Seo a
Department of Bioactive Material Sciences and Research Center of Bioactive Materials; Chonbuk National University, Jeonju, Korea b
Department of Chemistry and Research Institute of Physics and Chemistry; Chonbuk National University, Jeonju, Korea Accepted author version posted online: 07 Apr 2015.
Click for updates To cite this article: Kyounghee Lee & Pil Joon Seo (2015) The E3 ubiquitin ligase HOS1 is involved in ethylene regulation of leaf expansion in Arabidopsis, Plant Signaling & Behavior, 10:3, e1003755 To link to this article: http://dx.doi.org/10.1080/15592324.2014.1003755
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
SHORT COMMUNICATION Plant Signaling & Behavior 10:3, e1003755; March 2015; Copyright © Taylor & Francis Group, LLC
The E3 ubiquitin ligase HOS1 is involved in ethylene regulation of leaf expansion in Arabidopsis Kyounghee Lee1 and Pil Joon Seo1,2,* 1
Department of Bioactive Material Sciences and Research Center of Bioactive Materials; Chonbuk National University, Jeonju, Korea; 2 Department of Chemistry and Research Institute of Physics and Chemistry; Chonbuk National University, Jeonju, Korea
Keywords: Arabidopsis, ethylene, HOS1, leaf expansion
Downloaded by [University of Sherbrooke] at 08:58 04 May 2015
Abbreviations: CTR1, CONSTITUTIVE TRIPLE RESPONSE 1; EIN, ETHYLENE INSENSITIVE; ERF, ETHYLENERESPONSE FACTOR; ERS, ETHYLENE RESPONSE SENSOR; ESE1, ETHYLENE AND SALT INDUCIBLE 1; ETR, ETHYLENE RECEPTOR; HOS1, HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 1; STS, silver thiosulfate
Ethylene regulates a variety of physiological processes, such as flowering, senescence, abscission, and fruit ripening. In particular, leaf expansion is also controlled by ethylene in Arabidopsis. Exogenous treatment with ethylene inhibits leaf expansion, and consistently, ethylene insensitive mutants show increased leaf area. Here, we report that the RING finger-containing E3 ubiquitin ligase HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 1 (HOS1) regulates leaf expansion in an ethylene signaling pathway. The HOS1-deficient mutant showed reduced leaf area and was insensitive to ethylene perception inhibitor, silver thiosulfate (STS). Accordingly, genes encoding ethylene signaling components were significantly up-regulated in hos1-3. This study demonstrates that the HOS1 protein is involved in ethylene signal transduction for the proper regulation of leaf expansion possibly under environmentally stressful conditions.
Leaf expansion is a crucial process that not only determines the shape and size of mature leaves but also ensures its photosynthetic capacity for plant growth and development.1,2 It is influenced by multiplicity of environmental factors, such as water availability and day length.3,4 In addition, endogenous hormone signaling is also intensively involved in the control of leaf expansion. Promotive roles of auxin, brassinosteroid, and gibberellin in leaf expansion have been demonstrated.5-7 The simple hydrocarbon ethylene is a gaseous plant hormone that regulates a variety of developmental processes, such as seed germination, cell elongation, abscission, senescence, sex determination, and fruit ripening.8-13 It has been also proposed that ethylene negatively regulates leaf expansion process. Exogenous ethylene treatment results in reduced leaf area.14 Furthermore, ethylene insensitive mutants, such as ethylene receptor 1 (etr1) and ethylene response sensor 1 (ers1), show increased leaf size.15,16 Five receptor isoforms are responsible for ethylene perception: ETR1, ETR2, ERS1, ERS2, and ETHYLENE INSENSITIVE 4 (EIN4).17 Their ethylene perception is integrated into a negative regulator of ethylene signaling, CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1) Ser/Thr protein kinase,18 which in turn regulates a series of transcriptional cascades in order to control ethylene-dependent physiological processes. EIN2 is a representative positive signaling regulator and subsequently activates genes
encoding EIN3 and related EIN3-LIKE (EIL), which further regulate expression of ETHYLENE-RESPONSE FACTORs (ERFs).19,20 In the presence of ethylene, ethylene receptors inactivate kinase activity of CTR1 so that subsequent transcriptional cascades are activated.21 Although ethylene signaling pathways have been intensively investigated, its intricate networks with other signaling pathways remain to be unraveled. The RING-type E3 ligase HOS1 was originally reported as cold signaling attenuator.22 The cold-activated HOS1 protein executes protein turnover of the INDUCER OF CBF EXPRESSION1 (ICE1) MYC-like basic helix-loop-helix (bHLH) transcription factor,23,24 which activates the C-REPEAT BINDING FACTOR (CBF)-COLD-REGULATED (COR) pathway,23,25,26 indicating the homeostatic role in plant adaptation to long-term cold stress. In addition to its role in cold response, the HOS1 protein also mediates plant hormone signaling. For instance, HOS1 negatively regulates auxin biosynthesis in the control of hypocotyl elongation.27 It has been previously reported that hos1 mutants show reduced leaf area,28 although underlying molecular mechanism is elusive. Thus, we wanted to know how HOS1 regulates leaf expansion. We hypothesized that HOS1 is associated with ethylene signaling, because the hos1-3 mutant showed similar phenotypes in leaf expansion to the ctr1 mutant that exhibits constitutive ethylene responses.14
*Correspondence to: Pil Joon Seo; Email: [email protected] Submitted: 12/15/2014; Accepted: 12/20/2014 http://dx.doi.org/10.1080/15592324.2014.1003755
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Plant Signaling & Behavior
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Downloaded by [University of Sherbrooke] at 08:58 04 May 2015
require the copper ion for high-affinity ethylene binding.29 Silver can substitute for copper as a cofactor and thereby inhibit ethylene responses.30 In the presence of STS, wild-type plants showed increased leaf expansion as previously reported.31 However, the hos13 mutant was insensitive to STS and showed constitutively reduced leaf area (Fig. 1A and B). Quantitative analysis revealed that wild-type leaves exhibited approximately 4-fold increase in the leaf area upon the treatment with STS, whereas the hos1-3 mutant only showed 1.5-fold increase in its leave size (Fig. 1B). To convince the constitutive ethylFigure 1. The reduced leaf expansion of hos1-3 is insensitive to STS. The effects of 10 mM STS on leaf ene response in hos1-3, we analyzed expansion were examined using Arabidopsis wild-type (Columbia-0; Col-0) and hos1-3 seedlings. Bioexpression of ethylene signaling genes, logical triplicates were averaged and statistically analyzed by Student’s t-test (*P < 0.05). Bars indicate such as EIN3 and ETHYLENE AND standard error of the mean. SALT INDUCIBLE 1 (ESE1), in wildtype and hos1-3 seedlings. Consistent with its leaf expansion, ethyleneTo investigate whether alterations in ethylene signaling under- responsive genes were significantly upregulated in hos1-3 lie reduced leaf expansion of hos1-3, we employed a chemical (Fig. 2), indicating that HOS1 negatively regulates ethylene inhibitor of ethylene receptors, STS. The ethylene receptors signaling. Ethylene regulates leaf expansion largely through cell expansion.15 Ethylene-insensitive ers1 mutant shows increased cell expansion in leaf epidermal cells,15 whereas the ctr1 mutation
Figure 2. Ethylene signaling genes are up-regulated in hos1-3 mutant. Ten-day-old seedlings grown under long day conditions were used to analyze expression of genes encoding ethylene signaling components. Transcript accumulation was analyzed by quantitative RT-PCR (RT-qPCR). The EUKARYOTIC TRANSLATION INITIATION FACTOR 4A1 (eIF4a) gene (At3g13920) was used as an internal control. Biological triplicates were averaged and statistically analyzed by Student’s t-test (*P
Plant Signaling & Behavior Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/kpsb20
The E3 ubiquitin ligase HOS1 is involved in ethylene regulation of leaf expansion in Arabidopsis a
ab
Kyounghee Lee & Pil Joon Seo a
Department of Bioactive Material Sciences and Research Center of Bioactive Materials; Chonbuk National University, Jeonju, Korea b
Department of Chemistry and Research Institute of Physics and Chemistry; Chonbuk National University, Jeonju, Korea Accepted author version posted online: 07 Apr 2015.
Click for updates To cite this article: Kyounghee Lee & Pil Joon Seo (2015) The E3 ubiquitin ligase HOS1 is involved in ethylene regulation of leaf expansion in Arabidopsis, Plant Signaling & Behavior, 10:3, e1003755 To link to this article: http://dx.doi.org/10.1080/15592324.2014.1003755
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
SHORT COMMUNICATION Plant Signaling & Behavior 10:3, e1003755; March 2015; Copyright © Taylor & Francis Group, LLC
The E3 ubiquitin ligase HOS1 is involved in ethylene regulation of leaf expansion in Arabidopsis Kyounghee Lee1 and Pil Joon Seo1,2,* 1
Department of Bioactive Material Sciences and Research Center of Bioactive Materials; Chonbuk National University, Jeonju, Korea; 2 Department of Chemistry and Research Institute of Physics and Chemistry; Chonbuk National University, Jeonju, Korea
Keywords: Arabidopsis, ethylene, HOS1, leaf expansion
Downloaded by [University of Sherbrooke] at 08:58 04 May 2015
Abbreviations: CTR1, CONSTITUTIVE TRIPLE RESPONSE 1; EIN, ETHYLENE INSENSITIVE; ERF, ETHYLENERESPONSE FACTOR; ERS, ETHYLENE RESPONSE SENSOR; ESE1, ETHYLENE AND SALT INDUCIBLE 1; ETR, ETHYLENE RECEPTOR; HOS1, HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 1; STS, silver thiosulfate
Ethylene regulates a variety of physiological processes, such as flowering, senescence, abscission, and fruit ripening. In particular, leaf expansion is also controlled by ethylene in Arabidopsis. Exogenous treatment with ethylene inhibits leaf expansion, and consistently, ethylene insensitive mutants show increased leaf area. Here, we report that the RING finger-containing E3 ubiquitin ligase HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 1 (HOS1) regulates leaf expansion in an ethylene signaling pathway. The HOS1-deficient mutant showed reduced leaf area and was insensitive to ethylene perception inhibitor, silver thiosulfate (STS). Accordingly, genes encoding ethylene signaling components were significantly up-regulated in hos1-3. This study demonstrates that the HOS1 protein is involved in ethylene signal transduction for the proper regulation of leaf expansion possibly under environmentally stressful conditions.
Leaf expansion is a crucial process that not only determines the shape and size of mature leaves but also ensures its photosynthetic capacity for plant growth and development.1,2 It is influenced by multiplicity of environmental factors, such as water availability and day length.3,4 In addition, endogenous hormone signaling is also intensively involved in the control of leaf expansion. Promotive roles of auxin, brassinosteroid, and gibberellin in leaf expansion have been demonstrated.5-7 The simple hydrocarbon ethylene is a gaseous plant hormone that regulates a variety of developmental processes, such as seed germination, cell elongation, abscission, senescence, sex determination, and fruit ripening.8-13 It has been also proposed that ethylene negatively regulates leaf expansion process. Exogenous ethylene treatment results in reduced leaf area.14 Furthermore, ethylene insensitive mutants, such as ethylene receptor 1 (etr1) and ethylene response sensor 1 (ers1), show increased leaf size.15,16 Five receptor isoforms are responsible for ethylene perception: ETR1, ETR2, ERS1, ERS2, and ETHYLENE INSENSITIVE 4 (EIN4).17 Their ethylene perception is integrated into a negative regulator of ethylene signaling, CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1) Ser/Thr protein kinase,18 which in turn regulates a series of transcriptional cascades in order to control ethylene-dependent physiological processes. EIN2 is a representative positive signaling regulator and subsequently activates genes
encoding EIN3 and related EIN3-LIKE (EIL), which further regulate expression of ETHYLENE-RESPONSE FACTORs (ERFs).19,20 In the presence of ethylene, ethylene receptors inactivate kinase activity of CTR1 so that subsequent transcriptional cascades are activated.21 Although ethylene signaling pathways have been intensively investigated, its intricate networks with other signaling pathways remain to be unraveled. The RING-type E3 ligase HOS1 was originally reported as cold signaling attenuator.22 The cold-activated HOS1 protein executes protein turnover of the INDUCER OF CBF EXPRESSION1 (ICE1) MYC-like basic helix-loop-helix (bHLH) transcription factor,23,24 which activates the C-REPEAT BINDING FACTOR (CBF)-COLD-REGULATED (COR) pathway,23,25,26 indicating the homeostatic role in plant adaptation to long-term cold stress. In addition to its role in cold response, the HOS1 protein also mediates plant hormone signaling. For instance, HOS1 negatively regulates auxin biosynthesis in the control of hypocotyl elongation.27 It has been previously reported that hos1 mutants show reduced leaf area,28 although underlying molecular mechanism is elusive. Thus, we wanted to know how HOS1 regulates leaf expansion. We hypothesized that HOS1 is associated with ethylene signaling, because the hos1-3 mutant showed similar phenotypes in leaf expansion to the ctr1 mutant that exhibits constitutive ethylene responses.14
*Correspondence to: Pil Joon Seo; Email: [email protected] Submitted: 12/15/2014; Accepted: 12/20/2014 http://dx.doi.org/10.1080/15592324.2014.1003755
www.tandfonline.com
Plant Signaling & Behavior
e1003755-1
Downloaded by [University of Sherbrooke] at 08:58 04 May 2015
require the copper ion for high-affinity ethylene binding.29 Silver can substitute for copper as a cofactor and thereby inhibit ethylene responses.30 In the presence of STS, wild-type plants showed increased leaf expansion as previously reported.31 However, the hos13 mutant was insensitive to STS and showed constitutively reduced leaf area (Fig. 1A and B). Quantitative analysis revealed that wild-type leaves exhibited approximately 4-fold increase in the leaf area upon the treatment with STS, whereas the hos1-3 mutant only showed 1.5-fold increase in its leave size (Fig. 1B). To convince the constitutive ethylFigure 1. The reduced leaf expansion of hos1-3 is insensitive to STS. The effects of 10 mM STS on leaf ene response in hos1-3, we analyzed expansion were examined using Arabidopsis wild-type (Columbia-0; Col-0) and hos1-3 seedlings. Bioexpression of ethylene signaling genes, logical triplicates were averaged and statistically analyzed by Student’s t-test (*P < 0.05). Bars indicate such as EIN3 and ETHYLENE AND standard error of the mean. SALT INDUCIBLE 1 (ESE1), in wildtype and hos1-3 seedlings. Consistent with its leaf expansion, ethyleneTo investigate whether alterations in ethylene signaling under- responsive genes were significantly upregulated in hos1-3 lie reduced leaf expansion of hos1-3, we employed a chemical (Fig. 2), indicating that HOS1 negatively regulates ethylene inhibitor of ethylene receptors, STS. The ethylene receptors signaling. Ethylene regulates leaf expansion largely through cell expansion.15 Ethylene-insensitive ers1 mutant shows increased cell expansion in leaf epidermal cells,15 whereas the ctr1 mutation
Figure 2. Ethylene signaling genes are up-regulated in hos1-3 mutant. Ten-day-old seedlings grown under long day conditions were used to analyze expression of genes encoding ethylene signaling components. Transcript accumulation was analyzed by quantitative RT-PCR (RT-qPCR). The EUKARYOTIC TRANSLATION INITIATION FACTOR 4A1 (eIF4a) gene (At3g13920) was used as an internal control. Biological triplicates were averaged and statistically analyzed by Student’s t-test (*P
