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Tuominen, Hannele
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Wessels, B., Seyfferth, C., Escamez, S., Vain, T., Antos, K., Vahala, J., . . . Tuominen, H. (2019). An AP2/ERF transcription factor ERF139 coordinates xylem cell expansion and secondary cell wall deposition. New Phytologist
Open this publication in new window or tab >>An AP2/ERF transcription factor ERF139 coordinates xylem cell expansion and secondary cell wall deposition
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2019 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137Article in journal (Refereed) Epub ahead of print
Abstract [en]

Differentiation of xylem elements involves cell expansion, secondary cell wall (SCW) deposition and programmed cell death. Transitions between these phases require strict spatiotemporal control.

The function of Populus ERF139 (Potri.013G101100) in xylem differentiation was characterized in transgenic overexpression and dominant repressor lines of ERF139 in hybrid aspen (Populus tremula × tremuloides). Xylem properties, SCW chemistry and downstream targets were analyzed in both types of transgenic trees using microscopy techniques, Fourier transform‐infrared spectroscopy, pyrolysis‐GC/MS, wet chemistry methods and RNA sequencing.

Opposite phenotypes were observed in the secondary xylem vessel sizes and SCW chemistry in the two different types of transgenic trees, supporting the function of ERF139 in suppressing the radial expansion of vessel elements and stimulating accumulation of guaiacyl‐type lignin and possibly also xylan. Comparative transcriptomics identified genes related to SCW biosynthesis (LAC5, LBD15, MYB86) and salt and drought stress‐responsive genes (ANAC002, ABA1) as potential direct targets of ERF139.

The phenotypes of the transgenic trees and the stem expression profiles of ERF139potential target genes support the role of ERF139 as a transcriptional regulator of xylem cell expansion and SCW formation, possibly in response to osmotic changes of the cells.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2019
Keywords
cell expansion, ethylene response factor (ERF), hybrid aspen, lignin, Populus, secondary growth, xylem development
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-161696 (URN)10.1111/nph.15960 (DOI)000474107100001 ()31125440 (PubMedID)
Funder
Swedish Research Council Formas, 213-2011-1148Swedish Research Council Formas, 239-2011-1915The Kempe Foundations, SMK-1649The Kempe Foundations, SMK-1533Swedish Foundation for Strategic Research , RBP14-0011Knut and Alice Wallenberg Foundation, 2016-0341Bio4Energy
Available from: 2019-08-06 Created: 2019-08-06 Last updated: 2019-08-06
Seyfferth, C., Wessels, B. A., Gorzsás, A., Love, J. W., Rüggeberg, M., Delhomme, N., . . . Felten, J. (2019). Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen. Frontiers in Plant Science, 10, Article ID 1101.
Open this publication in new window or tab >>Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
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2019 (English)In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 10, article id 1101Article in journal (Refereed) Published
Abstract [en]

Tension wood (TW) in hybrid aspen trees forms on the upper side of displaced stems to generate a strain that leads to uplifting of the stem. TW is characterized by increased cambial growth, reduced vessel frequency and diameter, and the presence of gelatinous, cellulose-rich (G-)fibers with its microfibrils oriented parallel to the fiber cell axis. Knowledge remains limited about the molecular regulators required for the development of this special xylem tissue with its characteristic morphological, anatomical, and chemical features. In this study, we use transgenic, ethylene-insensitive (ETI) hybrid aspen trees together with time-lapse imaging to show that functional ethylene signaling is required for full uplifting of inclined stems. X-ray diffraction and Raman microspectroscopy of TW in ETI trees indicate that, although G-fibers form, the cellulose microfibril angle in the G-fiber S-layer is decreased, and the chemical composition of S- and G-layers is altered than in wild-type TW. The characteristic asymmetric growth and reduction of vessel density is suppressed during TW formation in ETI trees. A genome-wide transcriptome profiling reveals ethylene-dependent genes in TW, related to cell division, cell wall composition, vessel differentiation, microtubule orientation, and hormone crosstalk. Our results demonstrate that ethylene regulates transcriptional responses related to the amount of G-fiber formation and their properties (chemistry and cellulose microfibril angle) during TW formation. The quantitative and qualitative changes in G-fibers are likely to contribute to uplifting of stems that are displaced from their original position.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2019
Keywords
xylem, wood, ethylene, tension wood, lignin, microfibril angle, Raman microspectroscopy, transcriptomics
National Category
Forest Science
Identifiers
urn:nbn:se:umu:diva-164043 (URN)10.3389/fpls.2019.01101 (DOI)000487981600001 ()
Available from: 2019-10-15 Created: 2019-10-15 Last updated: 2019-10-15Bibliographically approved
Escamez, S., Stael, S., Vainonen, J. P., Willems, P., Jin, H., Kimura, S., . . . Tuominen, H. (2019). Extracellular peptide Kratos restricts cell death during vascular development and stress in Arabidopsis. Journal of Experimental Botany, 70(7), 2199-2210
Open this publication in new window or tab >>Extracellular peptide Kratos restricts cell death during vascular development and stress in Arabidopsis
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2019 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 70, no 7, p. 2199-2210Article in journal (Refereed) Published
Abstract [en]

During plant vascular development, xylem tracheary elements (TEs) form water-conducting, empty pipes by genetically regulated cell death. Cell death is prevented from spreading to non-TEs by unidentified intercellular mechanisms, downstream of METACASPASE9 (MC9)-mediated regulation of autophagy in TEs. Here, we identified differentially abundant extracellular peptides in vascular-differentiating wild-type and MC9-down-regulated Arabidopsis cell suspensions. A peptide named Kratos rescued the abnormally high ectopic non-TE death resulting from either MC9 knockout or TE-specific overexpression of the ATG5 autophagy protein during experimentally induced vascular differentiation in Arabidopsis cotyledons. Kratos also reduced cell death following mechanical damage and extracellular ROS production in Arabidopsis leaves. Stress-induced but not vascular non-TE cell death was enhanced by another identified peptide, named Bia. Bia is therefore reminiscent of several known plant cell death-inducing peptides acting as damage-associated molecular patterns. In contrast, Kratos plays a novel extracellular cell survival role in the context of development and during stress response.

Place, publisher, year, edition, pages
Oxford University Press, 2019
Keywords
Arabidopsis, autophagy, cell death, peptide, peptidomics, programmed cell death, stress response, vascular development, xylem
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-159631 (URN)10.1093/jxb/erz021 (DOI)000467901600018 ()30753577 (PubMedID)
Projects
Bio4Energy
Available from: 2019-06-10 Created: 2019-06-10 Last updated: 2019-08-30Bibliographically approved
Obudulu, O., Mähler, N., Skotare, T., Bygdell, J., Abreu, I. N., Ahnlund, M., . . . Tuominen, H. (2018). A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees. BMC Genomics, 19, Article ID 11.
Open this publication in new window or tab >>A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees
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2018 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 19, article id 11Article in journal (Refereed) Published
Abstract [en]

Background: Secretory Carrier-Associated Membrane Proteins (SCAMPs) are highly conserved 32–38 kDa proteins that are involved in membrane trafficking. A systems approach was taken to elucidate function of SCAMPs in wood formation of Populus trees. Phenotypic and multi-omics analyses were performed in woody tissues of transgenic Populus trees carrying an RNAi construct for Populus tremula x tremuloides SCAMP3 (PttSCAMP3;Potri.019G104000).

Results: The woody tissues of the transgenic trees displayed increased amounts of both polysaccharides and lignin oligomers, indicating increased deposition of both the carbohydrate and lignin components of the secondary cell walls. This coincided with a tendency towards increased wood density as well as significantly increased thickness of the suberized cork in the transgenic lines. Multivariate OnPLS (orthogonal projections to latent structures) modeling of five different omics datasets (the transcriptome, proteome, GC-MS metabolome, LC-MS metabolome and pyrolysis-GC/MS metabolome) collected from the secondary xylem tissues of the stem revealed systemic variation in the different variables in the transgenic lines, including changes that correlated with the changes in the secondary cell wall composition. The OnPLS model also identified a rather large number of proteins that were more abundant in the transgenic lines than in the wild type. Several of these were related to secretion and/or endocytosis as well as both primary and secondary cell wall biosynthesis.

Conclusions: Populus SCAMP proteins were shown to influence accumulation of secondary cell wall components, including polysaccharides and phenolic compounds, in the woody tissues of Populus tree stems. Our multi-omics analyses combined with the OnPLS modelling suggest that this function is mediated by changes in membrane trafficking to fine-tune the abundance of cell wall precursors and/or proteins involved in cell wall biosynthesis and transport. The data provides a multi-level source of information for future studies on the function of the SCAMP proteins in plant stem tissues.

Place, publisher, year, edition, pages
Springer Publishing Company, 2018
Keywords
Secretory Carrier-Associated Membrane Protein (SCAMP), Populus, Wood chemistry, Wood density, Biomass, Bioprocessing, Cork, Multi-omics
National Category
Cell Biology
Identifiers
urn:nbn:se:umu:diva-143890 (URN)10.1186/s12864-017-4411-1 (DOI)000419232000004 ()
Projects
Bio4Energy
Funder
Swedish Research Council Formas, 232-2009-1698
Available from: 2018-01-12 Created: 2018-01-12 Last updated: 2019-08-30Bibliographically approved
Seyfferth, C., Wessels, B., Jokipii-Lukkari, S., Sundberg, B., Delhomme, N., Felten, J. & Tuominen, H. (2018). Ethylene-Related Gene Expression Networks in Wood Formation. Frontiers in Plant Science, 9, Article ID 272.
Open this publication in new window or tab >>Ethylene-Related Gene Expression Networks in Wood Formation
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2018 (English)In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 9, article id 272Article in journal (Refereed) Published
Abstract [en]

Thickening of tree stems is the result of secondary growth, accomplished by the meristematic activity of the vascular cambium. Secondary growth of the stem entails developmental cascades resulting in the formation of secondary phloem outwards and secondary xylem (i.e., wood) inwards of the stem. Signaling and transcriptional reprogramming by the phytohormone ethylene modifies cambial growth and cell differentiation, but the molecular link between ethylene and secondary growth remains unknown. We addressed this shortcoming by analyzing expression profiles and co-expression networks of ethylene pathway genes using the AspWood transcriptome database which covers all stages of secondary growth in aspen (Populus tremula) stems. ACC synthase expression suggests that the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is synthesized during xylem expansion and xylem cell maturation. Ethylene-mediated transcriptional reprogramming occurs during all stages of secondary growth, as deduced from AspWood expression profiles of ethylene-responsive genes. A network centrality analysis of the AspWood dataset identified EIN3D and 11 ERFs as hubs. No overlap was found between the co-expressed genes of the EIN3 and ERF hubs, suggesting target diversification and hence independent roles for these transcription factor families during normal wood formation. The EIN3D hub was part of a large co-expression gene module, which contained 16 transcription factors, among them several new candidates that have not been earlier connected to wood formation and a VND-INTERACTING 2 (VNI2) homolog. We experimentally demonstrated Populus EIN3D function in ethylene signaling in Arabidopsis thaliana. The ERF hubs ERF118 and ERF119 were connected on the basis of their expression pattern and gene co-expression module composition to xylem cell expansion and secondary cell wall formation, respectively. We hereby establish data resources for ethylene-responsive genes and potential targets for EIN3D and ERF transcription factors in Populus stem tissues, which can help to understand the range of ethylene targeted biological processes during secondary growth.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2018
Keywords
ethylene signaling, secondary growth, wood development, co-expression network, EIN3, ERF
National Category
Bioinformatics and Systems Biology
Identifiers
urn:nbn:se:umu:diva-146209 (URN)10.3389/fpls.2018.00272 (DOI)000427359000001 ()29593753 (PubMedID)
Projects
Bio4Energy
Available from: 2018-05-14 Created: 2018-05-14 Last updated: 2019-09-06Bibliographically approved
Bollhöner, B., Jokipii-Lukkari, S., Bygdell, J., Stael, S., Adriasola, M., Muñiz, L., . . . Tuominen, H. (2018). The function of two type II metacaspases in woody tissues of Populus trees. New Phytologist, 217(4), 1551-1565
Open this publication in new window or tab >>The function of two type II metacaspases in woody tissues of Populus trees
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2018 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 217, no 4, p. 1551-1565Article in journal (Refereed) Published
Abstract [en]

Metacaspases (MCs) are cysteine proteases that are implicated in programmed cell death of plants. AtMC9 (Arabidopsis thaliana Metacaspase9) is a member of the Arabidopsis MC family that controls the rapid autolysis of the xylem vessel elements, but its downstream targets in xylem remain uncharacterized. PttMC13 and PttMC14 were identified as AtMC9 homologs in hybrid aspen (Populustremulaxtremuloides). A proteomic analysis was conducted in xylem tissues of transgenic hybrid aspen trees which carried either an overexpression or an RNA interference construct for PttMC13 and PttMC14. The proteomic analysis revealed modulation of levels of both previously known targets of metacaspases, such as Tudor staphylococcal nuclease, heat shock proteins and 14-3-3 proteins, as well as novel proteins, such as homologs of the PUTATIVE ASPARTIC PROTEASE3 (PASPA3) and the cysteine protease RD21 by PttMC13 and PttMC14. We identified here the pathways and processes that are modulated by PttMC13 and PttMC14 in xylem tissues. In particular, the results indicate involvement of PttMC13 and/or PttMC14 in downstream proteolytic processes and cell death of xylem elements. This work provides a valuable reference dataset on xylem-specific metacaspase functions for future functional and biochemical analyses.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2018
Keywords
aspartic protease, cellular autolysis, cysteine protease, metacaspase, Populus, programmed cell ath, wood formation, xylem differentiation
National Category
Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-145132 (URN)10.1111/nph.14945 (DOI)000424284400017 ()29243818 (PubMedID)
Projects
Bio4Energy
Available from: 2018-03-05 Created: 2018-03-05 Last updated: 2019-08-30Bibliographically approved
Jokipii-Lukkari, S., Delhomme, N., Schiffthaler, B., Mannapperuma, C., Prestele, J., Nilsson, O., . . . Tuominen, H. (2018). Transcriptional Roadmap to Seasonal Variation in Wood Formation of Norway Spruce. Plant Physiology, 176(4), 2851-2870
Open this publication in new window or tab >>Transcriptional Roadmap to Seasonal Variation in Wood Formation of Norway Spruce
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2018 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 176, no 4, p. 2851-2870Article in journal (Refereed) Published
Abstract [en]

Seasonal cues influence several aspects of the secondary growth of tree stems, including cambial activity, wood chemistry, and transition to latewood formation. We investigated seasonal changes in cambial activity, secondary cell wall formation, and tracheid cell death in woody tissues of Norway spruce (Picea abies) throughout one seasonal cycle. RNA sequencing was performed simultaneously in both the xylem and cambium/phloem tissues of the stem. Principal component analysis revealed gradual shifts in the transcriptomes that followed a chronological order throughout the season. A notable remodeling of the transcriptome was observed in the winter, with many genes having maximal expression during the coldest months of the year. A highly coexpressed set of monolignol biosynthesis genes showed high expression during the period of secondary cell wall formation as well as a second peak in midwinter. This midwinter peak in expression did not trigger lignin deposition, as determined by pyrolysis-gas chromatography/mass spectrometry. Coexpression consensus network analyses suggested the involvement of transcription factors belonging to the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES and MYELOBLASTOSIS-HOMEOBOX families in the seasonal control of secondary cell wall formation of tracheids. Interestingly, the lifetime of the latewood tracheids stretched beyond the winter dormancy period, correlating with a lack of cell death-related gene expression. Our transcriptomic analyses combined with phylogenetic and microscopic analyses also identified the cellulose and lignin biosynthetic genes and putative regulators for latewood formation and tracheid cell death in Norway spruce, providing a toolbox for further physiological and functional assays of these important phase transitions.

Place, publisher, year, edition, pages
American Society of Plant Biologists, 2018
National Category
Cell Biology
Identifiers
urn:nbn:se:umu:diva-148642 (URN)10.1104/pp.17.01590 (DOI)000429089100021 ()29487121 (PubMedID)
Projects
Bio4Energy
Funder
Knut and Alice Wallenberg Foundation, KAW 2013.0305The Kempe Foundations, SMK-1340Swedish Research Council, 621-2013-4949Vinnova, 2015-02290
Available from: 2018-06-21 Created: 2018-06-21 Last updated: 2019-08-30Bibliographically approved
Escamez, S., Latha Gandla, M., Derba-Maceluch, M., Lundqvist, S.-O., Mellerowicz, E. J., Jönsson, L. J. & Tuominen, H. (2017). A collection of genetically engineered Populus trees reveals wood biomass traits that predict glucose yield from enzymatic hydrolysis. Scientific Reports, 7, Article ID 15798.
Open this publication in new window or tab >>A collection of genetically engineered Populus trees reveals wood biomass traits that predict glucose yield from enzymatic hydrolysis
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2017 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 7, article id 15798Article in journal (Refereed) Published
Abstract [en]

Wood represents a promising source of sugars to produce bio-based renewables, including biofuels. However, breaking down lignocellulose requires costly pretreatments because lignocellulose is recalcitrant to enzymatic saccharification. Increasing saccharification potential would greatly contribute to make wood a competitive alternative to petroleum, but this requires improving wood properties. To identify wood biomass traits associated with saccharification, we analyzed a total of 65 traits related to wood chemistry, anatomy and structure, biomass production and saccharification in 40 genetically engineered Populus tree lines. These lines exhibited broad variation in quantitative traits, allowing for multivariate analyses and mathematical modeling. Modeling revealed that seven wood biomass traits associated in a predictive manner with saccharification of glucose after pretreatment. Four of these seven traits were also negatively associated with biomass production, suggesting a trade-off between saccharification potential and total biomass, which has previously been observed to offset the overall sugar yield from whole trees. We therefore estimated the "total-wood glucose yield" (TWG) from whole trees and found 22 biomass traits predictive of TWG after pretreatment. Both saccharification and TWG were associated with low abundant, often overlooked matrix polysaccharides such as arabinose and rhamnose which possibly represent new markers for improved Populus feedstocks.

Place, publisher, year, edition, pages
Nature Publishing Group, 2017
National Category
Biochemistry and Molecular Biology Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-142453 (URN)10.1038/s41598-017-16013-0 (DOI)000415658600043 ()29150693 (PubMedID)
Projects
Bio4Energy
Available from: 2017-12-04 Created: 2017-12-04 Last updated: 2019-09-06Bibliographically approved
Sundell, D., Street, N. R., Kumar, M., Mellerowicz, E. J., Kucukoglu, M., Johnsson, C., . . . Hvidsten, T. R. (2017). AspWood: High-Spatial-Resolution Transcriptome Profiles Reveal Uncharacterized Modularity of Wood Formation in Populus tremula. The Plant Cell, 29(7), 1585-1604
Open this publication in new window or tab >>AspWood: High-Spatial-Resolution Transcriptome Profiles Reveal Uncharacterized Modularity of Wood Formation in Populus tremula
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2017 (English)In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 29, no 7, p. 1585-1604Article in journal (Refereed) Published
Abstract [en]

Trees represent the largest terrestrial carbon sink and a renewable source of ligno-cellulose. There is significant scope for yield and quality improvement in these largely undomesticated species, and efforts to engineer elite varieties will benefit from improved understanding of the transcriptional network underlying cambial growth and wood formation. We generated high-spatial-resolution RNA sequencing data spanning the secondary phloem, vascular cambium, and wood-forming tissues of Populus tremula. The transcriptome comprised 28,294 expressed, annotated genes, 78 novel protein-coding genes, and 567 putative long intergenic noncoding RNAs. Most paralogs originating from the Salicaceae whole-genome duplication had diverged expression, with the exception of those highly expressed during secondary cell wall deposition. Coexpression network analyses revealed that regulation of the transcriptome underlying cambial growth and wood formation comprises numerous modules forming a continuum of active processes across the tissues. A comparative analysis revealed that a majority of these modules are conserved in Picea abies. The high spatial resolution of our data enabled identification of novel roles for characterized genes involved in xylan and cellulose biosynthesis, regulators of xylem vessel and fiber differentiation and lignification. An associated web resource (AspWood, http://aspwood.popgenie.org) provides interactive tools for exploring the expression profiles and coexpression network.

National Category
Bioinformatics and Systems Biology
Identifiers
urn:nbn:se:umu:diva-139016 (URN)10.1105/tpc.17.00153 (DOI)000407495000008 ()
Projects
Bio4Energy
Available from: 2017-09-06 Created: 2017-09-06 Last updated: 2019-08-30Bibliographically approved
Escamez, S. & Tuominen, H. (2017). Contribution of cellular autolysis to tissular functions during plant development. Current opinion in plant biology, 35, 124-130
Open this publication in new window or tab >>Contribution of cellular autolysis to tissular functions during plant development
2017 (English)In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 35, p. 124-130Article, review/survey (Refereed) Published
Abstract [en]

Plant development requires specific cells to be eliminated in a predictable and genetically regulated manner referred to as programmed cell death (PCD). However, the target cells do not merely die but they also undergo autolysis to degrade their cellular corpses. Recent progress in understanding developmental cell elimination suggests that distinct proteins execute PCD sensu stricto and autolysis. In addition, cell death alone and cell dismantlement can fulfill different functions. Hence, it appears biologically meaningful to distinguish between the modules of PCD and autolysis during plant development.

Place, publisher, year, edition, pages
CURRENT BIOLOGY LTD, 2017
National Category
Medical Biotechnology (with a focus on Cell Biology (including Stem Cell Biology), Molecular Biology, Microbiology, Biochemistry or Biopharmacy)
Identifiers
urn:nbn:se:umu:diva-133437 (URN)10.1016/j.pbi.2016.11.017 (DOI)000396959300019 ()27936412 (PubMedID)
Available from: 2017-04-21 Created: 2017-04-21 Last updated: 2018-06-09Bibliographically approved
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