Research

My research focuses on lignification and cell death of xylem elements and how these processes influence the chemical and physical properties of the secondary cell walls and woody tissues of vascular plants. We use two model systems. The roots and hypocotyls of Arabidopsis thaliana provide excellent models for understanding the molecular and genetic control of xylem differentiation, while the woody tissues of aspen (Populus tremula) trees are practical for high-resolution gene expression, genetic, genomic and functional assays.
Xylem elements mature by depositing cellulose-rich secondary cell walls until they die through programmed cell death. Cell death therefore controls the thickness of the secondary cell walls of the xylem by controlling the life time of the xylem elements. We have earlier shown that cell death also controls lignification of xylem elements. Work done in the Zinnia elegans tracheary element differentiation system revealed that lignin biosynthesis continues even after cell death and that lignin polymerization occurs only after cell death. This sequence of events needs to be strictly controlled in time and place. In my previous work I have characterized the cell death process and identified factors that control both lignification and cell death of the xylem elements. The current aim is to identify factors that initiate and execute xylem cell death. One of the focus areas is the signaling and functional characterisation of the Arabidopsis thaliana metacaspase gene family using reverse genetic, forward genetic and biochemical methods in intact plants and in ectopic, hormonally induced tracheary elements.
The fact that the lifetime of the xylem elements controls the thickness of the cell walls and hence the extent of biomass production within each cell implies that that the identification of cell death controlling factors could be used to modify overall biomass production in forest trees. We have taken two different approaches to investigate the relationships between xylem maturation, the chemical and physical properties of the secondary cell wall and the properties of wood. The first approach is to modify expression of selected candidate genes in transgenic aspen (Populus tremula) trees using cell-specific promoters, newest DNA editing technologies and tree phenotyping platform with the aim of delaying xylem cell death and thereby improving biomass properties. The second approach takes advantage of the natural variation within a Swedish aspen population with the aim to identify variation in the secondary cell wall and wood properties and the underlying molecular mechanism by genome-wide association mapping.
Team
- 2006: Docent, Plant developmental biology, University of Helsinki, Finland
- 1997: PhD, Forest Plant Physiology, The Swedish University of Agricultural Sciences, Umeå
- 1991: MSc, The University of Oulu, Finland
- Since 2020: Professor, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
- 2008-2019: Associate professor, Department of Plant Physiology, Umeå University
- 2005-2007: Assisting lecturer, Department of Plant Physiology, Umeå University
- 2001-2005: Assistant professor, Department of Plant Physiology, Umeå University
- 1997-2001: Post doc, Institute of Biotechnology, University of Helsinki, Finland
- 2008: Young Researcher Award (2 million SEK for research), Umeå university
- 2010-2014: Director of the Strong Research Environment BioImprove
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CV H. Tuominen
Education and academic degrees
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Publications

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@incollection{chantreau_spatio-temporal_2022, title = {Spatio-temporal regulation of lignification}, url = {https://www.sciencedirect.com/science/article/pii/S0065229622000398}, abstract = {Lignin is a poly-aromatic polymer found in plant cell walls. This polymer, mainly composed of three phenylpropanoid units, confers exceptional properties to the cell wall such as hydrophobicity, mechanical strength, or resistance against stresses. Thereby the cell wall deposition of lignin represents often the main molecular event that defines the biological function(s) of the lignified cell or tissue. The time and localization of lignin deposition as well as the composition of the polymer can be considered as the three essential components of the polymer that will define the biological function of the lignified tissue. In this review, we will cover the localizations, types and functions of lignin found in various part of land plants. Then, for the various lignified tissues, the mechanisms controlling the developmental deposition of lignin such as transcriptional regulation, intercellular coordinated control of lignification or posttranslational modification of proteins will be discussed. Finally, a focus will be made on the environmental cues that influence the lignification during radial tree growth, as well as the plant responses that these signals trigger in the regulation of lignification.}, language = {en}, urldate = {2022-04-26}, booktitle = {Advances in {Botanical} {Research}}, publisher = {Academic Press}, author = {Chantreau, Maxime and Tuominen, Hannele}, month = apr, year = {2022}, keywords = {Lignification, Lignin, Non-cell autonomous lignification, Regulation}, }
@article{escamez_fluorescence_2021, title = {Fluorescence {Lifetime} {Imaging} as an {In} {Situ} and {Label}-{Free} {Readout} for the {Chemical} {Composition} of {Lignin}}, volume = {9}, url = {https://doi.org/10.1021/acssuschemeng.1c06780}, doi = {10/gnr3sb}, abstract = {Naturally fluorescent polymeric molecules such as collagen, resilin, cutin, suberin, or lignin can serve as renewable sources of bioproducts. Theoretical physics predicts that the fluorescence lifetime of these polymers is related to their chemical composition. We verified this prediction for lignin, a major structural element in plant cell walls that form woody biomass. Lignin is composed of different phenylpropanoid units, and its composition affects its properties, biological functions, and the utilization of wood biomass. We carried out fluorescence lifetime imaging microscopy (FLIM) measurements of wood cell wall lignin in a population of 90 hybrid aspen trees genetically engineered to display differences in cell wall chemistry and structure. We also measured the wood cell wall composition by classical analytical methods in these trees. Using statistical modeling and machine learning algorithms, we identified parameters of fluorescence lifetime that predict the content of S-type and G-type lignin units, the two main types of units in the lignin of angiosperm (flowering) plants. In a first step toward tailoring lignin biosynthesis toward improvement of woody biomass feedstocks, we show how FLIM can reveal the dynamics of lignin biosynthesis in two different biological contexts, including in vivo while lignin is being synthesized in the walls of living cells.}, number = {51}, urldate = {2021-12-14}, journal = {ACS Sustainable Chemistry \& Engineering}, author = {Escamez, Sacha and Terryn, Christine and Gandla, Madhavi Latha and Yassin, Zakiya and Scheepers, Gerhard and Näsholm, Torgny and Sundman, Ola and Jönsson, Leif J. and Lundberg-Felten, Judith and Tuominen, Hannele and Niittylä, Totte and Paës, Gabriel}, month = dec, year = {2021}, pages = {17381--17392}, }
@article{gandla_overexpression_2021, title = {Overexpression of vesicle-associated membrane protein {PttVAP27}-17 as a tool to improve biomass production and the overall saccharification yields in {Populus} trees}, volume = {14}, issn = {1754-6834}, url = {https://biotechnologyforbiofuels.biomedcentral.com/articles/10.1186/s13068-021-01895-0}, doi = {10/gjd7kj}, abstract = {Abstract Background Bioconversion of wood into bioproducts and biofuels is hindered by the recalcitrance of woody raw material to bioprocesses such as enzymatic saccharification. Targeted modification of the chemical composition of the feedstock can improve saccharification but this gain is often abrogated by concomitant reduction in tree growth. Results In this study, we report on transgenic hybrid aspen ( Populus tremula × tremuloides ) lines that showed potential to increase biomass production both in the greenhouse and after 5 years of growth in the field. The transgenic lines carried an overexpression construct for Populus tremula × tremuloides vesicle-associated membrane protein (VAMP)-associated protein PttVAP27-17 that was selected from a gene-mining program for novel regulators of wood formation. Analytical-scale enzymatic saccharification without any pretreatment revealed for all greenhouse-grown transgenic lines, compared to the wild type, a 20–44\% increase in the glucose yield per dry weight after enzymatic saccharification, even though it was statistically significant only for one line. The glucose yield after enzymatic saccharification with a prior hydrothermal pretreatment step with sulfuric acid was not increased in the greenhouse-grown transgenic trees on a dry-weight basis, but increased by 26–50\% when calculated on a whole biomass basis in comparison to the wild-type control. Tendencies to increased glucose yields by up to 24\% were present on a whole tree biomass basis after acidic pretreatment and enzymatic saccharification also in the transgenic trees grown for 5 years on the field when compared to the wild-type control. Conclusions The results demonstrate the usefulness of gene-mining programs to identify novel genes with the potential to improve biofuel production in tree biotechnology programs. Furthermore, multi-omic analyses, including transcriptomic, proteomic and metabolomic analyses, performed here provide a toolbox for future studies on the function of VAP27 proteins in plants.}, language = {en}, number = {1}, urldate = {2021-06-03}, journal = {Biotechnology for Biofuels}, author = {Gandla, Madhavi Latha and Mähler, Niklas and Escamez, Sacha and Skotare, Tomas and Obudulu, Ogonna and Möller, Linus and Abreu, Ilka N. and Bygdell, Joakim and Hertzberg, Magnus and Hvidsten, Torgeir R. and Moritz, Thomas and Wingsle, Gunnar and Trygg, Johan and Tuominen, Hannele and Jönsson, Leif J.}, month = dec, year = {2021}, pages = {43}, }
@article{seyfferth_populuspterf85_2021, title = {{PopulusPtERF85} {Balances} {Xylem} {Cell} {Expansion} and {Secondary} {Cell} {Wall} {Formation} in {Hybrid} {Aspen}}, volume = {10}, copyright = {http://creativecommons.org/licenses/by/3.0/}, url = {https://www.mdpi.com/2073-4409/10/8/1971}, doi = {10.3390/cells10081971}, abstract = {Secondary growth relies on precise and specialized transcriptional networks that determine cell division, differentiation, and maturation of xylem cells. We identified a novel role for the ethylene-induced Populus Ethylene Response Factor PtERF85 (Potri.015G023200) in balancing xylem cell expansion and secondary cell wall (SCW) formation in hybrid aspen (Populus tremula x tremuloides). Expression of PtERF85 is high in phloem and cambium cells and during the expansion of xylem cells, while it is low in maturing xylem tissue. Extending PtERF85 expression into SCW forming zones of woody tissues through ectopic expression reduced wood density and SCW thickness of xylem fibers but increased fiber diameter. Xylem transcriptomes from the transgenic trees revealed transcriptional induction of genes involved in cell expansion, translation, and growth. The expression of genes associated with plant vascular development and the biosynthesis of SCW chemical components such as xylan and lignin, was down-regulated in the transgenic trees. Our results suggest that PtERF85 activates genes related to xylem cell expansion, while preventing transcriptional activation of genes related to SCW formation. The importance of precise spatial expression of PtERF85 during wood development together with the observed phenotypes in response to ectopic PtERF85 expression suggests that PtERF85 contributes to the transition of fiber cells from elongation to secondary cell wall deposition.}, language = {en}, number = {8}, urldate = {2021-09-02}, journal = {Cells}, author = {Seyfferth, Carolin and Wessels, Bernard A. and Vahala, Jorma and Kangasjärvi, Jaakko and Delhomme, Nicolas and Hvidsten, Torgeir R. and Tuominen, Hannele and Lundberg-Felten, Judith}, month = aug, year = {2021}, keywords = {ERF85 (CRF4), cell wall thickness, lignin, ribosome biogenesis, wood development, xylem expansion}, pages = {1971}, }
@article{milhinhos_acaulis5_2020, title = {{ACAULIS5} {Is} {Required} for {Cytokinin} {Accumulation} and {Function} {During} {Secondary} {Growth} of {Populus} {Trees}}, volume = {11}, issn = {1664-462X}, url = {https://www.frontiersin.org/articles/10.3389/fpls.2020.601858/full}, doi = {10.3389/fpls.2020.601858}, urldate = {2021-06-07}, journal = {Frontiers in Plant Science}, author = {Milhinhos, Ana and Bollhöner, Benjamin and Blazquez, Miguel A. and Novák, Ondřej and Miguel, Célia M. and Tuominen, Hannele}, month = nov, year = {2020}, pages = {601858}, }
@article{escamez_cell_2020, title = {Cell {Death} in {Cells} {Overlying} {Lateral} {Root} {Primordia} {Facilitates} {Organ} {Growth} in {Arabidopsis}}, volume = {30}, issn = {09609822}, url = {https://linkinghub.elsevier.com/retrieve/pii/S0960982219315805}, doi = {10/ggh2vm}, language = {en}, number = {3}, urldate = {2021-06-07}, journal = {Current Biology}, author = {Escamez, Sacha and André, Domenique and Sztojka, Bernadette and Bollhöner, Benjamin and Hall, Hardy and Berthet, Béatrice and Voß, Ute and Lers, Amnon and Maizel, Alexis and Andersson, Magnus and Bennett, Malcolm and Tuominen, Hannele}, month = feb, year = {2020}, pages = {455--464.e7}, }
@article{minina_classification_2020, title = {Classification and {Nomenclature} of {Metacaspases} and {Paracaspases}: {No} {More} {Confusion} with {Caspases}}, volume = {77}, issn = {10972765}, shorttitle = {Classification and {Nomenclature} of {Metacaspases} and {Paracaspases}}, url = {https://linkinghub.elsevier.com/retrieve/pii/S1097276519309505}, doi = {10.1016/j.molcel.2019.12.020}, language = {en}, number = {5}, urldate = {2021-06-07}, journal = {Molecular Cell}, author = {Minina, Elena A. and Staal, Jens and Alvarez, Vanina E. and Berges, John A. and Berman-Frank, Ilana and Beyaert, Rudi and Bidle, Kay D. and Bornancin, Frédéric and Casanova, Magali and Cazzulo, Juan J. and Choi, Chang Jae and Coll, Nuria S. and Dixit, Vishva M. and Dolinar, Marko and Fasel, Nicolas and Funk, Christiane and Gallois, Patrick and Gevaert, Kris and Gutierrez-Beltran, Emilio and Hailfinger, Stephan and Klemenčič, Marina and Koonin, Eugene V. and Krappmann, Daniel and Linusson, Anna and Machado, Maurício F.M. and Madeo, Frank and Megeney, Lynn A. and Moschou, Panagiotis N. and Mottram, Jeremy C. and Nyström, Thomas and Osiewacz, Heinz D. and Overall, Christopher M. and Pandey, Kailash C. and Ruland, Jürgen and Salvesen, Guy S. and Shi, Yigong and Smertenko, Andrei and Stael, Simon and Ståhlberg, Jerry and Suárez, María Fernanda and Thome, Margot and Tuominen, Hannele and Van Breusegem, Frank and van der Hoorn, Renier A.L. and Vardi, Assaf and Zhivotovsky, Boris and Lam, Eric and Bozhkov, Peter V.}, month = mar, year = {2020}, pages = {927--929}, }
@article{lakehal_ethylene_2020, title = {{ETHYLENE} {RESPONSE} {FACTOR} 115 integrates jasmonate and cytokinin signaling machineries to repress adventitious rooting in {Arabidopsis}}, volume = {228}, copyright = {©2020 The Authors. New Phytologist ©2020 New Phytologist Trust}, issn = {1469-8137}, url = {https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.16794}, doi = {10/ghhwk4}, abstract = {Adventitious root initiation (ARI) is a de novo organogenesis program and a key adaptive trait in plants. Several hormones regulate ARI but the underlying genetic architecture that integrates the hormonal crosstalk governing this process remains largely elusive. In this study, we use genetics, genome editing, transcriptomics, hormone profiling and cell biological approaches to demonstrate a crucial role played by the APETALA2/ETHYLENE RESPONSE FACTOR 115 transcription factor. We demonstrate that ERF115 functions as a repressor of ARI by activating the cytokinin (CK) signaling machinery. We also demonstrate that ERF115 is transcriptionally activated by jasmonate (JA), an oxylipin-derived phytohormone, which represses ARI in NINJA-dependent and independent manners. Our data indicate that NINJA-dependent JA signaling in pericycle cells blocks early events of ARI. Altogether, our results reveal a previously unreported molecular network involving cooperative crosstalk between JA and CK machineries that represses ARI.}, language = {en}, number = {5}, urldate = {2021-06-21}, journal = {New Phytologist}, author = {Lakehal, Abdellah and Dob, Asma and Rahneshan, Zahra and Novák, Ondřej and Escamez, Sacha and Alallaq, Sanaria and Strnad, Miroslav and Tuominen, Hannele and Bellini, Catherine}, year = {2020}, keywords = {AP2/ERF transcription factors, adventitious rooting, cytokinins, de novo organogenesis, jasmonate}, pages = {1611--1626}, }
@article{zhang_pirin2_2020, title = {{PIRIN2} suppresses {S}‐type lignin accumulation in a noncell‐autonomous manner in {Arabidopsis} xylem elements}, volume = {225}, issn = {0028-646X, 1469-8137}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.16271}, doi = {10.1111/nph.16271}, language = {en}, number = {5}, urldate = {2021-06-07}, journal = {New Phytologist}, author = {Zhang, Bo and Sztojka, Bernadette and Escamez, Sacha and Vanholme, Ruben and Hedenström, Mattias and Wang, Yin and Turumtay, Halbay and Gorzsás, András and Boerjan, Wout and Tuominen, Hannele}, month = mar, year = {2020}, pages = {1923--1935}, }
@article{zhang_chromatin-modifying_2020, title = {The chromatin-modifying protein {HUB2} is involved in the regulation of lignin composition in xylem vessels}, volume = {71}, issn = {0022-0957, 1460-2431}, url = {https://academic.oup.com/jxb/article/71/18/5484/5849544}, doi = {10.1093/jxb/eraa264}, abstract = {Abstract PIRIN2 (PRN2) was earlier reported to suppress syringyl (S)-type lignin accumulation of xylem vessels of Arabidopsis thaliana. In the present study, we report yeast two-hybrid results supporting the interaction of PRN2 with HISTONE MONOUBIQUITINATION2 (HUB2) in Arabidopsis. HUB2 has been previously implicated in several plant developmental processes, but not in lignification. Interaction between PRN2 and HUB2 was verified by β-galactosidase enzymatic and co-immunoprecipitation assays. HUB2 promoted the deposition of S-type lignin in the secondary cell walls of both stem and hypocotyl tissues, as analysed by pyrolysis-GC/MS. Chemical fingerprinting of individual xylem vessel cell walls by Raman and Fourier transform infrared microspectroscopy supported the function of HUB2 in lignin deposition. These results, together with a genetic analysis of the hub2 prn2 double mutant, support the antagonistic function of PRN2 and HUB2 in deposition of S-type lignin. Transcriptome analyses indicated the opposite regulation of the S-type lignin biosynthetic gene FERULATE-5-HYDROXYLASE1 by PRN2 and HUB2 as the underlying mechanism. PRN2 and HUB2 promoter activities co-localized in cells neighbouring the xylem vessel elements, suggesting that the S-type lignin-promoting function of HUB2 is antagonized by PRN2 for the benefit of the guaiacyl (G)-type lignin enrichment of the neighbouring xylem vessel elements.}, language = {en}, number = {18}, urldate = {2021-06-07}, journal = {Journal of Experimental Botany}, author = {Zhang, Bo and Sztojka, Bernadette and Seyfferth, Carolin and Escamez, Sacha and Miskolczi, Pál and Chantreau, Maxime and Bakó, László and Delhomme, Nicolas and Gorzsás, András and Bhalerao, Rishikesh P. and Tuominen, Hannele}, editor = {Turner, Simon}, month = sep, year = {2020}, pages = {5484--5494}, }
@article{wessels_ap2erf_2019, title = {An {AP2}/{ERF} transcription factor {ERF139} coordinates xylem cell expansion and secondary cell wall deposition}, volume = {224}, issn = {0028-646X, 1469-8137}, shorttitle = {An {\textless}span style="font-variant}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.15960}, doi = {10/gjcsfs}, language = {en}, number = {4}, urldate = {2021-06-07}, journal = {New Phytologist}, author = {Wessels, Bernard and Seyfferth, Carolin and Escamez, Sacha and Vain, Thomas and Antos, Kamil and Vahala, Jorma and Delhomme, Nicolas and Kangasjärvi, Jaakko and Eder, Michaela and Felten, Judith and Tuominen, Hannele}, month = dec, year = {2019}, pages = {1585--1599}, }
@article{seyfferth_ethylene_2019, title = {Ethylene {Signaling} {Is} {Required} for {Fully} {Functional} {Tension} {Wood} in {Hybrid} {Aspen}}, volume = {10}, issn = {1664-462X}, url = {https://www.frontiersin.org/article/10.3389/fpls.2019.01101/full}, doi = {10.3389/fpls.2019.01101}, urldate = {2021-06-07}, journal = {Frontiers in Plant Science}, author = {Seyfferth, Carolin and Wessels, Bernard A. and Gorzsás, András and Love, Jonathan W. and Rüggeberg, Markus and Delhomme, Nicolas and Vain, Thomas and Antos, Kamil and Tuominen, Hannele and Sundberg, Björn and Felten, Judith}, month = sep, year = {2019}, pages = {1101}, }
@article{escamez_extracellular_2019, title = {Extracellular peptide {Kratos} restricts cell death during vascular development and stress in {Arabidopsis}}, volume = {70}, issn = {0022-0957, 1460-2431}, url = {https://academic.oup.com/jxb/article/70/7/2199/5308826}, doi = {10/gjd42p}, language = {en}, number = {7}, urldate = {2021-06-07}, journal = {Journal of Experimental Botany}, author = {Escamez, Sacha and Stael, Simon and Vainonen, Julia P and Willems, Patrick and Jin, Huiting and Kimura, Sachie and Van Breusegem, Frank and Gevaert, Kris and Wrzaczek, Michael and Tuominen, Hannele}, month = apr, year = {2019}, pages = {2199--2210}, }
@incollection{giacomello_high_2019, title = {High {Spatial} {Resolution} {Profiling} in {Tree} {Species}}, isbn = {978-1-119-31299-4}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1002/9781119312994.apr0688}, abstract = {Until recently, the majority of genomics assays have been performed on bulk tissue samples containing multiple cell types. Tissues such as the wood formation zone in trees contain a complex mix of cell types organised in three-dimensional space. Moreover, cells within the wood formation zone represent a continual developmental progression from meristematic cambial initials through to cell death. This spatiotemporal developmental gradient and cell type information are not assayed by bulk samples. New and improved sampling methods coupled to next-generation sequencing assays are enabling the generation of high spatial resolution and single-cell transcriptomics data, offering unprecedented insight into the biology of unique cell types and cell developmental programs. We overview the application of these approaches to the study of wood development, in particular, and highlight challenges associated with the analysis of such data.}, language = {en}, urldate = {2021-10-20}, booktitle = {Annual {Plant} {Reviews} online}, publisher = {American Cancer Society}, author = {Giacomello, Stefania and Delhomme, Nicolas and Niittylä, Totte and Tuominen, Hannele and Street, Nathaniel R.}, year = {2019}, doi = {10.1002/9781119312994.apr0688}, note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/9781119312994.apr0688}, keywords = {RNA sequencing, cell type, single cell, spatial resolution, transcriptome, wood formation, xylem}, pages = {329--360}, }
@article{obudulu_multi-omics_2018, title = {A multi-omics approach reveals function of {Secretory} {Carrier}-{Associated} {Membrane} {Proteins} in wood formation of {Populus} trees}, volume = {19}, issn = {1471-2164}, url = {https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-017-4411-1}, doi = {10.1186/s12864-017-4411-1}, language = {en}, number = {1}, urldate = {2021-06-07}, journal = {BMC Genomics}, author = {Obudulu, Ogonna and Mähler, Niklas and Skotare, Tomas and Bygdell, Joakim and Abreu, Ilka N. and Ahnlund, Maria and Latha Gandla, Madhavi and Petterle, Anna and Moritz, Thomas and Hvidsten, Torgeir R. and Jönsson, Leif J. and Wingsle, Gunnar and Trygg, Johan and Tuominen, Hannele}, month = dec, year = {2018}, pages = {11}, }
@article{seyfferth_ethylene-related_2018, title = {Ethylene-{Related} {Gene} {Expression} {Networks} in {Wood} {Formation}}, volume = {9}, issn = {1664-462X}, url = {http://journal.frontiersin.org/article/10.3389/fpls.2018.00272/full}, doi = {10/gc7vds}, urldate = {2021-06-07}, journal = {Frontiers in Plant Science}, author = {Seyfferth, Carolin and Wessels, Bernard and Jokipii-Lukkari, Soile and Sundberg, Björn and Delhomme, Nicolas and Felten, Judith and Tuominen, Hannele}, month = mar, year = {2018}, pages = {272}, }
@article{bollhoner_function_2018, title = {The function of two type {II} metacaspases in woody tissues of \textit{{Populus}} trees}, volume = {217}, issn = {0028646X}, url = {http://doi.wiley.com/10.1111/nph.14945}, doi = {10/gczh42}, language = {en}, number = {4}, urldate = {2021-06-07}, journal = {New Phytologist}, author = {Bollhöner, Benjamin and Jokipii-Lukkari, Soile and Bygdell, Joakim and Stael, Simon and Adriasola, Mathilda and Muñiz, Luis and Van Breusegem, Frank and Ezcurra, Inés and Wingsle, Gunnar and Tuominen, Hannele}, month = mar, year = {2018}, pages = {1551--1565}, }
@article{jokipii-lukkari_transcriptional_2018, title = {Transcriptional {Roadmap} to {Seasonal} {Variation} in {Wood} {Formation} of {Norway} {Spruce}}, volume = {176}, issn = {0032-0889, 1532-2548}, url = {https://academic.oup.com/plphys/article/176/4/2851-2870/6117009}, doi = {10.1104/pp.17.01590}, language = {en}, number = {4}, urldate = {2021-06-07}, journal = {Plant Physiology}, author = {Jokipii-Lukkari, Soile and Delhomme, Nicolas and Schiffthaler, Bastian and Mannapperuma, Chanaka and Prestele, Jakob and Nilsson, Ove and Street, Nathaniel R. and Tuominen, Hannele}, month = apr, year = {2018}, pages = {2851--2870}, }
@article{escamez_collection_2017, title = {A collection of genetically engineered {Populus} trees reveals wood biomass traits that predict glucose yield from enzymatic hydrolysis}, volume = {7}, issn = {2045-2322}, url = {http://www.nature.com/articles/s41598-017-16013-0}, doi = {10/gcmn8b}, language = {en}, number = {1}, urldate = {2021-06-07}, journal = {Scientific Reports}, author = {Escamez, Sacha and Latha Gandla, Madhavi and Derba-Maceluch, Marta and Lundqvist, Sven-Olof and Mellerowicz, Ewa J. and Jönsson, Leif J. and Tuominen, Hannele}, month = dec, year = {2017}, pages = {15798}, }
@article{sundell_aspwood_2017, title = {{AspWood}: {High}-{Spatial}-{Resolution} {Transcriptome} {Profiles} {Reveal} {Uncharacterized} {Modularity} of {Wood} {Formation} in {Populus} tremula}, volume = {29}, issn = {1040-4651, 1532-298X}, shorttitle = {{AspWood}}, url = {https://academic.oup.com/plcell/article/29/7/1585-1604/6099151}, doi = {10/gbshnb}, language = {en}, number = {7}, urldate = {2021-06-07}, journal = {The Plant Cell}, author = {Sundell, David and Street, Nathaniel R. and Kumar, Manoj and Mellerowicz, Ewa J. and Kucukoglu, Melis and Johnsson, Christoffer and Kumar, Vikash and Mannapperuma, Chanaka and Delhomme, Nicolas and Nilsson, Ove and Tuominen, Hannele and Pesquet, Edouard and Fischer, Urs and Niittylä, Totte and Sundberg, Björn and Hvidsten, Torgeir R.}, month = jul, year = {2017}, pages = {1585--1604}, }
@article{escamez_contribution_2017, title = {Contribution of cellular autolysis to tissular functions during plant development}, volume = {35}, issn = {13695266}, url = {https://linkinghub.elsevier.com/retrieve/pii/S1369526616302126}, doi = {10.1016/j.pbi.2016.11.017}, language = {en}, urldate = {2021-06-07}, journal = {Current Opinion in Plant Biology}, author = {Escamez, Sacha and Tuominen, Hannele}, month = feb, year = {2017}, pages = {124--130}, }
@article{jokipiilukkari_norwood_2017, title = {{NorWood}: a gene expression resource for evo‐devo studies of conifer wood development}, volume = {216}, issn = {0028-646X, 1469-8137}, shorttitle = {{NorWood}}, url = {https://onlinelibrary.wiley.com/doi/10.1111/nph.14458}, doi = {10.1111/nph.14458}, language = {en}, number = {2}, urldate = {2021-06-07}, journal = {New Phytologist}, author = {Jokipii‐Lukkari, Soile and Sundell, David and Nilsson, Ove and Hvidsten, Torgeir R. and Street, Nathaniel R. and Tuominen, Hannele}, month = oct, year = {2017}, pages = {482--494}, }
@incollection{de_lucas_quick_2017, address = {New York, NY}, title = {Quick {Histochemical} {Staining} {Methods} to {Detect} {Cell} {Death} in {Xylem} {Elements} of {Plant} {Tissues}}, volume = {1544}, isbn = {978-1-4939-6720-9 978-1-4939-6722-3}, url = {http://link.springer.com/10.1007/978-1-4939-6722-3_3}, urldate = {2021-06-07}, booktitle = {Xylem}, publisher = {Springer New York}, author = {Escamez, Sacha and Bollhöner, Benjamin and Tuominen, Hannele}, editor = {de Lucas, Miguel and Etchhells, J. Peter}, year = {2017}, doi = {10.1007/978-1-4939-6722-3_3}, note = {Series Title: Methods in Molecular Biology}, pages = {27--36}, }
@article{escamez_metacaspase9_2016, title = {{METACASPASE9} modulates autophagy to confine cell death to the target cells during \textit{{Arabidopsis}} vascular xylem differentiation}, volume = {5}, issn = {2046-6390}, url = {https://journals.biologists.com/bio/article/5/2/122/643/METACASPASE9-modulates-autophagy-to-confine-cell}, doi = {10.1242/bio.015529}, abstract = {ABSTRACT We uncovered that the level of autophagy in plant cells undergoing programmed cell death determines the fate of the surrounding cells. Our approach consisted of using Arabidopsis thaliana cell cultures capable of differentiating into two different cell types: vascular tracheary elements (TEs) that undergo programmed cell death (PCD) and protoplast autolysis, and parenchymatic non-TEs that remain alive. The TE cell type displayed higher levels of autophagy when expression of the TE-specific METACASPASE9 (MC9) was reduced using RNAi (MC9-RNAi). Misregulation of autophagy in the MC9-RNAi TEs coincided with ectopic death of the non-TEs, implying the existence of an autophagy-dependent intercellular signalling from within the TEs towards the non-TEs. Viability of the non-TEs was restored when AUTOPHAGY2 (ATG2) was downregulated specifically in MC9-RNAi TEs, demonstrating the importance of autophagy in the spatial confinement of cell death. Our results suggest that other eukaryotic cells undergoing PCD might also need to tightly regulate their level of autophagy to avoid detrimental consequences for the surrounding cells.}, language = {en}, number = {2}, urldate = {2021-06-07}, journal = {Biology Open}, author = {Escamez, Sacha and André, Domenique and Zhang, Bo and Bollhöner, Benjamin and Pesquet, Edouard and Tuominen, Hannele}, month = feb, year = {2016}, pages = {122--129}, }
@article{vera-sirera_bhlh-based_2015, title = {A {bHLH}-{Based} {Feedback} {Loop} {Restricts} {Vascular} {Cell} {Proliferation} in {Plants}}, volume = {35}, issn = {1878-1551 (Electronic) 1534-5807 (Linking)}, url = {https://www.ncbi.nlm.nih.gov/pubmed/26609958}, doi = {10.1016/j.devcel.2015.10.022}, abstract = {Control of tissue dimensions in multicellular organisms requires the precise quantitative regulation of mitotic activity. In plants, where cells are immobile, tissue size is achieved through control of both cell division orientation and mitotic rate. The bHLH transcription factor heterodimer formed by target of monopteros5 (TMO5) and lonesome highway (LHW) is a central regulator of vascular width-increasing divisions. An important unanswered question is how its activity is limited to specify vascular tissue dimensions. Here we identify a regulatory network that restricts TMO5/LHW activity. We show that thermospermine synthase ACAULIS5 antagonizes TMO5/LHW activity by promoting the accumulation of SAC51-LIKE (SACL) bHLH transcription factors. SACL proteins heterodimerize with LHW-therefore likely competing with TMO5/LHW interactions-prevent activation of TMO5/LHW target genes, and suppress the over-proliferation caused by excess TMO5/LHW activity. These findings connect two thus-far disparate pathways and provide a mechanistic understanding of the quantitative control of vascular tissue growth.}, language = {en}, number = {4}, urldate = {2021-06-07}, journal = {Dev Cell}, author = {Vera-Sirera, F. and De Rybel, B. and Urbez, C. and Kouklas, E. and Pesquera, M. and Alvarez-Mahecha, J. C. and Minguet, E. G. and Tuominen, H. and Carbonell, J. and Borst, J. W. and Weijers, D. and Blazquez, M. A.}, month = nov, year = {2015}, keywords = {*Gene Expression Regulation, Plant, Arabidopsis Proteins/antagonists \& inhibitors/genetics/*metabolism, Arabidopsis/genetics/*growth \& development/metabolism, Basic Helix-Loop-Helix Transcription Factors/antagonists \&, Gene Expression Regulation, Developmental, Plant Roots/*cytology/metabolism, Plants, Genetically Modified/genetics/growth \& development/metabolism, RNA, Messenger/genetics, Real-Time Polymerase Chain Reaction, Reverse Transcriptase Polymerase Chain Reaction, Trans-Activators/antagonists \& inhibitors/genetics/metabolism, Xylem/*cytology/metabolism, inhibitors/genetics/*metabolism}, pages = {432--43}, }
@article{serk_cooperative_2015, title = {Cooperative lignification of xylem tracheary elements}, volume = {10}, issn = {1559-2324 (Electronic) 1559-2316 (Linking)}, url = {https://www.ncbi.nlm.nih.gov/pubmed/25761224}, doi = {10.1080/15592324.2014.1003753}, abstract = {The development of xylem tracheary elements (TEs)--the hydro-mineral sap conducting cells--has been an evolutionary breakthrough to enable long distance nutrition and upright growth of vascular land plants. To allow sap conduction, TEs form hollow laterally reinforced cylinders by combining programmed cell death and secondary cell wall formation. To ensure their structural resistance for sap conduction, TE cell walls are reinforced with the phenolic polymer lignin, which is deposited after TE cell death by the cooperative supply of monomers and other substrates from the surrounding living cells.}, language = {eng}, number = {4}, journal = {Plant Signal Behav}, author = {Serk, H. and Gorzsas, A. and Tuominen, H. and Pesquet, E.}, year = {2015}, note = {Edition: 2015/03/12}, keywords = {Arabidopsis, Arabidopsis Proteins, Arabidopsis Proteins/metabolism, Arabidopsis/metabolism, Asteraceae, Asteraceae/*metabolism, Cell Wall, Cell Wall/metabolism, Hypocotyl, Hypocotyl/metabolism, Lignin, Lignin/*metabolism, Time Factors, Xylem, Xylem/*metabolism, lignin, non-cell autonomous process, post-mortem lignification, secondary cell wall, tracheary elements, xylem/wood vessels}, pages = {e1003753}, }
@article{wrzaczek_grim_2015, title = {{GRIM} {REAPER} peptide binds to receptor kinase {PRK5} to trigger cell death in {Arabidopsis}}, volume = {34}, issn = {0261-4189}, url = {https://www.embopress.org/doi/full/10.15252/embj.201488582}, doi = {10/f2wbpv}, abstract = {Abstract Recognition of extracellular peptides by plasma membrane-localized receptor proteins is commonly used in signal transduction. In plants, very little is known about how extracellular peptides are processed and activated in order to allow recognition by receptors. Here, we show that induction of cell death in planta by a secreted plant protein GRIM REAPER (GRI) is dependent on the activity of the type II metacaspase METACASPASE-9. GRI is cleaved by METACASPASE-9 in vitro resulting in the release of an 11 amino acid peptide. This peptide bound in vivo to the extracellular domain of the plasma membrane-localized, atypical leucine-rich repeat receptor-like kinase POLLEN-SPECIFIC RECEPTOR-LIKE KINASE 5 (PRK5) and was sufficient to induce oxidative stress/ROS-dependent cell death. This shows a signaling pathway in plants from processing and activation of an extracellular protein to recognition by its receptor.}, number = {1}, urldate = {2021-06-21}, journal = {The EMBO Journal}, author = {Wrzaczek, Michael and Vainonen, Julia P and Stael, Simon and Tsiatsiani, Liana and Help-Rinta-Rahko, Hanna and Gauthier, Adrien and Kaufholdt, David and Bollhöner, Benjamin and Lamminmäki, Airi and Staes, An and Gevaert, Kris and Tuominen, Hannele and Van Breusegem, Frank and Helariutta, Ykä and Kangasjärvi, Jaakko}, month = jan, year = {2015}, note = {Publisher: John Wiley \& Sons, Ltd}, keywords = {ligand, protease, receptor-like kinase, secreted protein}, pages = {55--66}, }
link bibtex
@incollection{gunawardena_life_2015, address = {Cham}, title = {Life {Beyond} {Death}: {The} {Formation} of {Xylem} {Sap} {Conduits}}, isbn = {978-3-319-21032-2 978-3-319-21033-9}, shorttitle = {Life {Beyond} {Death}}, language = {en}, urldate = {2021-06-07}, booktitle = {Plant {Programmed} {Cell} {Death}}, publisher = {Springer International Publishing}, author = {Ménard, Delphine and Escamez, Sacha and Tuominen, Hannele and Pesquet, Edouard}, editor = {Gunawardena, Arunika N. and McCabe, Paul F.}, year = {2015}, pages = {55--76}, }
@article{zhang_pirin2_2014, title = {{PIRIN2} stabilizes cysteine protease {XCP2} and increases susceptibility to the vascular pathogen {Ralstonia} solanacearum in {Arabidopsis}}, volume = {79}, copyright = {© 2014 The Authors The Plant Journal published by Society for Experimental Biology and John Wiley \& Sons Ltd.}, issn = {1365-313X}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/tpj.12602}, doi = {10/f24qpz}, abstract = {PIRIN (PRN) is a member of the functionally diverse cupin protein superfamily. There are four members of the Arabidopsis thaliana PRN family, but the roles of these proteins are largely unknown. Here we describe a function of the Arabidopsis PIRIN2 (PRN2) that is related to susceptibility to the bacterial plant pathogen Ralstonia solanacearum. Two prn2 mutant alleles displayed decreased disease development and bacterial growth in response to R. solanacearum infection. We elucidated the underlying molecular mechanism by analyzing PRN2 interactions with the papain-like cysteine proteases (PLCPs) XCP2, RD21A, and RD21B, all of which bound to PRN2 in yeast two-hybrid assays and in Arabidopsis protoplast co-immunoprecipitation assays. We show that XCP2 is stabilized by PRN2 through inhibition of its autolysis on the basis of PLCP activity profiling assays and enzymatic assays with recombinant protein. The stabilization of XCP2 by PRN2 was also confirmed in planta. Like prn2 mutants, an xcp2 single knockout mutant and xcp2 prn2 double knockout mutant displayed decreased susceptibility to R. solanacearum, suggesting that stabilization of XCP2 by PRN2 underlies susceptibility to R. solanacearum in Arabidopsis.}, language = {en}, number = {6}, urldate = {2021-06-21}, journal = {The Plant Journal}, author = {Zhang, Bo and Tremousaygue, Dominique and Denancé, Nicolas and Esse, H. Peter van and Hörger, Anja C. and Dabos, Patrick and Goffner, Deborah and Thomma, Bart P. H. J. and Hoorn, Renier A. L. van der and Tuominen, Hannele}, year = {2014}, note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.12602}, keywords = {Arabidopsis thaliana, PIRIN2, Ralstonia solanacearum, XCP2, papain-like cysteine protease, vascular pathogen}, pages = {1009--1019}, }
@article{escamez_programmes_2014, title = {Programmes of cell death and autolysis in tracheary elements: when a suicidal cell arranges its own corpse removal}, volume = {65}, issn = {1460-2431, 0022-0957}, shorttitle = {Programmes of cell death and autolysis in tracheary elements}, url = {https://academic.oup.com/jxb/article-lookup/doi/10.1093/jxb/eru057}, doi = {10/f234sm}, language = {en}, number = {5}, urldate = {2021-06-08}, journal = {Journal of Experimental Botany}, author = {Escamez, Sacha and Tuominen, Hannele}, month = mar, year = {2014}, pages = {1313--1321}, }
@article{pesquet_non-cell-autonomous_2013, title = {Non-{Cell}-{Autonomous} {Postmortem} {Lignification} of {Tracheary} {Elements} in \textit{{Zinnia} elegans}}, volume = {25}, issn = {1532-298X, 1040-4651}, url = {https://academic.oup.com/plcell/article/25/4/1314/6100539}, doi = {10/f22bdv}, abstract = {Abstract Postmortem lignification of xylem tracheary elements (TEs) has been debated for decades. Here, we provide evidence in Zinnia elegans TE cell cultures, using pharmacological inhibitors and in intact Z. elegans plants using Fourier transform infrared microspectroscopy, that TE lignification occurs postmortem (i.e., after TE programmed cell death). In situ RT-PCR verified expression of the lignin monomer biosynthetic cinnamoyl CoA reductase and cinnamyl alcohol dehydrogenase in not only the lignifying TEs but also in the unlignified non-TE cells of Z. elegans TE cell cultures and in living, parenchymatic xylem cells that surround TEs in stems. These cells were also shown to have the capacity to synthesize and transport lignin monomers and reactive oxygen species to the cell walls of dead TEs. Differential gene expression analysis in Z. elegans TE cell cultures and concomitant functional analysis in Arabidopsis thaliana resulted in identification of several genes that were expressed in the non-TE cells and that affected lignin chemistry on the basis of pyrolysis–gas chromatography/mass spectrometry analysis. These data suggest that living, parenchymatic xylem cells contribute to TE lignification in a non-cell-autonomous manner, thus enabling the postmortem lignification of TEs.}, language = {en}, number = {4}, urldate = {2021-06-08}, journal = {The Plant Cell}, author = {Pesquet, Edouard and Zhang, Bo and Gorzsás, András and Puhakainen, Tuula and Serk, Henrik and Escamez, Sacha and Barbier, Odile and Gerber, Lorenz and Courtois-Moreau, Charleen and Alatalo, Edward and Paulin, Lars and Kangasjärvi, Jaakko and Sundberg, Björn and Goffner, Deborah and Tuominen, Hannele}, month = may, year = {2013}, pages = {1314--1328}, }
@article{bollhoner_post_2013, title = {Post mortem function of {AtMC9} in xylem vessel elements}, volume = {200}, copyright = {© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust}, issn = {1469-8137}, url = {https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.12387}, doi = {10/f228vk}, abstract = {Cell death of xylem elements is manifested by rupture of the tonoplast and subsequent autolysis of the cellular contents. Metacaspases have been implicated in various forms of plant cell death but regulation and execution of xylem cell death by metacaspases remains unknown. Analysis of the type II metacaspase gene family in Arabidopsis thaliana supported the function of METACASPASE 9 (AtMC9) in xylem cell death. Progression of xylem cell death was analysed in protoxylem vessel elements of 3-d-old atmc9 mutant roots using reporter gene analysis and electron microscopy. Protoxylem cell death was normally initiated in atmc9 mutant lines, but detailed electron microscopic analyses revealed a role for AtMC9 in clearance of the cell contents post mortem, that is after tonoplast rupture. Subcellular localization of fluorescent AtMC9 reporter fusions supported a post mortem role for AtMC9. Further, probe-based activity profiling suggested a function of AtMC9 on activities of papain-like cysteine proteases. Our data demonstrate that the function of AtMC9 in xylem cell death is to degrade vessel cell contents after vacuolar rupture. We further provide evidence on a proteolytic cascade in post mortem autolysis of xylem vessel elements and suggest that AtMC9 is part of this cascade.}, language = {en}, number = {2}, urldate = {2021-06-21}, journal = {New Phytologist}, author = {Bollhöner, Benjamin and Zhang, Bo and Stael, Simon and Denancé, Nicolas and Overmyer, Kirk and Goffner, Deborah and Breusegem, Frank Van and Tuominen, Hannele}, year = {2013}, note = {\_eprint: https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.12387}, keywords = {Arabidopsis thaliana, autolysis, metacaspase, protease, vessel element, xylem cell death}, pages = {498--510}, }
@article{nystedt_norway_2013, title = {The {Norway} spruce genome sequence and conifer genome evolution}, volume = {497}, issn = {0028-0836, 1476-4687}, url = {http://www.nature.com/articles/nature12211}, doi = {10/f2zsx6}, language = {en}, number = {7451}, urldate = {2021-06-08}, journal = {Nature}, author = {Nystedt, Björn and Street, Nathaniel R. and Wetterbom, Anna and Zuccolo, Andrea and Lin, Yao-Cheng and Scofield, Douglas G. and Vezzi, Francesco and Delhomme, Nicolas and Giacomello, Stefania and Alexeyenko, Andrey and Vicedomini, Riccardo and Sahlin, Kristoffer and Sherwood, Ellen and Elfstrand, Malin and Gramzow, Lydia and Holmberg, Kristina and Hällman, Jimmie and Keech, Olivier and Klasson, Lisa and Koriabine, Maxim and Kucukoglu, Melis and Käller, Max and Luthman, Johannes and Lysholm, Fredrik and Niittylä, Totte and Olson, Åke and Rilakovic, Nemanja and Ritland, Carol and Rosselló, Josep A. and Sena, Juliana and Svensson, Thomas and Talavera-López, Carlos and Theißen, Günter and Tuominen, Hannele and Vanneste, Kevin and Wu, Zhi-Qiang and Zhang, Bo and Zerbe, Philipp and Arvestad, Lars and Bhalerao, Rishikesh P. and Bohlmann, Joerg and Bousquet, Jean and Garcia Gil, Rosario and Hvidsten, Torgeir R. and de Jong, Pieter and MacKay, John and Morgante, Michele and Ritland, Kermit and Sundberg, Björn and Lee Thompson, Stacey and Van de Peer, Yves and Andersson, Björn and Nilsson, Ove and Ingvarsson, Pär K. and Lundeberg, Joakim and Jansson, Stefan}, month = may, year = {2013}, pages = {579--584}, }
@article{milhinhos_thermospermine_2013, title = {Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in \textit{{Populus}} xylem}, volume = {75}, issn = {09607412}, url = {http://doi.wiley.com/10.1111/tpj.12231}, doi = {10/f22nbr}, language = {en}, number = {4}, urldate = {2021-06-08}, journal = {The Plant Journal}, author = {Milhinhos, Ana and Prestele, Jakob and Bollhöner, Benjamin and Matos, Andreia and Vera-Sirera, Francisco and Rambla, José L. and Ljung, Karin and Carbonell, Juan and Blázquez, Miguel A. and Tuominen, Hannele and Miguel, Célia M.}, month = aug, year = {2013}, pages = {685--698}, }
@article{bollhoner_xylem_2012, title = {Xylem cell death: emerging understanding of regulation and function}, volume = {63}, issn = {0022-0957, 1460-2431}, shorttitle = {Xylem cell death}, url = {https://academic.oup.com/jxb/article-lookup/doi/10.1093/jxb/err438}, doi = {10/fx99k4}, language = {en}, number = {3}, urldate = {2021-06-08}, journal = {Journal of Experimental Botany}, author = {Bollhoner, B. and Prestele, J. and Tuominen, H.}, month = feb, year = {2012}, pages = {1081--1094}, }
@article{pesquet_ethylene_2011, title = {Ethylene stimulates tracheary element differentiation in \textit{{Zinnia} elegans} cell cultures}, volume = {190}, issn = {0028-646X, 1469-8137}, url = {https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2010.03600.x}, doi = {10/cpkfn3}, language = {en}, number = {1}, urldate = {2021-06-08}, journal = {New Phytologist}, author = {Pesquet, Edouard and Tuominen, Hannele}, month = apr, year = {2011}, pages = {138--149}, }
@article{vera-sirera_role_2010, title = {Role of polyamines in plant vascular development}, volume = {48}, issn = {09819428}, url = {https://linkinghub.elsevier.com/retrieve/pii/S0981942810000173}, doi = {10/c429rn}, language = {en}, number = {7}, urldate = {2021-06-08}, journal = {Plant Physiology and Biochemistry}, author = {Vera-Sirera, Francisco and Minguet, Eugenio G. and Singh, Sunil Kumar and Ljung, Karin and Tuominen, Hannele and Blázquez, Miguel A. and Carbonell, Juan}, month = jul, year = {2010}, pages = {534--539}, }
@article{courtois-moreau_unique_2009, title = {A unique program for cell death in xylem fibers of \textit{{Populus}} stem}, volume = {58}, issn = {09607412, 1365313X}, url = {http://doi.wiley.com/10.1111/j.1365-313X.2008.03777.x}, doi = {10/bqdrgm}, language = {en}, number = {2}, urldate = {2021-06-08}, journal = {The Plant Journal}, author = {Courtois-Moreau, Charleen L. and Pesquet, Edouard and Sjödin, Andreas and Muñiz, Luis and Bollhöner, Benjamin and Kaneda, Minako and Samuels, Lacey and Jansson, Stefan and Tuominen, Hannele}, month = apr, year = {2009}, pages = {260--274}, }
@article{fracheboud_control_2009, title = {The {Control} of {Autumn} {Senescence} in {European} {Aspen}}, volume = {149}, issn = {1532-2548}, url = {https://academic.oup.com/plphys/article/149/4/1982/6107938}, doi = {10/b8n86h}, abstract = {Abstract The initiation, progression, and natural variation of autumn senescence in European aspen (Populus tremula) was investigated by monitoring chlorophyll degradation in (1) trees growing in natural stands and (2) cloned trees growing in a greenhouse under various light regimes. The main trigger for the initiation of autumn senescence in aspen is the shortening photoperiod, but there was a large degree of variation in the onset of senescence, both within local populations and among trees originating from different populations, where it correlated with the latitude of their respective origins. The variation for onset of senescence with a population was much larger than the variation of bud set. Once started, autumn senescence was accelerated by low temperature and longer nights, and clones that started to senescence late had a faster senescence. Bud set and autumn senescence appeared to be under the control of two independent critical photoperiods, but senescence could not be initiated until a certain time after bud set, suggesting that bud set and growth arrest are important for the trees to acquire competence to respond to the photoperiodic trigger to undergo autumn senescence. A timetable of events related to bud set and autumn senescence is presented.}, language = {en}, number = {4}, urldate = {2021-06-08}, journal = {Plant Physiology}, author = {Fracheboud, Yvan and Luquez, Virginia and Björkén, Lars and Sjödin, Andreas and Tuominen, Hannele and Jansson, Stefan}, month = apr, year = {2009}, pages = {1982--1991}, }
@article{muniz_acaulis5_2008, title = {{ACAULIS5} controls \textit{{Arabidopsis}} xylem specification through the prevention of premature cell death}, volume = {135}, issn = {1477-9129, 0950-1991}, url = {https://journals.biologists.com/dev/article/135/15/2573/64801/ACAULIS5-controls-Arabidopsis-xylem-specification}, doi = {10/bktf62}, abstract = {Cell size and secondary cell wall patterning are crucial for the proper functioning of xylem vessel elements in the vascular tissues of plants. Through detailed anatomical characterization of Arabidopsis thalianahypocotyls, we observed that mutations in the putative spermine biosynthetic gene ACL5 severely affected xylem specification: the xylem vessel elements of the acl5 mutant were small and mainly of the spiral type,and the normally predominant pitted vessels as well as the xylem fibers were completely missing. The cell-specific expression of ACL5 in the early developing vessel elements, as detected by in situ hybridization and reporter gene analyses, suggested that the observed xylem vessel defects were caused directly by the acl5 mutation. Exogenous spermine prolonged xylem element differentiation and stimulated cell expansion and cell wall elaboration in xylogenic cell cultures of Zinnia elegans, suggesting that ACL5 prevents premature death of the developing vessel elements to allow complete expansion and secondary cell wall patterning. This was further supported by our observations that the vessel elements of acl5 seemed to initiate the cell death program too early and that the xylem defects associated with acl5 could be largely phenocopied by induction of premature, diphtheria toxin-mediated cell death in the ACL5-expressing vessel elements. We therefore provide, for the first time, mechanistic evidence for the function of ACL5 in xylem specification through its action on the duration of xylem element differentiation.}, language = {en}, number = {15}, urldate = {2021-06-10}, journal = {Development}, author = {Muñiz, Luis and Minguet, Eugenio G. and Singh, Sunil Kumar and Pesquet, Edouard and Vera-Sirera, Francisco and Moreau-Courtois, Charleen L. and Carbonell, Juan and Blázquez, Miguel A. and Tuominen, Hannele}, month = aug, year = {2008}, pages = {2573--2582}, }
@article{overmyer_complex_2008, title = {Complex phenotypic profiles leading to ozone sensitivity in \textit{{Arabidopsis} thaliana} mutants}, volume = {31}, issn = {01407791, 13653040}, url = {http://doi.wiley.com/10.1111/j.1365-3040.2008.01837.x}, doi = {10/bvqtdg}, language = {en}, number = {9}, urldate = {2021-06-10}, journal = {Plant, Cell \& Environment}, author = {Overmyer, Kirk and Kollist, Hannes and Tuominen, Hannele and Betz, Christian and Langebartels, Christian and Wingsle, Gunnar and Kangasjärvi, Saijaliisa and Brader, Günter and Mullineaux, Phil and Kangasjärvi, Jaakko}, month = sep, year = {2008}, pages = {1237--1249}, }
@article{keech_different_2007, title = {The different fates of mitochondria and chloroplasts during dark-induced senescence in {Arabidopsis} leaves}, volume = {30}, issn = {0140-7791, 1365-3040}, url = {http://doi.wiley.com/10.1111/j.1365-3040.2007.01724.x}, doi = {10/bpfzq8}, language = {en}, number = {12}, urldate = {2021-06-10}, journal = {Plant, Cell \& Environment}, author = {Keech, Olivier and Pesquet, Edouard and Ahad, Abdul and Askne, Anna and Nordvall, Dag and Vodnala, Sharvani Munender and Tuominen, Hannele and Hurry, Vaughan and Dizengremel, Pierre and Gardeström, Per}, month = dec, year = {2007}, pages = {1523--1534}, }
doi link bibtex abstract
@article{ruonala_transitions_2006, title = {Transitions in the functioning of the shoot apical meristem in birch ({Betula} pendula) involve ethylene}, volume = {46}, issn = {0960-7412}, doi = {10/dmkh9w}, abstract = {In many trees, a short photoperiod (SD) triggers substantial physiological adjustments necessary for over-wintering. We have used transgenic ethylene-insensitive birches (Betula pendula), which express the Arabidopsis ethylene receptor gene ETR1 carrying the dominant mutation etr1-1, to investigate the role of ethylene in SD-induced responses in the shoot apical meristem (SAM). Under SD, the ethylene-insensitive trees ceased elongation growth comparably to the wild-type. In contrast, the formation of terminal buds, which in trees is typically induced by SD, was abolished. However, although delayed, endo-dormancy did eventually develop in the ethylene-insensitive trees. This, together with the rapid resumption of growth in the ethylene-insensitive trees after transfer from non-permissive to permissive conditions suggests that ethylene facilitates the SD-induced terminal bud formation, as well as growth arrest. In addition, apical buds of the ethylene-insensitive birch did not accumulate abscisic acid (ABA) under SD, suggesting interaction between ethylene and ABA signalling in the bud. Alterations in SAM functioning were further exemplified by reduced apical dominance and early flowering in ethylene-insensitive birches. Gene expression analysis of shoot apices revealed that the ethylene-insensitive birch lacked the marked increase in expression of a beta-xylosidase gene typical to the SD-exposed wild-type. The ethylene-dependent beta-xylosidase gene expression is hypothesized to relate to modification of cell walls in terminal buds during SD-induced growth cessation. Our results suggest that ethylene is involved in terminal bud formation and in the timely suppression of SAM activity, not only in the shoot apex, but also in axillary and reproductive meristems.}, language = {English}, number = {4}, journal = {Plant Journal}, author = {Ruonala, R. and Rinne, P. L. H. and Baghour, M. and Moritz, T. and Tuominen, H. and Kangasjarvi, J.}, month = may, year = {2006}, note = {Place: Hoboken Publisher: Wiley WOS:000237098000008}, keywords = {abscisic-acid, apical dominance, arabidopsis-thaliana, beta-xylosidase gene, birch, bud dormancy, cell-wall metabolism, dormancy, ethylene, expression, flowering, freezing tolerance, induction, lateral bud growth, response pathway, xylosidase}, pages = {628--640}, }
doi link bibtex abstract
@article{moreau_genomic_2005, title = {A genomic approach to investigate developmental cell death in woody tissues of {Populus} trees}, volume = {6}, issn = {1474-760X}, doi = {10.1186/gb-2005-6-4-r34}, abstract = {Background: Poplar ( Populus sp.) has emerged as the main model system for molecular and genetic studies of forest trees. A Populus expressed sequence tag ( EST) database (POPULUSDB) was previously created from 19 cDNA libraries each originating from different Populus tree tissues, and opened to the public in September 2004. We used this dataset for in silico transcript profiling of a particular process in the woody tissues of the Populus stem: the programmed death of xylem fibers. Results: One EST library in POPULUSDB originates from woody tissues of the Populus stem where xylem fibers undergo cell death. Analysis of EST abundances and library distribution within the POPULUSDB revealed a large number of previously uncharacterized transcripts that were unique in this library and possibly related to the death of xylem fibers. The in silico analysis was complemented by a microarray analysis utilizing a novel Populus cDNA array with a unigene set of 25,000 sequences. Conclusions: In silico analysis, combined with the microarray analysis, revealed the usefulness of non-normalized EST libraries in elucidating transcriptional regulation of previously uncharacterized physiological processes. The data suggested the involvement of two novel extracellular serine proteases, nodulin-like proteins and an Arabidopsis thaliana OPEN STOMATA 1 (AtOST1) homolog in signaling fiber-cell death, as well as mechanisms responsible for hormonal control, nutrient remobilization, regulation of vacuolar integrity and autolysis of the dying fibers.}, language = {English}, number = {4}, journal = {Genome Biology}, author = {Moreau, C. and Aksenov, N. and Lorenzo, M. G. and Segerman, B. and Funk, C. and Nilsson, P. and Jansson, S. and Tuominen, H.}, year = {2005}, note = {Place: London Publisher: Bmc WOS:000228436000011}, keywords = {arabidopsis, arabinogalactan proteins, expression, poplar, secondary growth, senescence, serine proteases, tracheary element differentiation, transcriptome, xylogenesis}, pages = {R34}, }
@article{overmyer_ozone-induced_2005, title = {Ozone-{Induced} {Programmed} {Cell} {Death} in the {Arabidopsis} radical-induced cell death1 {Mutant}}, volume = {137}, issn = {0032-0889}, url = {https://doi.org/10.1104/pp.104.055681}, doi = {10/dqjtb3}, abstract = {Short, high-concentration peaks of the atmospheric pollutant ozone (O3) cause the formation of cell death lesions on the leaves of sensitive plants. Numerous similarities between the plant responses to O3 and pathogens suggest that O3 triggers hypersensitive response-like programmed cell death (PCD). We examined O3 and superoxide-induced cell death in the O3-sensitive radical-induced cell death1 (rcd1) mutant. Dying cells in O3-exposed rcd1 exhibited several of the typical morphological characteristics of the hypersensitive response and PCD. Double-mutant analyses indicated a requirement for salicylic acid and the function of the cyclic nucleotide-gated ion channel AtCNGC2 in cell death. Furthermore, a requirement for ATPases, kinases, transcription, Ca2+ flux, caspase-like proteolytic activity, and also one or more phenylmethylsulfonyl fluoride-sensitive protease activities was shown for the development of cell death lesions in rcd1. Furthermore, mitogen-activated protein kinases showed differential activation patterns in rcd1 and Columbia. Taken together, these results directly demonstrate the induction of PCD by O3.}, number = {3}, urldate = {2021-06-11}, journal = {Plant Physiology}, author = {Overmyer, Kirk and Brosché, Mikael and Pellinen, Riikka and Kuittinen, Tero and Tuominen, Hannele and Ahlfors, Reetta and Keinänen, Markku and Saarma, Mart and Scheel, Dierk and Kangasjärvi, Jaakko}, month = mar, year = {2005}, pages = {1092--1104}, }
@article{ahlfors_arabidopsis_2004, title = {Arabidopsis {RADICAL}-{INDUCED} {CELL} {DEATH1} {Belongs} to the {WWE} {Protein}–{Protein} {Interaction} {Domain} {Protein} {Family} and {Modulates} {Abscisic} {Acid}, {Ethylene}, and {Methyl} {Jasmonate} {Responses}}, volume = {16}, issn = {1040-4651}, url = {https://academic.oup.com/plcell/article/16/7/1925/6010421}, doi = {10/c8t7cs}, abstract = {Abstract. Experiments with several Arabidopsis thaliana mutants have revealed a web of interactions between hormonal signaling. Here, we show that the Arabidops}, language = {en}, number = {7}, urldate = {2021-06-15}, journal = {The Plant Cell}, author = {Ahlfors, Reetta and Lång, Saara and Overmyer, Kirk and Jaspers, Pinja and Broscheé, Mikael and Tauriainen, Airi and Kollist, Hannes and Tuominen, Hannele and Belles-Boix, Enric and Piippo, Mirva and Inzeé, Dirk and Palva, E. Tapio and Kangasjärvi, Jaakko}, month = jul, year = {2004}, note = {Publisher: Oxford Academic}, pages = {1925--1937}, }
@article{tuominen_mutual_2004, title = {Mutual antagonism of ethylene and jasmonic acid regulates ozone-induced spreading cell death in {Arabidopsis}}, volume = {39}, issn = {1365-313X}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-313X.2004.02107.x}, doi = {10/ft54t9}, abstract = {Ethylene (ET) and jasmonic acid (JA) have opposite effects on ozone (O3)-induced spreading cell death; ET stimulates, and is required for the spreading cell death, whereas JA protects tissues. We studied the underlying molecular mechanisms with the O3-sensitive, JA-insensitive jasmonate resistant 1 (jar1), and the O3-tolerant, ET-insensitive ethylene insensitive 2 (ein2) mutants. Blocking ET perception pharmacologically with norbornadiene (NBD) in jar1, or ET signaling genetically in the jar1 ein2 double mutant prevented the spread of cell death. This suggests that EIN2 function is epistatic to JAR1, and that the JAR1-dependent JA pathway halts oxidative cell death by directly inhibiting ET signaling. JAR1-dependent suppression of the ET pathway was apparent also as increased EIN2-dependent gene expression and ET hypersensitivity of jar1. Physiological experiments suggested that the target of JA is upstream of Constitutive Triple Response 1 (CTR1), but downstream of ET biosynthesis. Gene expression analysis of 1-aminocyclopropane-1-carboxylic acid (ACC)-treated and O3-exposed ein2 and jar1 revealed reciprocal antagonism: the EIN2-mediated suppression of the JA pathway. The results imply that the O3-induced spreading cell death is stimulated by early, rapid accumulation of ET, which can suppress the protecting function of JA thereby allowing cell death to proceed. Extended spreading cell death induces late accumulation of JA, which inhibits the propagation of cell death through inhibition of the ET pathway.}, language = {en}, number = {1}, urldate = {2021-06-15}, journal = {The Plant Journal}, author = {Tuominen, Hannele and Overmyer, Kirk and Keinänen, Markku and Kollist, Hannes and Kangasjärvi, Jaakko}, year = {2004}, note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2004.02107.x}, keywords = {antagonism, ethylene, hormonal interactions, jasmonic acid, oxidative stress, ozone}, pages = {59--69}, }
link bibtex
@article{ahlfors_hormonal_2003, title = {Hormonal interactions and {ROS}-dependent cell death}, volume = {37}, issn = {1071-5762}, language = {English}, journal = {Free Radical Research}, author = {Ahlfors, R. and Keinanen, M. and Kollist, H. and Kuusela, T. and Lang, S. and Overmyer, K. and Pulkkinen, P. and Tuominen, H. and Kangasjarvi, J.}, year = {2003}, note = {Place: Abingdon Publisher: Taylor \& Francis Ltd WOS:000185828100016}, keywords = {⛔ No DOI found}, pages = {6--7}, }
@article{tuominen_cambial-region-specific_2000, title = {Cambial-{Region}-{Specific} {Expression} of the {Agrobacterium} iaa {Genes} in {Transgenic} {Aspen} {Visualized} by a {Linked} {uidA} {Reporter} {Gene}}, volume = {123}, issn = {0032-0889}, url = {https://www.ncbi.nlm.nih.gov/pmc/articles/PMC59021/}, abstract = {The level of indole-3-acetic acid (IAA) was locally modified in cambial tissues of transgenic aspen (Populus tremula L. × Populus tremuloides Michx.). We also demonstrate the use of a linked reporter gene to visualize the expression of the iaa genes. The rate-limiting bacterial IAA-biosynthetic gene iaaM and the reporter gene for β-glucuronidase (GUS), uidA, were each fused to the cambial-region-specific Agrobacterium rhizogenes rolC promoter and linked on the same T-DNA. In situ hybridization of the iaaM gene confirmed that histochemical analysis of GUS activity could be used to predict iaaM gene expression. Moreover, quantitative fluorometric analysis of GUS activity allowed estimation of the level of de novo production of IAA in transgenic lines carrying a single-copy insert of the iaaM, uidA T-DNA. Microscale analysis of the IAA concentration across the cambial region tissues showed an increase in IAA concentration of about 35\% to 40\% in the two transgenic lines, but no changes in the radial distribution pattern of IAA compared with wild-type plants. This increase did not result in any changes in the developmental pattern of cambial derivatives or the cambial growth rate, which emphasizes the importance of the radial distribution pattern of IAA in controlling the development of secondary xylem, and suggests that a moderate increase in IAA concentration does not necessarily stimulate growth.}, number = {2}, urldate = {2021-11-08}, journal = {Plant Physiology}, author = {Tuominen, Hannele and Puech, Laurence and Regan, Sharon and Fink, Siegfried and Olsson, Olof and Sundberg, Björn}, month = jun, year = {2000}, pmid = {10859183}, pmcid = {PMC59021}, pages = {531--542}, }
@article{overmyer_ozone-sensitive_2000, title = {Ozone-{Sensitive} {Arabidopsis} rcd1 {Mutant} {Reveals} {Opposite} {Roles} for {Ethylene} and {Jasmonate} {Signaling} {Pathways} in {Regulating} {Superoxide}-{Dependent} {Cell} {Death}}, volume = {12}, url = {https://www.ncbi.nlm.nih.gov/sites/ppmc/articles/PMC149124/}, doi = {10/bmk4p4}, abstract = {We have isolated a codominant Arabidopsis mutant, radical-induced cell death1 (rcd1), in which ozone (O[3] ) and extracellular superoxide (O[2] [•−] ), but not hydrogen peroxide, induce cellular O[2] [•−] accumulation ...}, language = {en}, number = {10}, urldate = {2021-11-08}, journal = {The Plant Cell}, author = {Overmyer, Kirk and Tuominen, Hannele and Kettunen, Reetta and Betz, Christian and Langebartels, Christian and Sandermann, Heinrich and Jr and Kangasjärvi, Jaakko}, month = oct, year = {2000}, pmid = {11041881}, note = {Publisher: Oxford University Press}, pages = {1849}, }
@article{regan_accurate_1999, title = {Accurate and high resolution in situ hybridization analysis of gene expression in secondary stem tissues}, volume = {19}, issn = {1365-313X}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1365-313X.1999.00536.x}, doi = {10.1046/j.1365-313X.1999.00536.x}, abstract = {Accurate in situ hybridization analysis in secondary stem tissues of plants has been hindered by specific characteristics of these tissues. First, secondary cell walls non-specifically bind probes used for in situ hybridization thus preventing gene expression analysis in the lignified regions of the stem, such as the xylem. Second, the mRNA in the cambial meristem and its recent derivatives are prone to inadequate fixation when conventional techniques are used. Here we describe an in situ hybridization technique which uses fast freezing and freeze substitution to cryoimmobilize the mRNA followed by embedding in a methacrylate resin for high-resolution analysis of gene expression. By using a transgenic poplar line harbouring rolC::uidA, rolC::iaaM, the gene expression pattern could be compared with histochemical GUS staining. This in situ hybridization technique results in superior preservation of cellular contents, retention of mRNA in all cell types in the poplar stem, a significant reduction of non-specific binding to secondary cell walls and a resolution not previously possible in secondary tissues. This technique will be particularly valuable for the expression analysis of genes involved in xylogenesis and wood formation.}, language = {en}, number = {3}, urldate = {2021-11-08}, journal = {The Plant Journal}, author = {Regan, Sharon and Bourquin, Veronica and Tuominen, Hannele and Sundberg, Björn}, year = {1999}, note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313X.1999.00536.x}, pages = {363--369}, }
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Svenska

Min forskning fokuserar på lignifiering och celldöd av xylemceller och hur dessa processer påverkar de kemiska och fysiskaliska egenskaperna i de sekundära cellväggarna och vedvävnader av kärlväxter. Vi använder två modellsystem; backtrav (Arabidopsis thaliana) som är en utmärkt modell för att förstå den molekylära och genetiska kontrollen av xylem differentiering, och asp (Populus tremula) som är praktisk för högupplösta studier av genuttryck, genetik, genomik och genfunktion i vedbildning.
Utveckling av xylemceller består av uppbyggnad av cellulosa-rika sekundära cellväggar tills de dör genom programmerad celldöd. Celldöd styr därför tjockleken på de sekundära cellväggarna genom att kontrollera livslängden på xylemcellerna. Vi har tidigare visat att celldöd kontrollerar också lignifiering av xylemcellerna. Arbete som utfördes i Zinnia elegans xylemcellkulturer visade att ligninbiosyntesen fortsätter även efter celldöd och att ligninpolymerisering sker först efter celldöd. Denna sekvens av händelser måste kontrolleras strikt i tid och plats. I mitt tidigare arbete har jag karakteriserat celldödsprocessen och identifierat faktorer som styr både lignifiering och celldöd av xylemcellerna. Det nuvarande målet är att identifiera funktionen av dessa faktorer. Ett av fokusområdena är signalering och funktionell karakterisering av metakaspas genfamiljen genom att använda genetiska och biokemiska metoder.
Det faktum att xylemcellernas livslängd styr cellväggarnas tjocklek och därmed omfattningen av produktionen av biomassa inom varje cell innebär att identifieringen av celldödskontrollerande faktorer skulle kunna användas för att öka den totala biomassaproduktionen i skogsträd. Vi har tagit fram två olika metoder för att undersöka kopplingen mellan xylemutveckling, de kemiska och fysikaliska egenskaper i den sekundära cellväggen, och egenskaperna hos trä. Det första tillvägagångssättet är att ändra uttryck för utvalda kandidatgener i transgen asp (Populus tremula) träd med cellspecifika promotorer och nyaste DNA-redigeringsteknik i syfte att fördröja xylemcelldöd och därigenom förbättra biomassaegenskaper. Det andra tillvägagångssättet utnyttjar den naturliga variationen inom en svensk asppopulation med målet att identifiera dels variationen i de sekundära cellväggs- och träegenskaperna och dels den underliggande molekylära mekanismen för denna variation genom en genomtäckande associationsstudie (GWAS).
Det långsiktiga målet i min forskning är att höja intresset för odling av snabbväxande lövträd, vilket bidrar till en snabbare övergång till hållbar produktion av biobaserade material, bränslen och energi.