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  • 1. Ahlfors, Reetta
    et al.
    Lång, Saara
    Overmyer, Kirk
    Jaspers, Pinja
    Brosché, Mikael
    Tauriainen, Airi
    Kollist, Hannes
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Belles-Boix, Enric
    Piippo, Mirva
    Inzé, Dirk
    Palva, E Tapio
    Kangasjärvi, Jaakko
    Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses.2004In: The Plant Cell, ISSN 1040-4651, Vol. 16, no 7, p. 1925-37Article in journal (Refereed)
    Abstract [en]

    Experiments with several Arabidopsis thaliana mutants have revealed a web of interactions between hormonal signaling. Here, we show that the Arabidopsis mutant radical-induced cell death1 (rcd1), although hypersensitive to apoplastic superoxide and ozone, is more resistant to chloroplastic superoxide formation, exhibits reduced sensitivity to abscisic acid, ethylene, and methyl jasmonate, and has altered expression of several hormonally regulated genes. Furthermore, rcd1 has higher stomatal conductance than the wild type. The rcd1-1 mutation was mapped to the gene At1g32230 where it disrupts an intron splice site resulting in a truncated protein. RCD1 belongs to the (ADP-ribosyl)transferase domain–containing subfamily of the WWE protein–protein interaction domain protein family. The results suggest that RCD1 could act as an integrative node in hormonal signaling and in the regulation of several stress-responsive genes.

  • 2.
    Bollhoner, Benjamin
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Prestele, Jakob
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Xylem cell death: emerging understanding of regulation and function2012In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 63, no 3, p. 1081-1094Article, review/survey (Refereed)
    Abstract [en]

    Evolutionary, as well as genetic, evidence suggests that vascular development evolved originally as a cell death programme that allowed enhanced movement of water in the extinct protracheophytes, and that secondary wall formation in the water-conducting cells evolved afterwards, providing mechanical support for effective long-distance transport of water. The extant vascular plants possess a common regulatory network to coordinate the different phases of xylem maturation, including secondary wall formation, cell death, and finally autolysis of the cell contents, by the action of recently identified NAC domain transcription factors. Consequently, xylem cell death is an inseparable part of the xylem maturation programme, making it difficult to uncouple cell death mechanistically from secondary wall formation, and thus identify the key factors specifically involved in regulation of cell death. Current knowledge suggests that the necessary components for xylem cell death are produced early during xylem differentiation, and cell death is prevented through the action of inhibitors and storage of hydrolytic enzymes in inactive forms in compartments such as the vacuole. Bursting of the central vacuole triggers autolytic hydrolysis of the cell contents, which ultimately leads to cell death. This cascade of events varies between the different xylem cell types. The water-transporting tracheary elements rely on a rapid cell death programme, with hydrolysis of cell contents taking place for the most part, if not entirely, after vacuolar bursting, while the xylem fibres disintegrate cellular contents at a slower pace, well before cell death. This review includes a detailed description of cell morphology, function of plant growth regulators, such as ethylene and thermospermine, and the action of hydrolytic nucleases and proteases during cell death of the different xylem cell types.

  • 3.
    Bollhöner, Benjamin
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Jokipii-Lukkari, Soile
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Bygdell, Joakim
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Stael, Simon
    Adriasola, Mathilda
    Muñiz, Luis
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Van Breusegem, Frank
    Ezcurra, Inés
    Wingsle, Gunnar
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    The function of two type II metacaspases in woody tissues of Populus trees2018In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 217, no 4, p. 1551-1565Article in journal (Refereed)
    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.

  • 4.
    Bollhöner, Benjamin
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Voss, Ute
    Prestele, Jakob
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Wilson, Michael
    Kenobi, Kim
    Viotti, Corrado
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    André, Domenique
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Lers, Amnon
    Bennett, Malcolm
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Programmed cell death in overlying tissues facilitates lateral root emergenceManuscript (preprint) (Other academic)
  • 5.
    Bollhöner, Benjamin
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Zhang, Bo
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Stael, Simon
    Denancé, Nicolas
    Overmyer, Kirk
    Goffner, Deborah
    Van Breusegem, Frank
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Post mortem function of AtMC9 in xylem vessel elements2013In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 200, no 2, p. 498-510Article in journal (Refereed)
    Abstract [en]

    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.

  • 6.
    Courtois-Moreau, Charleen L
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Pesquet, Edouard
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Sjödin, Andreas
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Muñiz, Luis
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Bollhöner, Benjamin
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Kaneda, Minako
    Department of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
    Samuels, Lacey
    Department of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
    Jansson, Stefan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    A unique program for cell death in xylem fibers of Populus stem2009In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 58, no 2, p. 260-274Article in journal (Refereed)
    Abstract [en]

    Maturation of the xylem elements involves extensive deposition of secondary cell-wall material and autolytic processes resulting in cell death. We describe here a unique type of cell-death program in xylem fibers of hybrid aspen (Populus tremula x P. tremuloides) stems, including gradual degradative processes in both the nucleus and cytoplasm concurrently with the phase of active cell-wall deposition. Nuclear DNA integrity, as determined by TUNEL (terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling) and Comet (single-cell gel electrophoresis) assays, was compromised early during fiber maturation. In addition, degradation of the cytoplasmic contents, as detected by electron microscopy of samples fixed by high-pressure freezing/freeze substitution (HPF-FS), was gradual and resulted in complete loss of the cytoplasmic contents well before the loss of vacuolar integrity, which is considered to be the moment of death. This type of cell death differs significantly from that seen in xylem vessels. The loss of vacuolar integrity, which is thought to initiate cell degradative processes in the xylem vessels, is one of the last processes to occur before the final autolysis of the remaining cell contents in xylem fibers. High-resolution microarray analysis in the vascular tissues of Populus stem, combined with in silico analysis of publicly available data repositories, suggests the involvement of several previously uncharacterized transcription factors, ethylene, sphingolipids and light signaling as well as autophagy in the control of fiber cell death.

  • 7.
    Escamez, Sacha
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    André, Domenique
    Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå S-901 83, Sweden.
    Zhang, Bo
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Bollhöner, Benjamin
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Pesquet, Edouard
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91 Stockholm, Sweden.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    METACASPASE9 modulates autophagy to confine cell death tothe target cells during Arabidopsis vascular xylem differentiation2016In: Biology Open, ISSN 2046-6390, Vol. 5, no 2, p. 122-129Article in journal (Refereed)
    Abstract [en]

    We uncovered that the level of autophagy in plant cells undergoingprogrammed cell death determines the fate of the surrounding cells.Our approach consisted of using Arabidopsis thaliana cell culturescapable of differentiating into two different cell types: vasculartracheary elements (TEs) that undergo programmed cell death(PCD) and protoplast autolysis, and parenchymatic non-TEs thatremain alive. The TE cell type displayed higher levels of autophagywhen expression of the TE-specific METACASPASE9 (MC9) wasreduced using RNAi (MC9-RNAi). Misregulation of autophagy in theMC9-RNAi TEs coincided with ectopic death of the non-TEs, implyingthe existence of an autophagy-dependent intercellular signallingfrom within the TEs towards the non-TEs. Viability of the non-TEswas restored when AUTOPHAGY2 (ATG2) was downregulatedspecifically in MC9-RNAi TEs, demonstrating the importance ofautophagy in the spatial confinement of cell death. Our resultssuggest that other eukaryotic cells undergoing PCD might also needto tightly regulate their level of autophagy to avoid detrimentalconsequences for the surrounding cells.

  • 8.
    Escamez, Sacha
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Latha Gandla, Madhavi
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Derba-Maceluch, Marta
    Lundqvist, Sven-Olof
    Mellerowicz, Ewa J.
    Jönsson, Leif J.
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    A collection of genetically engineered Populus trees reveals wood biomass traits that predict glucose yield from enzymatic hydrolysis2017In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 7, article id 15798Article in journal (Refereed)
    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.

  • 9.
    Escamez, Sacha
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Stael, Simon
    Vainonen, Julia P.
    Willems, Patrick
    Jin, Huiting
    Kimura, Sachie
    Van Breusegem, Frank
    Gevaert, Kris
    Wrzaczek, Michael
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Extracellular peptide Kratos restricts cell death during vascular development and stress in Arabidopsis2019In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 70, no 7, p. 2199-2210Article in journal (Refereed)
    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.

  • 10.
    Escamez, Sacha
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Contribution of cellular autolysis to tissular functions during plant development2017In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 35, p. 124-130Article, review/survey (Refereed)
    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.

  • 11.
    Escamez, Sacha
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Programmes of cell death and autolysis in tracheary elements: when a suicidal cell arranges its own corpse removal2014In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 65, no 5, p. 1313-1321Article, review/survey (Refereed)
    Abstract [en]

    Differentiation of tracheary elements (TEs) is finalized by programmed cell death (PCD) and autolysis. This review integrates TE differentiation, PCD, and autolysis in a biological and evolutionary context.Tracheary element (TE) differentiation represents a unique system to study plant developmental programmed cell death (PCD). TE PCD occurs after deposition of the secondary cell walls when an unknown signal induces tonoplast rupture and the arrest of cytoplasmic streaming. TE PCD is tightly followed by autolysis of the protoplast and partial hydrolysis of the primary cell walls. This review integrates TE differentiation, programmed cell death (PCD), and autolysis in a biological and evolutionary context. The collective evidence from the evolutionary and molecular studies suggests that TE differentiation consists primarily of a programme for cell death and autolysis under the direct control of the transcriptional master switches VASCULAR NAC DOMAIN 6 (VND6) and VND7. In this scenario, secondary cell walls represent a later innovation to improve the water transport capacity of TEs which necessitates transcriptional regulators downstream of VND6 and VND7. One of the most fascinating features of TEs is that they need to prepare their own corpse removal by expression and accumulation of hydrolases that are released from the vacuole after TE cell death. Therefore, TE differentiation involves, in addition to PCD, a programmed autolysis which is initiated before cell death and executed post-mortem. It has recently become clear that TE PCD and autolysis are separate processes with separate molecular regulation. Therefore, the importance of distinguishing between the cell death programme per se and autolysis in all plant PCD research and of careful description of the morphological, biochemical, and molecular sequences in each of these processes, is advocated.

  • 12. Fracheboud, Yvan
    et al.
    Luquez, Virginia
    Björkén, Lars
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Sjödin, Andreas
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Jansson, Stefan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    The control of autumn senescence in European aspen2009In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 149, no 4, p. 1982-1991Article in journal (Refereed)
    Abstract [en]

    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.

  • 13.
    Jokipii-Lukkari, Soile
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Sveriges Lantbruksuniversitet, SE-901 83 Umeå, Sweden.
    Delhomme, Nicolas
    Schiffthaler, Bastian
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Mannapperuma, Chanaka
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Prestele, Jakob
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Nilsson, Ove
    Street, Nathaniel
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Transcriptional Roadmap to Seasonal Variation in Wood Formation of Norway Spruce2018In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 176, no 4, p. 2851-2870Article in journal (Refereed)
    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.

  • 14.
    Jokipii-Lukkari, Soile
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology,Swedish University of Agricultural Sciences, SE-901 84 Umeå, Sweden.
    Sundell, David
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Nilsson, Ove
    Hvidsten, Torgeir R.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1430 Ås, Norway.
    Street, Nathaniel R.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    NorWood: a gene expression resource for evo-devo studies of conifer wood development2017In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 216, no 2, p. 482-494Article in journal (Refereed)
    Abstract [en]

    The secondary xylem of conifers is composed mainly of tracheids that differ anatomically and chemically from angiosperm xylem cells. There is currently no high-spatial-resolution data available profiling gene expression during wood formation for any coniferous species, which limits insight into tracheid development.

    RNA-sequencing data from replicated, high-spatial-resolution section series throughout the cambial and woody tissues of Picea abies were used to generate the NorWood.conGenIE.org web resource, which facilitates exploration of the associated gene expression profiles and co-expression networks.

    Integration within PlantGenIE.org enabled a comparative regulomics analysis, revealing divergent co-expression networks between P. abies and the two angiosperm species Arabidopsis thaliana and Populus tremula for the secondary cell wall (SCW) master regulator NAC Class IIB transcription factors. The SCW cellulose synthase genes (CesAs) were located in the neighbourhoods of the NAC factors in Athaliana and P. tremula, but not in Pabies. The NorWood co-expression network enabled identification of potential SCW CesA regulators in P. abies.

    The NorWood web resource represents a powerful community tool for generating evo-devo insights into the divergence of wood formation between angiosperms and gymnosperms and for advancing understanding of the regulation of wood development in P. abies.

  • 15.
    Keech, Olivier
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Pesquet, Edouard
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Sjödin, Andreas
    Jansson, Stefan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Ahad, Abdul
    Gardeström, Per
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Disruption of the microtubules during dark-induced senescenceManuscript (Other (popular science, discussion, etc.))
  • 16. Milhinhos, Ana
    et al.
    Prestele, Jakob
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Bollhöner, Benjamin
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Matos, Andreia
    Vera-Sirera, Francisco
    Rambla, Jose L
    Ljung, Karin
    Carbonell, Juan
    Blazquez, Miguel A
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Miguel, Celia M
    Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem2013In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 75, no 4, p. 685-698Article in journal (Refereed)
    Abstract [en]

    Polyamines are small polycationic amines that are widespread in living organisms. Thermospermine, synthesized by thermospermine synthase ACAULIS5 (ACL5), was recently shown to be an endogenous plant polyamine. Thermospermine is critical for proper vascular development and xylem cell specification, but it is not known how thermospermine homeostasis is controlled in the xylem. We present data in the Populus model system supporting the existence of a negative feedback control of thermospermine levels in stem xylem tissues, the main site of thermospermine biosynthesis. While over-expression of the ACL5 homologue in Populus, POPACAULIS5, resulted in strong up-regulation of ACL5 expression and thermospermine accumulation in leaves, the corresponding levels in the secondary xylem tissues of the stem were similar or lower than those in the wild-type. POPACAULIS5 over-expression had a negative effect on accumulation of indole-3-acetic acid, while exogenous auxin had a positive effect on POPACAULIS5 expression, thus promoting thermospermine accumulation. Further, over-expression of POPACAULIS5 negatively affected expression of the classIII homeodomain leucine zipper (HD-ZipIII) transcription factor gene PttHB8, a homologue of AtHB8, while up-regulation of PttHB8 positively affected POPACAULIS5 expression. These results indicate that excessive accumulation of thermospermine is prevented by a negative feedback control of POPACAULIS5 transcript levels through suppression of indole-3-acetic acid levels, and that PttHB8 is involved in the control of POPACAULIS5 expression. We propose that this negative feedback loop functions to maintain steady-state levels of thermospermine, which is required for proper xylem development, and that it is dependent on the presence of high concentrations of endogenous indole-3-acetic acid, such as those present in the secondary xylem tissues.

  • 17. Minina, E. A.
    et al.
    Coll, N. S.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Bozhkov, P. V.
    Metacaspases versus caspases in development and cell fate regulation2017In: Cell Death and Differentiation, ISSN 1350-9047, E-ISSN 1476-5403, Vol. 24, no 8, p. 1314-1325Article, review/survey (Refereed)
    Abstract [en]

    Initially found to be critically involved in inflammation and apoptosis, caspases have since then been implicated in the regulation of various signaling pathways in animals. How caspases and caspase-mediated processes evolved is a topic of great interest and hot debate. In fact, caspases are just the tip of the iceberg, representing a relatively small group of mostly animal-specific enzymes within a broad family of structurally related cysteine proteases (family C14 of CD clan) found in all kingdoms of life. Apart from caspases, this family encompasses para-and metacaspases, and all three groups of proteases exhibit significant variation in biochemistry and function in vivo. Notably, metacaspases are present in all eukaryotic lineages with a remarkable absence in animals. Thus, metacaspases and caspases must have adapted to operate under distinct cellular and physiological settings. Here we discuss biochemical properties and biological functions of metacaspases in comparison to caspases, with a major focus on the regulation of developmental aspects in plants versus animals.

  • 18.
    Moreau, Charleen
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Aksenov, Nikolay
    García-Lorenzo, Maribel
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Segerman, Bo
    Funk, Christiane
    Umeå University, Faculty of Science and Technology, Department of Chemistry. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Nilsson, Peter
    Jansson, Stefan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    A genomic approach to investigate developmental cell death in woody tissues of Populus trees2005In: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 6, no 4, p. R34:1-14Article in journal (Refereed)
    Abstract [en]

    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.

  • 19.
    Muñiz, Luis
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Minguet, Eugenio G
    Singh, Sunil Kumar
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Pesquet, Edouard
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Vera-Sirera, Francisco
    Moreau-Courtois, Charleen L
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Carbonell, Juan
    Blázquez, Miguel A
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death.2008In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 135, no 15, p. 2573-82Article in journal (Refereed)
    Abstract [en]

    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 thaliana hypocotyls, 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.

  • 20. Nystedt, Björn
    et al.
    Street, Nathaniel Robert
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Wetterbom, Anna
    Zuccolo, Andrea
    Lin, Yao-Cheng
    Scofield, Douglas G.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Vezzi, Francesco
    Delhomme, Nicolas
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Giacomello, Stefania
    Alexeyenko, Andrey
    Vicedomini, Riccardo
    Sahlin, Kristoffer
    Sherwood, Ellen
    Elfstrand, Malin
    Gramzow, Lydia
    Holmberg, Kristina
    Hällman, Jimmie
    Keech, Olivier
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Klasson, Lisa
    Koriabine, Maxim
    Kucukoglu, Melis
    Käller, Max
    Luthman, Johannes
    Lysholm, Fredrik
    Niittylä, Totte
    Olson, Åke
    Rilakovic, Nemanja
    Ritland, Carol
    Rosselló, Josep A.
    Sena, Juliana
    Svensson, Thomas
    Talavera-López, Carlos
    Theißen, Günter
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Vanneste, Kevin
    Wu, Zhi-Qiang
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Zhang, Bo
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Zerbe, Philipp
    Arvestad, Lars
    Bhalerao, Rishikesh
    Bohlmann, Joerg
    Bousquet, Jean
    Gil, Rosario Garcia
    Hvidsten, Torgeir R.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    de Jong, Pieter
    MacKay, John
    Morgante, Michele
    Ritland, Kermit
    Sundberg, Björn
    Thompson, Stacey Lee
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Van de Peer, Yves
    Andersson, Björn
    Nilsson, Ove
    Ingvarsson, Pär K.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Lundeberg, Joakim
    Jansson, Stefan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    The Norway spruce genome sequence and conifer genome evolution2013In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 497, no 7451, p. 579-584Article in journal (Refereed)
    Abstract [en]

    Conifers have dominated forests for more than 200 million years and are of huge ecological and economic importance. Here we present the draft assembly of the 20-gigabase genome of Norway spruce (Picea abies), the first available for any gymnosperm. The number of well-supported genes (28,354) is similar to the >100 times smaller genome of Arabidopsis thaliana, and there is no evidence of a recent whole-genome duplication in the gymnosperm lineage. Instead, the large genome size seems to result from the slow and steady accumulation of a diverse set of long-terminal repeat transposable elements, possibly owing to the lack of an efficient elimination mechanism. Comparative sequencing of Pinus sylvestris, Abies sibirica, Juniperus communis, Taxus baccata and Gnetum gnemon reveals that the transposable element diversity is shared among extant conifers. Expression of 24-nucleotide small RNAs, previously implicated in transposable element silencing, is tissue-specific and much lower than in other plants. We further identify numerous long (>10,000 base pairs) introns, gene-like fragments, uncharacterized long non-coding RNAs and short RNAs. This opens up new genomic avenues for conifer forestry and breeding.

  • 21.
    Obudulu, Ogonna
    et al.
    Umeå University, Faculty of Science and Technology, Department of Chemistry. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, Sweden.
    Mähler, Niklas
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Faculty of Chemistry, Biotechnology and Food Science, Norwegian, University of Life Sciences, 1432 Ås, Norway.
    Skotare, Tomas
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Bygdell, Joakim
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Abreu, Ilka N.
    Ahnlund, Maria
    Latha Gandla, Madhavi
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Petterle, Anna
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Moritz, Thomas
    Hvidsten, Torgeir R.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Faculty of Chemistry, Biotechnology and Food Science, Norwegian, University of Life Sciences, 1432 Ås, Norway.
    Jönsson, Leif J.
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Wingsle, Gunnar
    Trygg, Johan
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees2018In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 19, article id 11Article in journal (Refereed)
    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.

  • 22. Overmyer, Kirk
    et al.
    Brosché, Mikael
    Pellinen, Riikka
    Kuittinen, Tero
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Ahlfors, Reetta
    Keinänen, Markku
    Saarma, Mart
    Scheel, Dierk
    Kangasjärvi, Jaakko
    Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant.2005In: Plant Physiology, ISSN 0032-0889, Vol. 137, no 3, p. 1092-104Article in journal (Refereed)
    Abstract [en]

    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.

  • 23. Overmyer, Kirk
    et al.
    Kollist, Hannes
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Betz, Christian
    Langebartels, Christian
    Wingsle, Gunnar
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Kangasjärvi, Saijaliisa
    Brader, Günter
    Mullineaux, Phil
    Kangasjärvi, Jaakko
    Complex phenotypic profiles leading to ozone sensitivity in Arabidopsis thaliana mutants.2008In: Plant, Cell and Environment, ISSN 1365-3040, Vol. 31, no 9, p. 1237-49Article in journal (Refereed)
    Abstract [en]

    enetically tractable model plants offer the possibility of defining the plant O3 response at the molecular level. To this end, we have isolated a collection of ozone (O3)-sensitive mutants of Arabidopsis thaliana. Mutant phenotypes and genetics were characterized. Additionally, parameters associated with O3 sensitivity were analysed, including stomatal conductance, sensitivity to and accumulation of reactive oxygen species, antioxidants, stress gene-expression and the accumulation of stress hormones. Each mutant has a unique phenotypic profile, with O3 sensitivity caused by a unique set of alterations in these systems. O3 sensitivity in these mutants is not caused by gross deficiencies in the antioxidant pathways tested here. The rcd3 mutant exhibits misregulated stomata. All mutants exhibited changes in stress hormones consistent with the known hormonal roles in defence and cell death regulation. One mutant, dubbed re-8, is an allele of the classic leaf development mutant reticulata and exhibits phenotypes dependent on light conditions. This study shows that O3 sensitivity can be determined by deficiencies in multiple interacting plant systems and provides genetic evidence linking these systems.

  • 24.
    Pesquet, Edouard
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Ethylene stimulates tracheary element differentiation in Zinnia elegans cell cultures2011In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 190, no 1, p. 138-149Article in journal (Refereed)
    Abstract [en]

    • The exact role of ethylene in xylogenesis remains unclear, but the Zinnia elegans cell culture system provides an excellent model with which to study its role during the differentiation of tracheary elements (TEs) in vitro. • Here, we analysed ethylene homeostasis and function during Z. elegans TE differentiation using biochemical, molecular and pharmacological methods. • Ethylene evolution was confined to specific stages of TE differentiation. It was found to peak at the time of TE maturation and to correlate with the activity of the ethylene biosynthetic 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase. The ethylene precursor ACC was exported and accumulated to high concentrations in the extracellular medium, which also displayed a high capacity to convert ACC into ethylene. The effects of adding inhibitors of the ethylene biosynthetic ACC synthase and ACC oxidase enzymes to the TE cultures demonstrated for the first time strict dependence of TE differentiation on ethylene biosynthesis and a stimulatory effect of ethylene on the rate of TE differentiation. • In a whole-plant context, our results suggest that ethylene synthesis occurs in the apoplast of the xylem elements and that ethylene participates, in a paracrine manner, in the control of the cambial stem cell pool size during secondary xylem formation.

  • 25.
    Pesquet, Edouard
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Unravelling ethylene biosynthesis and its role during tracheary element formation in Zinnia elegans2007In: Advances in plant ethylene research: proceedings of the 7th international symposium on the plant hormone ethylene / [ed] Angelo Ramina, Caren Chang, Jim Giovannoni, Harry Klee, Pierdomenico Perata, Ernst Woltering, Dordrecht: Springer Netherlands, 2007, p. 147-149Conference paper (Refereed)
    Abstract [en]

    Xylem is the plant vascular tissue responsible for raw sap conduction. It comprises two main types of cells that are derived from differentiating cambium: tracheary elements (TEs) and fibres that have conducting and mechanical role, respectively. Xylem formation is a developmental process and is under strict hormonal control involving a stew of phytohormones including auxin, cytokinin and ethylene.

  • 26.
    Pesquet, Edouard
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Zhang, Bo
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Gorzsas, Andras
    Puhakainen, Tuula
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Serk, Henrik
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Escamez, Sacha
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Barbier, Odile
    Gerber, Lorenz
    Courtois-Moreau, Charleen
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Alatalo, Edward
    Paulin, Lars
    Kangasjärvi, Jaakko
    Sundberg, Björn
    Goffner, Deborah
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans2013In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 25, no 4, p. 1314-1328Article in journal (Refereed)
    Abstract [en]

    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-cellautonomous manner, thus enabling the postmortem lignification of TEs.

  • 27.
    Serk, Henrik
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Gorzsás, András
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Pesquet, Edouard
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Cooperative lignification of xylem tracheary elements2015In: Plant Signalling & Behavior, ISSN 1559-2316, E-ISSN 1559-2324, Vol. 10, no 4, article id e1003753Article in journal (Refereed)
    Abstract [en]

    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.

  • 28.
    Seyfferth, Carolin
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Wessels, Bernard A.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Gorzsás, András
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Love, Jonathan W.
    Rüggeberg, Markus
    Delhomme, Nicolas
    Vain, Thomas
    Antos, Kamil
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Sundberg, Björn
    Felten, Judith
    Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen2019In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 10, article id 1101Article in journal (Refereed)
    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.

  • 29.
    Seyfferth, Carolin
    et al.
    Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Wessels, Bernard
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Jokipii-Lukkari, Soile
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Sundberg, Björn
    Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Delhomme, Nicolas
    Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Felten, Judith
    Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Ethylene-Related Gene Expression Networks in Wood Formation2018In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 9, article id 272Article in journal (Refereed)
    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.

  • 30. Seyfferth, Carolin
    et al.
    Wessels, Bernard
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Vahala, J.
    Kangasjärvi, J.
    Bauer, G.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Eder, M.
    Delhomme, Nicolas
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Felten, J.
    Populus ERF85 mediates the transition between xylem cell expansion and secondary cell wall formation in hybrid aspenManuscript (preprint) (Other academic)
  • 31.
    Sundell, David
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Street, Nathaniel R.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Kumar, Manoj
    Mellerowicz, Ewa J.
    Kucukoglu, Melis
    Johnsson, Christoffer
    Kumar, Vikash
    Mannapperuma, Chanaka
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Delhomme, Nicolas
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Nilsson, Ove
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Pesquet, Edouard
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Ecology, Environment and Plant Sciences, Stockholm University, 106 91 Stockholm, Sweden.
    Fischer, Urs
    Niittyla, Totte
    Sundberg, Bjorn
    Hvidsten, Torgeir R.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Chemistry, Biotechnology and Food Sciences, Norwegian University of Life Sciences, 1433 Ås, Norway.
    AspWood: High-Spatial-Resolution Transcriptome Profiles Reveal Uncharacterized Modularity of Wood Formation in Populus tremula2017In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 29, no 7, p. 1585-1604Article in journal (Refereed)
    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.

  • 32.
    Sundell, David
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Street, Nathaniel R
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Kumar, Manoj
    Mellerowicz, Ewa J
    Kucukoglu, Melis
    Johnsson, Christoffer
    Kumar, Vikash
    Mannapperuma, Chanaka
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Nilsson, Ove
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Pesquet, Edouard
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Ecology, Environment and Plant Sciences, Stockholm University, Sweden.
    Fischer, Urs
    Niittyla, Totte
    Sundberg, Bjoern
    Hvidsten, Torgeir R
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Chemistry, Biotechnology and Food Sciences, Norwegian University of Life Sciences, Ås, Norway.
    High-spatial-resolution transcriptome profiling reveals uncharacterized regulatory complexity underlying cambial growth and wood formation in Populus tremula2016Manuscript (preprint) (Other academic)
    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, however, efforts to engineer new, elite varieties are constrained by the lack of a comprehensive understanding of the transcriptional network underlying cambial growth and wood formation. We generated RNA Sequencing transcriptome data for four mature, wild-growing aspens (Populus tremula) from high-spatial-resolution tangential cryosection series spanning the secondary phloem, vascular cambium, expanding and secondary cell wall forming xylem cells, cell death zone and the previous years annual ring. The transcriptome comprised 28,294 expressed, previously annotated protein-coding genes, 78 novel protein-coding genes and 567 long intergenic non-coding RNAs. Most paralogs originating from the Salicaceae whole genome duplication had diverged expression, with the notable exception of those with high expression during secondary cell wall deposition. We performed co-expression network analysis to identify central transcriptional modules and associated several of these with known biological processes. This revealed previously uncharacterized complexity underlying the regulation of cambial growth and wood formation, with modules forming a continuum of activated processes across the tissues. The high spatial resolution suggested novel roles for known genes involved in xylan and cellulose biosynthesis, regulators of xylem vessel and fiber differentiation and components of lignification. The associated web resource (AspWood, http://aspwood.popgenie.org) integrates the data within a set of interactive tools for exploring the co-expression network of cambial growth and wood formation.

  • 33.
    Tuominen, Hannele
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Overmyer, Kirk
    Keinänen, Markku
    Kollist, Hannes
    Kangasjärvi, Jaakko
    Mutual antagonism of ethylene and jasmonic acid regulates ozone-induced spreading cell death in Arabidopsis.2004In: The Plant Journal, ISSN 0960-7412, Vol. 39, no 1, p. 59-69Article in journal (Refereed)
    Abstract [en]

    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.

  • 34. Vera-Sirera, Francisco
    et al.
    De Rybel, Bert
    Urbez, Cristina
    Kouklas, Evangelos
    Pesquera, Marta
    Camilo Alvarez-Mahecha, Juan
    Minguet, Eugenio G.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Carbonell, Juan
    Borst, Jan Willem
    Weijers, Dolf
    Blazquez, Miguel A.
    A bHLH-Based Feedback Loop Restricts Vascular Cell Proliferation in Plants2015In: Developmental Cell, ISSN 1534-5807, E-ISSN 1878-1551, Vol. 35, no 4, p. 432-443Article in journal (Refereed)
    Abstract [en]

    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 (LHVV) 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.

  • 35. Vera-Sirera, Francisco
    et al.
    Minguet, Eugenio G.
    Singh, Sunil Kumar
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Ljung, Karin
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Blazquez, Miguel A.
    Carbonell, Juan
    Role of polyamines in plant vascular development2010In: Plant physiology and biochemistry (Paris), ISSN 0981-9428, E-ISSN 1873-2690, Vol. 48, no 7, p. 534-539Article in journal (Refereed)
    Abstract [en]

    Several pieces of evidence suggest a role for polyamines in the regulation of plant vascular development. For instance, polyamine oxidase gene expression has been shown to be associated with lignification, and downregulation of S-adenosylmethionine decarboxylase causes dwarfism and enlargement of the vasculature. Recent evidence from Arabidopsis thaliana also suggests that the active polyamine in the regulation of vascular development is the tetraamine thermospermine. Thermospermine biosynthesis is catalyzed by the aminopropyl transferase encoded by ACAULIS5, which is specifically expressed in xylem vessel elements. Both genetic and molecular evidence support a fundamental role for thermospermine in preventing premature maturation and death of the xylem vessel elements. This safeguard action of thermospermine has significant impact on xylem cell morphology, cell wall patterning and cell death as well as on plant growth in general. This manuscript reviews recent reports on polyamine function and places polyamines in the context of the known regulatory mechanisms that govern vascular development. (C) 2010 Elsevier Masson SAS. All rights reserved.

  • 36.
    Wessels, Bernard
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Seyfferth, Carolin
    Escamez, Sacha
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Vain, T.
    Antos, K.
    Vahala, J.
    Delhomme, Nicolas
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Kangasjärvi, J.
    Eder, M.
    Felten, J.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    An AP/ERF transcription factor ERF139 affects growth and lignin deposition in hybrid aspenManuscript (preprint) (Other academic)
  • 37.
    Wessels, Bernard
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Seyfferth, Carolin
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Escamez, Sacha
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Vain, Thomas
    Antos, Kamil
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Vahala, Jorma
    Delhomme, Nicolas
    Kangasjarvi, Jaakko
    Eder, Michaela
    Felten, Judith
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    An AP2/ERF transcription factor ERF139 coordinates xylem cell expansion and secondary cell wall deposition2019In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137Article in journal (Refereed)
    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.

  • 38.
    Wessels, Bernard
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Seyfferth, Carolin
    Vain, T.
    Antos, K.
    Felten, J.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Ethylene suppresses vessel element formation during the tension wood response of hybrid aspenManuscript (preprint) (Other academic)
  • 39. Wrzaczek, Michael
    et al.
    Vainonen, Julia P.
    Stael, Simon
    Tsiatsiani, Liana
    Help-Rinta-Rahko, Hanna
    Gauthier, Adrien
    Kaufholdt, David
    Bollhöner, Benjamin
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Lamminmaki, Airi
    Staes, An
    Gevaert, Kris
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Van Breusegem, Frank
    Helariutta, Yka
    Kangasjarvi, Jaakko
    GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis2015In: EMBO Journal, ISSN 0261-4189, E-ISSN 1460-2075, Vol. 31, no 1, p. 55-66Article in journal (Refereed)
    Abstract [en]

    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.

  • 40.
    Zhang, Bo
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tremousaygue, Dominique
    Denancé, Nicolas
    van Esse, H. Peter
    Hörger, Anja C.
    Dabos, Patrick
    Goffner, Deborah
    Thomma, Bart P. H. J.
    van der Hoorn, Renier A. L.
    Tuominen, Hannele
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    PIRIN2 stabilizes cysteine protease XCP2 and increases susceptibility to the vascular pathogen Ralstonia solanacearum in Arabidopsis2014In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 79, no 6, p. 1009-1019Article in journal (Refereed)
    Abstract [en]

    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.

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