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.

Touminen Hannele 1150 2

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 lifetime 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 functionally characterise several of these newly identified factors. 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.

HanneleTuominen bild

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.


sweden_greySvensk sammanfattning

Publication list

  1. Overexpression of vesicle-associated membrane protein PttVAP27-17 as a tool to improve biomass production and the overall saccharification yields in Populus trees
    Biotechnol Biofuels. 2021, 14(1):43
  2. ACAULIS5 Is Required for Cytokinin Accumulation and Function During Secondary Growth of Populus Trees
    Front Plant Sci 2020, 11:601858
  3. ETHYLENE RESPONSE FACTOR 115 integrates jasmonate and cytokinin signaling machineries to repress adventitious rooting in Arabidopsis
    New Phytol. 2020 Jul 7 [Epub ahead of print]
  4. The chromatin-modifying protein HUB2 is involved in the regulation of lignin composition in xylem vessels
    J Exp Bot. 2020, 71(18):5484-5494
  5. Classification and Nomenclature of Metacaspases and Paracaspases: No More Confusion with Caspases
    Mol Cell. 2020, 77(5):927-929
  6. Cell death in cells overlying lateral root primordia facilitates organ growth in Arabidopsis
    Current Biology 2020, 30(3):455-464
  7. PIRIN2 suppresses S-type lignin accumulation in a non-cell-autonomous manner in Arabidopsis xylem elements
    New Phytol. 2019 Oct 18 [Epub ahead of print]
  8. Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
    FRONTIERS IN PLANT SCIENCE 2019, 10
  9. An AP2/ERF transcription factor ERF139 coordinates xylem cell expansion and secondary cell wall deposition
    New Phytol. 2019, 224(4):1585-1599
  10. High Spatial Resolution Profiling in Tree Species
    Annual Plant Reviews Online 2019
  11. Extracellular peptide Kratos restricts cell death during vascular development and stress in Arabidopsis
    J Exp Bot. 2019, 70(7):2199-2210
  12. Ethylene-Related Gene Expression Networks in Wood Formation
    FRONTIERS IN PLANT SCIENCE 2018, 9:272
  13. Transcriptional roadmap to seasonal variation in wood formation of Norway spruce
    Plant Physiol. 2018, 176(4):2851-2870
  14. A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of​ ​​Populus​​ ​trees
    BMC Genomics. 2018, 19(1)
  15. The function of two type II metacaspases in woody tissues of Populus trees
    New Phytol. 2018, 217(4):1551-1565
  16. A collection of genetically engineered Populus trees reveals wood biomass traits that predict glucose yield from enzymatic hydrolysis
    Sci Rep 2017, 7(1):15798
  17. Metacaspases versus caspases in development and cell fate regulation
    Cell Death Differ. 2017, 24(8):1314-1325
  18. AspWood: High-spatial-resolution transcriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula
    Plant Cell. 2017, 29 (7):1585-1604
  19. NorWood: a gene expression resource for evo-devo studies of conifer wood development
    New Phytol. 2017, 216(2):482-494
  20. Quick Histochemical Staining Methods to Detect Cell Death in Xylem Elements of Plant Tissues
    Methods Mol Biol. 2017;1544:27-36
  21. Contribution of cellular autolysis to tissular functions during plant development
    Curr Opin Plant Biol. 2017, 35:124-130
  22. METACASPASE9 modulates autophagy to confine cell death to the target cells during Arabidopsis vascular xylem differentiation
    Biol Open. 2016, 5(2):122-129
  23. A bHLH-Based Feedback Loop Restricts Vascular Cell Proliferation in Plants
    Dev Cell. 2015, 35(4):432-443
  24. Life Beyond Death: The Formation of Xylem Sap Conduits
    In: Gunawardena A., McCabe P. (eds) Plant Programmed Cell Death. Springer, Cham. (2015) pp 55-76
  25. Cooperative Lignification of Xylem Tracheary Elements
    Plant Signal Behav. 2015;10(4):e1003753
  26. GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis
    EMBO J. 2015, 31(1):55-66
  27. PIRIN2 stabilizes cysteine protease XCP2 and increases susceptibility to the vascular pathogen Ralstonia solanacearum in Arabidopsis
    Plant J. 2014, 79(6):1009-1019
  28. Programmes of cell death and autolysis in tracheary elements: when a suicidal cell arranges its own corpse removal
    J Exp Bot. 2014; 65(5):1313-1321
  29. Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem
    The Plant Journal 2013, 75:685–698
  30. Post mortem function of AtMC9 in xylem vessel elements
    New Phytol. 2013, 200(2):498-510
  31. The Norway spruce genome sequence and conifer genome evolution
    Nature 2013; 497(7451):579-584
  32. Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans
    Plant Cell. 2013; 25(4):1314-1328
  33. Bollhöner B, Prestele J, Tuominen H
    Xylem cell death: emerging understanding of regulation and function
    Journal of Experimental Botany 2012 63(3):1081-94
  34. Pesquet E, Tuominen H
    Ethylene stimulates tracheary element differentiation in Zinnia elegans cell cultures
    New Phytologist: 2011 190:138-149
  35. Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blázquez MA, Carbonell J
    Role of polyamines in plant vascular development
    Plant Physiology and Biochemistry: 2010 48:534-539
  36. Fracheboud Y, Luquez V, Björkén L, Sjödin A, Tuominen H, Jansson S
    The control of autumn senescence in European aspen
    Plant Physiology: 2009 149:1982-1991
  37. Fracheboud Y, Luquez V, Björkén L, Sjödin A, Tuominen H, Jansson S
    The control of autumn senescence in European aspen
    Plant Physiology: 2009 149:1982-1991
  38. Courtois-Moreau CL, Pesquet E, Sjödin A, Muniz L, Bollhöner B, Kaneda M, Samuels L, Jansson S, Tuominen H
    A unique program for cell death in xylem fibers of Populus stem
    The Plant Journal: 2009 58(2):260-274
  39. Overmeyer K, Kollist H, Tuominen H, Betz, C, Langebartels C, Wingsle G, Kangasjärvi S, Brader G, Mullineaux P, Kangasjärvi J
    Complex phenotypic profiles leading to ozone sensitivity in Arabidopsis thaliana mutants
    Plant, Cell and Environment: 2008 31: 1237-1249
  40. Overmeyer K, Kollist H, Tuominen H, Betz, C, Langebartels C, Wingsle G, Kangasjärvi S, Brader G, Mullineaux P, Kangasjärvi J
    Complex phenotypic profiles leading to ozone sensitivity in Arabidopsis thaliana mutants
    Plant, Cell and Environment: 2008 31: 1237-1249
  41. Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau-Courtois CL, Carbonell J, Blázquez MA, Tuominen H
    ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death
    Development: 2008 135:2573-2582
  42. Muniz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau-Courtois CL, Carbonell J, Blázquez MA, Tuominen H
    ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death
    Development: 2008 135:2573-2582
  43. Keech O, Pesquet E, Ahad A, Askne A, Nordvall D, Vodnala SM, Tuominen H, Hurry V, Dizengremel P, Gardeström P
    The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves
    Plant, Cell and Environment: 2007 30:1523-1534
  44. Ruonala R, Rinne PLH, Baghour M, Moritz T, Tuominen H, Kangasjarvi J
    Transitions in the functioning of the shoot apical meristem in birch (Betula pendula) involve ethylene
    Plant Journal: 2006 46:628-640
  45. Moreau C, Aksenov N, Lorenzo MG, Segerman B, Funk C, Nilsson P, Jansson S, Tuominen H
    A genomic approach to investigate developmental cell death in woody tissues of Populus trees
    Genome Biology: 2005 6:R34
  46. Overmyer K, BroschE M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinanen M, Saarma M, Scheel D, Kangasjarvi J
    Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant
    Plant Physiol: 2005 137:1092-1104
  47. Ahlfors R, Lång S, Overmyer K, Jaspers P, BroschE M, Tauriainen A, Kollist H, Tuominen H, Boix EB, Piippo M, InzE D, Palva ET, Kangasjarvi J
    Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses
    Plant Cell: 2004 16:1925-1937
  48. Tuominen H, Overmyer K, Keinanen M, Kollist H, Kangasjarvi J
    Mutual antagonism of ethylene and jasmonic acid regulates ozone-induced spreading cell death in Arabidopsis
    Plant J: 2004 39:59-69
  49. Ahlfors R, Keinanen M, Kollist H, Kuusela T, Lang S, Overmyer K, Pulkkinen P, Tuominen H, Kangasjarvi J
    Hormonal interactions and ROS-dependent cell death
    Free Radical Research: 2003 37:6-7
  50. Vahala J, Ruonala R, Keinanen M, Tuominen H, Kangasjarvi J
    Ethylene insensitivity modulates ozone-induced cell death in birch
    Plant Physiol: 2003 132:185-195
  51. Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H, Kangasjarvi J
    Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death
    Plant Cell: 2000 12:1849-1862
  52. Tuominen H, Puech L, Regan S, Fink S, Olsson O, Sundberg B
    Cambial-region-specific expression of the Agrobacterium iaa genes in transgenic aspen visualized by a linked uidA reporter gene
    Plant Physiology: 2000 123:531-541
  53. Regan S, Bourquin V, Tuominen H, Sundberg B
    Accurate and high resolution in situ hybridization analysis of gene expression in secondary stem tissues
    Plant J: 1999 19:363-369
  54. Nilsson O, Tuominen H, Sundberg B, Olsson O
    The Agrobacterium rhizogenes rolB and rolC promoters are expressed in pericycle cells competent to serve as root initials in transgenic hybrid aspen
    Physiologia Plantarum: 1997 100:456-462
  55. Tuominen H, Puech L, Fink S, Sundberg B
    A Radial Concentration Gradient of Indole- 3- Acetic Acid Is Related to Secondary Xylem Development in Hybrid Aspen
    Plant Physiol: 1997 115:577-585
  56. Tuominen H, Sitbon F, Jacobsson C, Sandberg G, Olsson O, Sundberg B
    Altered Growth and Wood Characteristics in Transgenic Hybrid Aspen Expressing Agrobacterium -Tumefaciens T -DNA Indoleacetic -Acid Biosynthetic Genes
    Plant Physiology: 1995 109:1179-1189
  57. Sundberg B, Tuominen H, Little CHA
    Effects of the Indole- 3- Acetic- Acid (Iaa) Transport Inhibitors N- 1- Naphthylphthalamic Acid and Morphactin on Endogenous Iaa Dynamics in Relation to Compression Wood Formation in 1- Year- Old Pinus- Sylvestris (L) Shoots
    Plant Physiology: 1994 106:469-476
  58. Tuominen H, Ostin A, Sandberg G, Sundberg B
    A Novel Metabolic Pathway for Indole- 3- Acetic- Acid in Apical Shoots of Populus- Tremula (L) X Populus-Tremuloides (Michx)
    Plant Physiology: 1994 106:1511-1520
  59. Rinne P, Tuominen H, Sundberg B
    Growth-Patterns and Endogenous Indole- 3- Acetic- Acid Concentrations in Current- Year Coppice Shoots and Seedlings of 2 Betula Species
    Physiologia Plantarum: 1993 88:403-412
  60. Rinne P, Tuominen H, Junttila O
    Arrested Leaf Abscission in the Nonabscising Variety of Pubescent Birch - Developmental, Morphological and Hormonal Aspects
    Journal of Experimental Botany: 1992 43:975-982