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Bollhöner, Benjamin
Alternative names
Publications (10 of 12) Show all publications
Milhinhos, A., Bollhöner, B., Blazquez, M. A., Novak, O., Miguel, C. M. & Tuominen, H. (2020). ACAULIS5 Is Required for Cytokinin Accumulation and Function During Secondary Growth of Populus Trees. Frontiers in Plant Science, 11, Article ID 601858.
Open this publication in new window or tab >>ACAULIS5 Is Required for Cytokinin Accumulation and Function During Secondary Growth of Populus Trees
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2020 (English)In: Frontiers in Plant Science, E-ISSN 1664-462X, Vol. 11, article id 601858Article in journal (Refereed) Published
Abstract [en]

In the primary root and young hypocotyl of Arabidopsis, ACAULIS5 promotes translation of SUPPRESSOR OF ACAULIS51 (SAC51) and thereby inhibits cytokinin biosynthesis and vascular cell division. In this study, the relationships between ACAULIS5, SAC51 and cytokinin biosynthesis were investigated during secondary growth of Populus stems. Overexpression of ACAULIS5 from the constitutive 35S promoter in hybrid aspen (Populus tremula x Populus tremuloides) trees suppressed the expression level of ACAULIS5, which resulted in low levels of the physiologically active cytokinin bases as well as their direct riboside precursors in the transgenic lines. Low ACAULIS5 expression and low cytokinin levels of the transgenic trees coincided with low cambial activity of the stem. ACAULIS5 therefore, contrary to its function in young seedlings in Arabidopsis, stimulates cytokinin accumulation and cambial activity during secondary growth of the stem. This function is not derived from maturing secondary xylem tissues as transgenic suppression of ACAULIS5 levels in these tissues did not influence secondary growth. Interestingly, evidence was obtained for increased activity of the anticlinal division of the cambial initials under conditions of low ACAULIS5 expression and low cytokinin accumulation. We propose that ACAULIS5 integrates auxin and cytokinin signaling to promote extensive secondary growth of tree stems.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2020
Keywords
ACAULIS5, cytokinin, POPACAULIS5, polyamine, Populus tremula × Populus tremuloides, thermospermine, wood development, xylem
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-177731 (URN)10.3389/fpls.2020.601858 (DOI)000593932900001 ()33304375 (PubMedID)2-s2.0-85096938631 (Scopus ID)
Available from: 2020-12-17 Created: 2020-12-17 Last updated: 2024-01-17Bibliographically approved
Escamez, S., André, D., Sztojka, B., Bollhöner, B., Hall, H., Berthet, B., . . . Tuominen, H. (2020). Cell Death in Cells Overlying Lateral Root Primordia Facilitates Organ Growth in Arabidopsis. Current Biology, 30(3), 455-464
Open this publication in new window or tab >>Cell Death in Cells Overlying Lateral Root Primordia Facilitates Organ Growth in Arabidopsis
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2020 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 30, no 3, p. 455-464Article in journal (Refereed) Published
Abstract [en]

Plant organ growth is widely accepted to be determined by cell division and cell expansion, but, unlike that in animals, the contribution of cell elimination has rarely been recognized. We investigated this paradigm during Arabidopsis lateral root formation, when the lateral root primordia (LRP) must traverse three overlying cell layers within the parent root. A subset of LRP-overlying cells displayed the induction of marker genes for cell types undergoing developmental cell death, and their cell death was detected by electron, confocal, and light sheet microscopy techniques. LRP growth was delayed in cell-deathdeficient mutants lacking the positive cell death regulator ORESARA1/ANAC092 (ORE1). LRP growth was restored in ore1-2 knockout plants by genetically inducing cell elimination in cells overlying the LRP or by physically killing LRP-overlying cells by ablation with optical tweezers. Our results support that, in addition to previously discovered mechanisms, cell elimination contributes to regulating lateral root emergence.

Place, publisher, year, edition, pages
Elsevier, 2020
National Category
Developmental Biology Other Physics Topics
Identifiers
urn:nbn:se:umu:diva-168335 (URN)10.1016/j.cub.2019.11.078 (DOI)000511287900024 ()31956028 (PubMedID)2-s2.0-85078465553 (Scopus ID)
Projects
Bio4Energy
Funder
Bio4Energy
Available from: 2020-02-24 Created: 2020-02-24 Last updated: 2023-03-24Bibliographically approved
Bollhöner, B., Jokipii-Lukkari, S., Bygdell, J., Stael, S., Adriasola, M., Muñiz, L., . . . Tuominen, H. (2018). The function of two type II metacaspases in woody tissues of Populus trees. New Phytologist, 217(4), 1551-1565
Open this publication in new window or tab >>The function of two type II metacaspases in woody tissues of Populus trees
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2018 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 217, no 4, p. 1551-1565Article in journal (Refereed) Published
Abstract [en]

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

Place, publisher, year, edition, pages
Wiley-Blackwell, 2018
Keywords
aspartic protease, cellular autolysis, cysteine protease, metacaspase, Populus, programmed cell ath, wood formation, xylem differentiation
National Category
Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-145132 (URN)10.1111/nph.14945 (DOI)000424284400017 ()29243818 (PubMedID)2-s2.0-85037999750 (Scopus ID)
Projects
Bio4Energy
Funder
Bio4Energy
Available from: 2018-03-05 Created: 2018-03-05 Last updated: 2023-03-24Bibliographically approved
Escamez, S., Bollhöner, B. & Tuominen, H. (2017). Quick histochemical staining methods to detect cell death in xylem elements of plant tissues (1ed.). In: Miguel de Lucas; J. Peter Etchhells (Ed.), Xylem: methods and protocols (pp. 27-36). New York: Humana Press
Open this publication in new window or tab >>Quick histochemical staining methods to detect cell death in xylem elements of plant tissues
2017 (English)In: Xylem: methods and protocols / [ed] Miguel de Lucas; J. Peter Etchhells, New York: Humana Press, 2017, 1, , p. 10p. 27-36Chapter in book (Refereed)
Abstract [en]

Histochemical assays of xylem cell death cannot take advantage of the conventional methods for detection of cell death, such as staining with propidium iodide or trypan/Evans blue or the TUNEL staining. This chapter presents two alternative histochemical methods that can be used to detect xylem cell death quickly and reliably using light microscopy. The first method is a viability stain that can be used to detect cell death of different types of xylem elements in basically any plant species. The second method reveals cell death in xylem vessel elements based on their functionality in transport of water and small water-soluble stains.

Place, publisher, year, edition, pages
New York: Humana Press, 2017. p. 10 Edition: 1
Series
Methods in Molecular Biology, ISSN 1064-3745, E-ISSN 1940-6029 ; 1544
Keywords
Arabidopsis, Libriform fiber, Nitroblue tetrazolium, Populus, Programmed cell death, Sulforhodamine, Tracheary element, Viability stain, Wood, Xylem
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-208657 (URN)10.1007/978-1-4939-6722-3_3 (DOI)28050826 (PubMedID)2-s2.0-85008932636 (Scopus ID)9781493967209 (ISBN)9781493967223 (ISBN)
Available from: 2023-06-09 Created: 2023-06-09 Last updated: 2023-06-27Bibliographically approved
Escamez, S., André, D., Zhang, B., Bollhöner, B., Pesquet, E. & Tuominen, H. (2016). METACASPASE9 modulates autophagy to confine cell death tothe target cells during Arabidopsis vascular xylem differentiation. Biology Open, 5(2), 122-129
Open this publication in new window or tab >>METACASPASE9 modulates autophagy to confine cell death tothe target cells during Arabidopsis vascular xylem differentiation
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2016 (English)In: Biology Open, ISSN 2046-6390, Vol. 5, no 2, p. 122-129Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
The Company of Biologists ltd, 2016
Keywords
Arabidopsis thaliana, Autophagy, Intercellular signalling, Metacaspase, Programmed cell death, Tracheary element
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-115784 (URN)10.1242/bio.015529 (DOI)000370240300005 ()26740571 (PubMedID)2-s2.0-84976594179 (Scopus ID)
Projects
Bio4Energy
Funder
Bio4Energy
Available from: 2016-02-04 Created: 2016-02-04 Last updated: 2023-03-23Bibliographically approved
Wrzaczek, M., Vainonen, J. P., Stael, S., Tsiatsiani, L., Help-Rinta-Rahko, H., Gauthier, A., . . . Kangasjarvi, J. (2015). GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis. EMBO Journal, 31(1), 55-66
Open this publication in new window or tab >>GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis
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2015 (English)In: EMBO Journal, ISSN 0261-4189, E-ISSN 1460-2075, Vol. 31, no 1, p. 55-66Article in journal (Refereed) Published
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.

Keywords
ligand, protease, receptor-like kinase, secreted protein
National Category
Genetics Botany
Identifiers
urn:nbn:se:umu:diva-99353 (URN)10.15252/embj.201488582 (DOI)000347167900005 ()2-s2.0-84920398025 (Scopus ID)
Available from: 2015-03-09 Created: 2015-02-07 Last updated: 2023-03-23Bibliographically approved
Bollhöner, B., Zhang, B., Stael, S., Denancé, N., Overmyer, K., Goffner, D., . . . Tuominen, H. (2013). Post mortem function of AtMC9 in xylem vessel elements. New Phytologist, 200(2), 498-510
Open this publication in new window or tab >>Post mortem function of AtMC9 in xylem vessel elements
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2013 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 200, no 2, p. 498-510Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
John Wiley & Sons, 2013
Keywords
Arabidopsis thaliana, autolysis, metacaspase, protease, vessel element, xylem cell death
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-81218 (URN)10.1111/nph.12387 (DOI)000324621600021 ()23834670 (PubMedID)2-s2.0-84884416703 (Scopus ID)
Available from: 2013-10-04 Created: 2013-10-04 Last updated: 2023-03-24Bibliographically approved
Bollhöner, B. (2013). Significance of hydrolytic enzymes expressed during xylem cell death. (Doctoral dissertation). Umeå: Umeå universitet
Open this publication in new window or tab >>Significance of hydrolytic enzymes expressed during xylem cell death
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
Betydelsen av hydrolytiska enzymer uttryckta under xylemcelldöd
Abstract [en]

Xylem is an inherent feature of all vascular plants and functions in water transport and mechanical support. In order to efficiently transport water, xylem cells are reinforced by secondary walls before they undergo programmed cell death and their cell contents are removed by autolysis to create a hollow tube. During their differentiation, xylem cells express various hydrolytic enzymes, such as proteases, nucleases and lipases, but only in a few examples has their role in xylem cell death been characterized. This thesis focuses on the regulatory aspects of xylem cell death and the autolytic cell clearance in vessel elements and fibers of hybrid aspen (Populus tremula L. x tremuloides Michx.) and in vessel elements of Arabidopsis thaliana. Using comparative transcriptomic analysis, candidate genes for fiber-specific cell death processes were identified. Further, a hypothesis is presented on the regulation of thermospermine levels in the vasculature by a negative feedback-loop involving auxin and the class III Homeodomain-Leucine Zipper (HD-ZIP III) transcription factor HOMEOBOX8 (PtHB8). The role of the Arabidopsis METACASPASE9 (AtMC9) in xylem cell death was characterized using molecular tools, such as reporter lines and fluorescent fusion proteins, and electron microscopy (TEM). This showed that cell death initiation is not controlled by AtMC9. Instead, evidence is presented for the involvement of AtMC9 in the post mortem autolysis of vessel elements that follows tonoplast rupture and leads to the formation of the hollow conduit. Cell death-associated genes were further observed to be expressed during the emergence of lateral roots in Arabidopsis thaliana. This led to the discovery that cells overlying a lateral root primordium undergo cell death, which was demonstrated by detection of DNA degradation and TEM analysis. It is concluded that cell death facilitates emergence of lateral roots through the overlying tissues in a concerted manner with cell wall remodelling. Together, these findings show that although individual hydrolytic enzymes may be dispensable for plant growth and development, their common regulators are the tool for understanding their function and importance.

Abstract [sv]

Xylem är en karakteristisk vävnad i alla kärlväxter som leder vatten och mineraler samt har mekanisk stödfunktion. För att effektivt kunna transportera vatten förstärks xylemceller med sekundära cellväggar innan de dör genom programmerad celldöd. Deras cellinnehåll bryts ner genom autolys för att skapa ett ihåligt rör. Xylemceller uttrycker under sin differentiering olika hydrolytiska enzymer, såsom proteaser, lipaser och nukleaser, men bara för ett fåtal av dessa har funktionen under xylemcelldöd kartlagts. Denna avhandling fokuserar på reglering av xylemcelldöden och den autolytiska nedbrytningen av cellen, i såväl kärlelement och fibrer av hybridasp (Populus tremula L. x tremuloides Michx.) som i kärlelement av backtrav (Arabidopsis thaliana). Med hjälp av jämförande transkriptomanalys identifierades kandidatgener för fiber-specifika celldödsprocesser i hybridasp. Vidare utvecklades en hypotes om reglering av termosperminnivåer i vaskulaturen genom en negativ feedback-loop, som omfattar auxin reglering och klass III homeodomän-leucinzipper (HD-ZIP III) transkriptionsfaktorn HOMEOBOX8 (PtHB8). Funktionen av Arabidopsis METACASPASE9 (AtMC9) under xylemcelldöd karakteriserades med molekylära verktyg, såsom reporterlinjer och fluorescerande fusionsproteiner och elektronmikroskopi (TEM). Dessa analyser visade att celldödens initiering inte styrs av AtMC9. Istället presenteras bevis för en roll av AtMC9 i autolysen av kärlelement som sker post mortem efter att vakuolen har gått sönder och som slutför bildandet av det tomma kärlet. Genuttryck som associeras med celldöd observerades också under utvecklingen av laterala rötter i Arabidopsis thaliana. Detta ledde till upptäckten att celler som ligger ovanför ett lateralrotprimordium dör en programmerad celldöd och visar tecken på DNA-nedbrytning och autolys i TEM-analyser. Slutsatsen av denna studie är att celldöd i samspel med cellväggsmodifiering underlättar utväxten av laterala rötter genom de överliggande cellagren. Sammantaget tyder dessa upptäckter på att även om enstaka hydrolyserande enzymer inte är nödvändiga för växternas tillväxt och utveckling, så kan deras gemensamma reglering nyttjas för att förstå deras funktion och betydelse.

Place, publisher, year, edition, pages
Umeå: Umeå universitet, 2013. p. 49
Keywords
Arabidopsis, Populus, xylem cell death, metacaspase, fiber, lateral root emergence
National Category
Botany
Research subject
Molecular Biology; Physiological Botany; molecular cell biology
Identifiers
urn:nbn:se:umu:diva-81340 (URN)978-91-7459-739-4 (ISBN)
Public defence
2013-11-08, Hörsal F, Humanisthuset, Umeå universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2013-10-16 Created: 2013-10-07 Last updated: 2018-06-08Bibliographically approved
Milhinhos, A., Prestele, J., Bollhöner, B., Matos, A., Vera-Sirera, F., Rambla, J. L., . . . Miguel, C. M. (2013). Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem. The Plant Journal, 75(4), 685-698
Open this publication in new window or tab >>Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem
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2013 (English)In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 75, no 4, p. 685-698Article in journal (Refereed) Published
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.

Keywords
POPACAULIS5, ACAULIS5 (ACL5), class III homeodomain leucine zipper transcription factors (HD-ZipIII), wood development, polyamine, Populus tremulax, Populus tremuloides, Populus trichocarpa
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-80064 (URN)10.1111/tpj.12231 (DOI)000322898800013 ()2-s2.0-84882455661 (Scopus ID)
Available from: 2013-09-11 Created: 2013-09-09 Last updated: 2023-03-24Bibliographically approved
Bollhoner, B., Prestele, J. & Tuominen, H. (2012). Xylem cell death: emerging understanding of regulation and function. Journal of Experimental Botany, 63(3), 1081-1094
Open this publication in new window or tab >>Xylem cell death: emerging understanding of regulation and function
2012 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 63, no 3, p. 1081-1094Article, review/survey (Refereed) Published
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.

Place, publisher, year, edition, pages
Oxford University Press, 2012
Keywords
Autolysis, ethylene, fibre, metacaspase, protease, thermospermine, tracheary element, VND
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-53114 (URN)10.1093/jxb/err438 (DOI)000300238400003 ()2-s2.0-84856926093 (Scopus ID)
Available from: 2012-03-14 Created: 2012-03-13 Last updated: 2023-03-24Bibliographically approved
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