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The significance of ethylene and ETHYLENE RESPONSE FACTORS in wood formation of hybrid aspen
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). (Hannele Tuominen)ORCID iD: 0000-0003-0717-1630
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The woody tissues serve to stabilise plants, store nutrients and translocate water and minerals. The formation of wood, or ’secondary xylem’, follows a well-defined developmental gradient which is initiated by cell division activity in the vascular cambium. The ’xylem cambial derivatives’ then expand before deposition of the secondary cell wall (SCW), which is where most of the biomass of wood originates. After this, some cells of the xylem typically undergo programmed cell death (PCD). Cellulose and lignin are chemical components of the SCW that provide structural support and water impermeability, respectively. The chemical composition of the SCWs is also important economically since it affects the efficiency of wood processing during pulping and enzymatic hydrolysis. Two dominant xylem cell types of angiosperm tree species like Populus are the fibers and the vessel elements. Fibers are important for the mechanical strength of the wood and provide the majority of the wood biomass. Vessel elements join endwise to form hollow tubes, or vessels, for the purposes of water and solute transport in the stem.

 

Formation of wood is a complex process, subject to multiple levels of regulation. Plant hormones are important for wood formation, and ethylene signalling has been shown to stimulate cambial activity, affect the ratio between fibers and vessel elements, as well as the expansion of the cambial derivatives. Ethylene is also involved in the ‘tension wood’ response of stems that are displaced from their original vertical position. Formation of ’tension wood’ generates a force that lifts the stem back to the upright growing position. What remains unknown is the molecular link between ethylene signalling and wood formation. The work in this thesis focuses on providing this link using the model tree species hybrid aspen (Populus tremula x tremuloides).

 

Using a state-of-the-art transcriptomic database that spans all phases of xylem differentiation in hybrid aspen wood, from cell division through xylem cell expansion to xylem maturation (SCW deposition and PCD), the expression of the ethylene pathway related genes was investigated during normal wood formation. The analyses reveal ethylene perception and transcriptional reprogramming is possible across all zones of wood formation. Previously uncharacterised components were identified that may be important contributors to wood formation. Furthermore, although ethylene is known to affect the ratio between the abundance of the vessel elements and the fibers, genetic evidence is lacking. Using the tension wood response and transgenic trees modified in ethylene signalling, it was shown that ethylene is a negative regulator of vessel formation and important for a functional tension wood response. Furthermore, characterisation of two transcription factors (TFs), belonging to the ethylene response factor (ERF) gene family, suggests that aspects of xylem cell division, expansion and subsequent SCW formation, including lignification, can be affected by ERF85 and ERF139 in an ethylene-dependent manner. Phase transitions during wood formation need to be controlled spatiotemporally, and transcriptional regulation by these ERFs seems to be part of such control to establish correct transitions between cell expansion, secondary cell wall formation and lignification. The work presented here also identifies promising additions to the toolkit available for forest tree biotechnology and molecular breeding programmes.

Abstract [sv]

Växternas ledningsvävnad består till stora delar av vedartad vävnad som bidrar till att stabilisera plantan, lagra näringsämnen och transportera vatten och mineraler. Bildandet av veden, eller "det sekundära xylemet", är en väldefinierad process som börjar med celldelningsaktiviteten i det vaskulära kambiet.  Celler som bildas i kambiet differentierar genom att först expandera och sedan bilda en tjock sekundär cellvägg (SCV) som ger upphov till största delen av biomassa i veden. Efter detta, vissa celler i xylemet dör genom ett genetiskt styrt celldödsprogram.  SCV innehåller kemiska komponenter, så som cellulosa och lignin, som är viktiga för funktionen av hela plantan. Cellulosa utformar skelettet i SCV och lignin ger en hydrofobisk yta som behövs för vattentransport. Sammansättningen och mängden av SCV komponenter är viktiga också för industriella tillämpningar. Cellulosa är värdeful som råvara för produktion av pappersmassa och olika bioprodukter medans lignin oftast är en störande komponent som måste avlägsnas i dessa processer. De vanligaste xylem celltyper i trädslag som poplar och aspar är ’kärlelement’ och ’fibrer’. Fibrer ger mekanisk hållfasthet och största delen av vedbiomassan. Kärlelement bildar ihåliga rör, eller ’kärl’, som transporterar vatten och mineraler i stammen.

Vedbildning är en komplicerad process  some regleras av olika faktorer så som växthormoner. En är de viktigaste växthormoner i vedbildning är etylen. Den har visats stimulera kambieaktiviteten, påverka förhållandet mellan fibrer och kärlelement, och expansion av xylemceller. Etylen är också involverad i bildandet av såkallad ”dragved” som sker när trädstammen flyttas från sitt ursprungliga vertikala läge p.g.a. till exempel vind. Bildandet av dragved genererar en kraft som lyfter stammen tillbaka till den upprätt växande ställningen. Det som fortfarande är okänt är den molekylära kopplingen mellan etylensignalering och vedbildning. Arbetet i denna avhandling har haft en målsättning att avslöja åtminstone delar av denna koppling i hybrid asp (Populus tremula x tremuloides).

En databas över genutryck användes för att visa att etylensignalering pågår i flera olika faser av xylemutveckling. Det är därför troligt att etylen kan också reglera flera olika processer som sker under differentiering av xylemceller.  Flera nya komponenter kunde också identifieras som verkar delta i reglering av vedbildning. Farmakologiska experiment och genetisk modifiering av etylensignalering avslöjade att etylen reglerar negativt bildning av nya kärlelement i veden. Ökat antal kärlelement i etylenokänsliga, genetiskt modifierade hybrid asp träd korrelerade negativt med  trädens kapacitet att nå upprätt växande ställning efter att de hade placerats i en vågrätt ställning, vilket tyder på att andelen kärlelement är central för funktionen av dragved.  Vidare studerades två transkriptionsfaktorer som hör till ETYLEN RESPONS FAKTOR (ERF) genfamilj. ERF85 och ERF139 är både uttryckta i xylemet, och deras genuttryck kräver funktionell etylen signalering. Globala genuttrycksstudier i hybrid asp träd som var genetiskt modifierade antingen för ERF85 eller ERF139 avslöjade att de har olika molekylära mekanismer men att de båda verkade influera övergången mellan olika faser av xylem differentiering. Detta bekräftades också genom analys av xylem differentiering och vedkemi i de genetiskt modifierade träden. Det samlade data från arbeten som presenteras i denna avhandling identifierar också lovande tillägg till den verktygslåda som finns för biotekniska initiativ och molekylär avel i skogsträd.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2018. , p. 80
Keywords [en]
ethylene, wood formation, hybrid aspen, Populus, ETHYLENE RESPONSE FACTOR, ERF85, ERF139, cambium, lignin, xylem expansion, secondary cell wall, tension wood, cambial derivative cell fate, vessel element, time-lapse photography
National Category
Biochemistry and Molecular Biology Botany Cell Biology
Research subject
molecular biotechnology (dept of biochem); Genetics; Physiological Botany
Identifiers
URN: urn:nbn:se:umu:diva-151724ISBN: 978-91-7601-935-1 (print)OAI: oai:DiVA.org:umu-151724DiVA, id: diva2:1247192
Public defence
2018-10-05, KB.E3.01, KBC-Huset, Umeå, 09:00 (English)
Opponent
Supervisors
Available from: 2018-09-14 Created: 2018-09-11 Last updated: 2018-10-09Bibliographically approved
List of papers
1. Ethylene-Related Gene Expression Networks in Wood Formation
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2018 (English)In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 9, article id 272Article in journal (Refereed) Published
Abstract [en]

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

Place, publisher, year, edition, pages
Frontiers Media S.A., 2018
Keywords
ethylene signaling, secondary growth, wood development, co-expression network, EIN3, ERF
National Category
Bioinformatics and Systems Biology
Identifiers
urn:nbn:se:umu:diva-146209 (URN)10.3389/fpls.2018.00272 (DOI)000427359000001 ()29593753 (PubMedID)
Projects
Bio4Energy
Available from: 2018-05-14 Created: 2018-05-14 Last updated: 2019-09-06Bibliographically approved
2. Ethylene suppresses vessel element formation during the tension wood response of hybrid aspen
Open this publication in new window or tab >>Ethylene suppresses vessel element formation during the tension wood response of hybrid aspen
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-151827 (URN)
Available from: 2018-09-13 Created: 2018-09-13 Last updated: 2018-09-13
3. Populus ERF85 mediates the transition between xylem cell expansion and secondary cell wall formation in hybrid aspen
Open this publication in new window or tab >>Populus ERF85 mediates the transition between xylem cell expansion and secondary cell wall formation in hybrid aspen
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-151829 (URN)
Available from: 2018-09-13 Created: 2018-09-13 Last updated: 2018-09-13
4. An AP/ERF transcription factor ERF139 affects growth and lignin deposition in hybrid aspen
Open this publication in new window or tab >>An AP/ERF transcription factor ERF139 affects growth and lignin deposition in hybrid aspen
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-151831 (URN)
Available from: 2018-09-13 Created: 2018-09-13 Last updated: 2018-09-13

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