scholarly journals Populus ERF85 balances xylem cell expansion and secondary cell wall formation in hybrid aspen

2021 ◽  
Author(s):  
Carolin Seyfferth ◽  
Bernard A Wessels ◽  
Jorma Vahala ◽  
Jaakko Kangasjarvi ◽  
Nicolas Delhomme ◽  
...  

Secondary growth relies on precise and specialized transcriptional networks that determine cell division, differentiation, and maturation of xylem cells. We identify a novel role for the ethylene induced Populus ETHYLENE RESPONSE FACTOR ERF85 (Potri.015G023200) in balancing xylem cell expansion and secondary cell wall (SCW) formation in hybrid aspen (Populus tremula x tremuloides). Expression of ERF85 is high in phloem and cambium cells and during expansion of xylem cells, while it is low in maturing xylem tissue. Extending ERF85 expression into SCW forming zones of woody tissues through ectopic expression reduced wood density and SCW thickness of xylem fibers but increased fiber diameter. Xylem transcriptomes from the transgenic trees revealed transcriptional induction of genes involved in cell expansion, translation and growth. Expression of genes associated with plant vascular development and biosynthesis of SCW chemical components such as xylan and lignin, was downregulated in the transgenic trees. Our results suggest that ERF85 activates genes related with xylem cell expansion, while preventing transcriptional activation of genes related to SCW formation. The importance of precise spatial expression of ERF85 during wood development together with the observed phenotypes in response to ectopic ERF85 expression suggests that ERF85 functions as a switch between different phases of xylem differentiation during wood formation.

Cells ◽  
2021 ◽  
Vol 10 (8) ◽  
pp. 1971
Author(s):  
Carolin Seyfferth ◽  
Bernard A. Wessels ◽  
Jorma Vahala ◽  
Jaakko Kangasjärvi ◽  
Nicolas Delhomme ◽  
...  

Secondary growth relies on precise and specialized transcriptional networks that determine cell division, differentiation, and maturation of xylem cells. We identified a novel role for the ethylene-induced Populus ethylene response factor PtERF85 (Potri.015G023200) in balancing xylem cell expansion and secondary cell wall (SCW) formation in hybrid aspen (Populus tremula x tremuloides). Expression of PtERF85 is high in phloem and cambium cells and during the expansion of xylem cells, while it is low in maturing xylem tissue. Extending PtERF85 expression into SCW forming zones of woody tissues through ectopic expression reduced wood density and SCW thickness of xylem fibers but increased fiber diameter. Xylem transcriptomes from the transgenic trees revealed transcriptional induction of genes involved in cell expansion, translation, and growth. The expression of genes associated with plant vascular development and the biosynthesis of SCW chemical components such as xylan and lignin, was down-regulated in the transgenic trees. Our results suggest that PtERF85 activates genes related to xylem cell expansion, while preventing transcriptional activation of genes related to SCW formation. The importance of precise spatial expression of PtERF85 during wood development together with the observed phenotypes in response to ectopic PtERF85 expression suggests that PtERF85 contributes to the transition of fiber cells from elongation to secondary cell wall deposition.


2019 ◽  
Vol 224 (4) ◽  
pp. 1585-1599 ◽  
Author(s):  
Bernard Wessels ◽  
Carolin Seyfferth ◽  
Sacha Escamez ◽  
Thomas Vain ◽  
Kamil Antos ◽  
...  

2005 ◽  
Vol 137 (3) ◽  
pp. 983-997 ◽  
Author(s):  
Henrik Aspeborg ◽  
Jarmo Schrader ◽  
Pedro M. Coutinho ◽  
Mark Stam ◽  
Åsa Kallas ◽  
...  

Genes ◽  
2019 ◽  
Vol 11 (1) ◽  
pp. 20
Author(s):  
Fernando Manuel Matias Hurtado ◽  
Maísa de Siqueira Pinto ◽  
Perla Novais de Oliveira ◽  
Diego Mauricio Riaño-Pachón ◽  
Laura Beatriz Inocente ◽  
...  

NAC proteins are one of the largest families of plant-specific transcription factors (TFs). They regulate diverse complex biological processes, including secondary xylem differentiation and wood formation. Recent genomic and transcriptomic studies of Tectona grandis L.f. (teak), one of the most valuable hardwood trees in the world, have allowed identification and analysis of developmental genes. In the present work, T. grandis NAC genes were identified and analyzed regarding to their evolution and expression profile during wood formation. We analyzed the recently published T. grandis genome, and identified 130 NAC proteins that are coded by 107 gene loci. These proteins were classified into 23 clades of the NAC family, together with Populus, Eucalyptus, and Arabidopsis. Data on transcript expression revealed specific temporal and spatial expression patterns for the majority of teak NAC genes. RT-PCR indicated expression of VND genes (Tg11g04450-VND2 and Tg15g08390-VND4) related to secondary cell wall formation in xylem vessels of 16-year-old juvenile trees. Our findings open a way to further understanding of NAC transcription factor genes in T. grandis wood biosynthesis, while they are potentially useful for future studies aiming to improve biomass and wood quality using biotechnological approaches.


2019 ◽  
Author(s):  
Sunita Kushwah ◽  
Alicja Banasiak ◽  
Nobuyuki Nishikubo ◽  
Marta Derba-Maceluch ◽  
Mateusz Majda ◽  
...  

ABSTRACTIn dicotyledons, xyloglucan is the major hemicellulose of primary walls affecting the load-bearing framework with participation of XTH enzymes. We used loss- and gain-of function approaches to study functions of abundant cambial region expressed XTH4 and XTH9 in secondary growth. In secondarily thickened hypocotyls, these enzymes had positive effects on vessel element expansion and fiber intrusive growth. In addition, they stimulated secondary wall thickening, but reduced secondary xylem production. Cell wall analyses of inflorescence stems revealed changes in lignin, cellulose, and matrix sugar composition, indicating overall increase in secondary versus primary walls in the mutants, indicative of higher xylem production compared to wild type (since secondary walls were thinner). Intriguingly, the number of secondary cell wall layers was increased in xth9 and reduced in xth4, whereas the double mutant xth4x9 displayed intermediate number of layers. These changes correlated with certain Raman signals from the walls, indicating changes in lignin and cellulose. Secondary walls were affected also in the interfascicular fibers where neither XTH4 nor XTH9 were expressed, indicating that these effects were indirect. Transcripts involved in secondary wall biosynthesis and in cell wall integrity sensing, including THE1 and WAK2, were highly induced in the mutants, indicating that deficiency in XTH4 and XTH9 triggers cell wall integrity signaling, which, we propose, stimulates the xylem cell production and modulates secondary wall thickening. Prominent effects of XTH4 and XTH9 on secondary xylem support the hypothesis that altered xyloglucan can affect wood properties both directly and via cell wall integrity sensing.SIGNIFICANCE STATEMENTXyloglucan is a ubiquitous component of primary cell walls in all land plants but has not been so far reported in secondary walls. It is metabolized in muro by cell wall-residing enzymes - xyloglucan endotransglycosylases/hydrolases (XTHs), which are reportedly abundant in vascular tissues, but their role in these tissues is unclear. Here we report that two vascular expressed enzymes in Arabidopsis, XTH4 and XTH9 contribute to the secondary xylem cell radial expansion and intrusive elongation in secondary vascular tissues.Unexpectedly, deficiency in their activities highly affect chemistry and ultrastructure of secondary cell walls by non-cell autonomous mechanisms, including transcriptional induction of secondary wall-related biosynthetic genes and cell wall integrity sensors. These results link xyloglucan metabolism with cell wall integrity pathways, shedding new light on previous reports about prominent effects of xyloglucan metabolism on secondary walls.One sentence summaryXTH4 and XTH9 positively regulate xylem cell expansion and fiber intrusive tip growth, and their deficiency alters secondary wall formation via cell wall integrity sensing mechanisms.


2018 ◽  
Author(s):  
Akiva Shalit-Kaneh ◽  
Tamar Eviatar–Ribak ◽  
Guy Horev ◽  
Naomi Suss ◽  
Roni Aloni ◽  
...  

AbstractThe protein hormone florigen is a universal systemic inducer of flowering and a generic growth terminator across meristems. To understand the developmental rational for its pleiotropic functions and to uncover the deep cellular systems mobilized by florigen beyond flowering we explored termination of radial expansion of stems. Employing the power of tomato genetics along with RNAseq and histological validations we show that endogenous, mobile, or induced florigen accelerates secondary cell wall biogenesis (SCWB), and hence vascular maturation, independently of flowering. This finding is supported by a systemic florigen antagonist from the non-floweringGinkgo biloba, which arrests SCWB and byMADSandMIFgenes downstream of florigen that similarly suppress or enhance, respectively, vascular maturation independent of flowering. We also show that florigen is remarkably stable and distributed to all organs regardless of existing endogenous levels. By accelerating SCWB, florigen reprograms the distribution of resources, signals and mechanical loads required for the ensuing reproductive phase it had originally set into motion.Developmental HighlightsFlorigen accelerates SCWB: A prime case for a long-range regulation of a complete metabolic network by a plant hormone.The dual acceleration of flowering and vascular maturation by Florigen provides a paradigm for a dynamic regulation of global, independent, developmental programs.The growth termination functions of florigen and the auto-regulatory mechanism for its production and distribution provide a communication network enveloping the shoot system.A stable florigen provides a possible mechanism for the quantitative regulation of floweringLateral stimulation of xylem differentiation links the phloem-travelling florigen with the annual rings in trunks.MADS genes are common relay partners in Florigen circuits; vascular maturation in stems and reproductive transition in apical meristems.


2017 ◽  
Author(s):  
Judith Felten ◽  
Jorma Vahala ◽  
Jonathan Love ◽  
András Gorzsás ◽  
Markus Rüggeberg ◽  
...  

SummaryResearch conductedThe phytohormone ethylene impacts secondary stem growth in plants by stimulating cambial activity, xylem development and fiber over vessel formation. Here we report the effect of ethylene on secondary cell wall formation and the molecular connection between ethylene signaling and wood formation.MethodsWe applied exogenous ethylene or its precursor 1-aminocyclopropane-1-carboxylic acid (ACC) to wild type and ethylene insensitive hybrid aspen trees (Populus tremula x tremuloides) and studied secondary cell wall anatomy, chemistry and ultrastructure. We furthermore analyzed the transcriptome (RNA Seq) after ACC application to wild type and ethylene insensitive trees.Key resultsWe demonstrate that ACC and ethylene induce gelatinous-layers (G-layers) and alter the fiber cell wall cellulose microfibril angle. G-layers are tertiary wall layers rich in cellulose, typically found in tension wood of aspen trees. A vast majority of transcripts affected by ACC are downstream of ethylene perception and include a large number of transcription factors (TFs). Motif-analyses reveal potential connections between ethylene TFs (ERFs, EIN3/EIL1) and wood formation.ConclusionG-layer formation upon ethylene application suggests that the increase in ethylene biosynthesis observed during tension wood formation is important for its formation. Ethylene-regulated TFs of the ERF and EIN3/EIL1 type could transmit the ethylene signal.


2020 ◽  
Author(s):  
Emilie Aubry ◽  
Beate Hoffmann ◽  
Françoise Vilaine ◽  
Françoise Gilard ◽  
Patrick A.W. Klemens ◽  
...  

ABSTRACTIn higher plants, the development of the vascular system is controlled by a complex network of transcription factors. However, how nutrient availability in the vascular cells affects their development remains to be addressed. At the cellular level, cytosolic sugar availability is regulated mainly by sugar exchanges at the tonoplast through active and/or facilitated transport. In Arabidopsis thaliana, among the tonoplastic transporters, SWEET16 and SWEET17 have been previously localized in the vascular system. Here, using a reverse genetic approach, we propose that sugar exchanges at the tonoplast, mediated by SWEET16, are important for xylem cell division as revealed in particular by the decreased number of xylem cells in the swt16 mutant and the expression of SWEET16 at the procambium-xylem boundary. In addition, we demonstrate that transport of hexoses mediated by SWEET16 and/or SWEET17 is required to sustain the formation of the xylem secondary cell wall. This result is in line with a defect in the xylem cell wall composition as measured by FTIR in the swt16swt17 double mutant and by upregulation of several genes involved in secondary cell wall synthesis. Our work therefore supports a model in which xylem development is partially dependent on the exchange of hexoses at the tonoplast of xylem-forming cells.


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