Anne Lacey Samuels
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Graduate Student Supervision
Doctoral Student Supervision (Jan 2008 - Nov 2019)
Secondary cell walls (SCWs) containing the hemicellulose xylan are essential for normal plant growth and development. Great strides have been made to identify the many Golgi-localized biosynthetic enzymes that work in concert to make xylan, however, we still understand little about how these critical proteins and their product are organized in the Golgi to facilitate synthesis and trafficking. To address this question, I characterized the Arabidopsis Golgi in cells producing SCWs using a combination of confocal and transmission electron microscopy (TEM). This analysis indicates that the number of Golgi stacks increases significantly with the onset of SCW synthesis, and that during this process the randomly distributed Golgi stacks work together to produce and secrete xylan. Furthermore, nanoscale characterization of Golgi structure revealed significant increases in Golgi diameter, swelling of the cisternal margins, and secretory vesicle size. Loss of the xylan-biosynthetic enzyme IRREGULAR XYLEM 9 (IRX9) resulted in a dramatic increase in cisternal fenestration and a decrease in swollen margins, but did not affect the number or size of Golgi. Finally, immunogold labelling was used to map IRX9-GFP and xylan to different regions of Golgi cisternae, indicating that xylan is abundant in the outer margins of trans-cisternae, IRX9-GFP is abundant in an inner margin of medial-cisternae, and both are absent from cisternal centers. This new concentric circle model of Golgi organization has expanded our understanding of Golgi structure and function and has implications for Golgi function in other cell types and organisms.The second part of this thesis explores problem-solving instruction in undergraduate cell biology classes, by testing how different teaching techniques affect student attitudes and performance. These results demonstrate that worked examples can be effective teaching techniques for cell biology problem-solving, with lower-performing students seeing greater benefits. Furthermore, providing worked examples did not ameliorate student desires for answer keys to practice problems. This work can be used to guide the appropriate level of instructional support for students of different expertise levels in future courses, and across curricula.
The formation of plant secondary cell walls requires a complex network of transcriptional regulation, culminating in a coordinated suite of biosynthetic genes depositing walls, in a spatial and temporal fashion. The transcription factor KNOTTED ARABIDOPSIS THALIANA7 (KNAT7) is a Class II KNOTTED1-like homeobox (KNOX2) gene, that acts as a negative regulator of secondary cell wall biosynthesis in interfascicular fibers. Previously, members of Ovate Family Proteins (OFP1 and OFP4), were shown to interact with KNAT7 to negatively regulate wall formation. However, the function of other closely related KNOX2 and OFP genes in secondary wall formation remains unclear. Herein, I showed that knat3knat7 double mutants possess an enhanced irregular xylem (irx) phenotype relative to single mutants, and decreased interfascicular fiber cell wall thickness. Additionally, unlike the increased lignin content characteristic of knat7 mutants, knat3knat7 had no change in lignin content, while the monomeric lignin composition was substantially reduced relative to the wild-type plants. In contrast, KNAT3 overexpression resulted in thicker interfascicular fiber secondary walls, suggesting a positive regulation of KNAT3 in wall development.A thorough examination of OFP mutants showed that none of the single mutants revealed any wall defects, including ofp4, which was previously shown to interact with KNAT7. However, they do display leaf phenotypes. In contrast, plants overexpressing OFP isoforms consistently exhibited cell swelling, disordered microtubules, and dark-grown de-etiolated phenotypes, resembling phenotypes common to brassinosteroid deficient mutants. Using yeast two-hybrid and bimolecular fluorescence complementation assays, I identified two genes that interacted with OFP4, NAP1;1 and NAP1;2, members of the Nucleosome Assembly Protein 1 (NAP1) family. Higher-order, loss-of-function NAP1 and OFP mutants also exhibit altered cotyledon shape and a reduced cotyledon width:length ratio. The kidney-shaped cotyledon phenotype apparent in OFP4 overexpressing plants was suppressed in the nap1;1 nap1;2 nap1;3 triple mutant background. Together, my research suggests that in addition to KNAT7, KNAT3 also contributes to cell wall deposition, and that a complex network of positive and negative regulation governed by KNOX2 proteins regulates secondary wall formation. Moreover, the complex of OFP4 and NAP1 plays a significant role in the cotyledon development.
The full abstract for this thesis is available in the body of the thesis, and will be available when the embargo expires.
Cellulose is the most abundant polymer in nature and is a major component of both primary and secondary cell walls in plants. The cellulose produced in these different walls are synthesized by completely independent sets of non-redundant CELLULOSE SYNTHASE (CESA) enzymes. In the last decade, live cell imaging techniques have answered a number of fundamental questions regarding CESA dynamics and organization in the primary cell wall. However, attempts to repeat these experiments in cells producing secondary cell walls has been met with limited success due to the fact that cells forming secondary walls are deep inside plant organs. The development of an inducible system driving the ectopic expression of the master regulator for protoxylem tracheary element development, VASCULAR RELATED NAC-DOMAIN7 (VND7), has generated a valuable biological tool to track secondary cell wall synthesis via live-cell imaging. With these tools, I was able to directly visualize secondary cell wall-specific CESA complexes moving around the plasma membrane, and to quantify that they move at a significantly faster rate than primary cell wall-specific complexes. Additionally, bundling of the underlying cortical microtubules causes the densities of the CESA complexes to be much higher during secondary wall synthesis than during primary wall synthesis, giving a possible explanation for the rapid and abundant development of these walls. Analysis of the transition from primary to secondary cell wall production revealed that primary wall-specific CESAs are selectively targeted into distinct pre-vacuolar compartments for degradation to the lytic vacuole, while secondary cell wall-specific CESAs accumulate. Finally, cesa mutants were investigated to explore the effects of the loss of each of the three CESAs involved in secondary cell wall cellulose synthesis on both the wall patterning and localization of their interacting partners. While the loss of a CESA causes significant defects in secondary cell wall cellulose patterning, the loss of CESA7 specifically resulted in the complete loss in patterning, indicating a possible role for CESA7 in anchoring the CESA complexes to the underlying cortical microtubules. Taken together, these results refine our model of how plant cells coordinate their cellulose synthesis machinery during secondary cell wall production.
Cellulose biosynthesis is a dynamic and specialized cellular process with multiple layers of organization. This abundant, vital polymer is synthesized by cellulose synthase complexes (CSCs) localized at the plasma membrane. Cellulose chains are extruded into the apoplast, and rapidly self-assemble into microfibrils. The mechanisms controlling organization of the product, cellulose microfibrils, are still unclear. The GPI-anchored protein COBRA (COB), localized at the outer leaflet of the plasma membrane, is required for normal cellulose deposition in primary cell walls. A closely related protein, COBRA-LIKE4 (COBL4), is required for secondary cell cellulose organization. Loss-of-function, in Arabidopsis cobl4 mutants originally called irregular xylem 6 (irx6), results in reduced cellulose content, cellulose of lower crystallinity, and thinner secondary cell walls. To better understand COBL4 function, I investigated the chemical and ultrastructural properties of novel irx6-2 and irx6-3 alleles of Arabidopsis. I followed this up by demonstrating functional conservation between COBL4 in woody (Populus trichocarpa) and herbaceous (Arabidopsis) species. A fluorescently labelled poplar COBL4, PtCOB4a, was co-localized with secondary cell wall thickenings in an inducible Arabidopsis protoxylem experimental system. To further refine our understanding the molecular role of COBL4, AtCOBL4 was over-expressed in hybrid poplar, in a secondary cell wall specific manner. Increased AtCOBL4 abundance did not significantly alter cell wall derived glucose content compared to control plants; this was confirmed by the absence of a significant increase in α-cellulose. The ultra-structural characteristics of deposited cellulose, specifically cellulose DP and cellulose crystallinity, were significantly increased in a number of over expression lines relative to control trees. These findings confirm COBL4 as a protein involved in organizing cellulose biosynthesis in plants. The increased cellulose DP and subsequent proportion of crystalline cellulose suggest that COBL4, in part, affects cellulose biosynthesis efficiency. To further resolve the role that cellulose ultrastructure plays in limiting intrusive tip growth of fibre cells, we measured xylary fibre lengths of AtCOBL4 overexpression poplar lines. Overexpression lines had on average shorter fibres than wild-type trees. This demonstrates that increased DP and the overall structural organization of cellulose, mediated by AtCOBL4, may be sufficient to restrict intrusive growth of fibre cells.
Arabinogalactan proteins (AGPs) are cell wall proteins with abundant glycosylation, belonging to the large, multi-gene hydroxyproline-rich glycoprotein (HRGP) family. It has been reported that AGPs may contribute to cell expansion, xylem cell differentiation and secondary cell wall deposition. However, the roles of specific AGP in wood developmental processes have never been thoroughly elucidated. Therefore, the objective of this thesis was to investigate the functional role(s) of three AGPs in wood cell wall development. Specifically, the lysine-rich AGP18; a classical AGP, AGP9; and an AGP peptide, AGP14 were studied, because they demonstrated high gene expression levels in the developing xylem of Populus trichocarpa during transcriptome re-sequencing initiatives. Based on the phenotypic changes observed when PtAGP18 was down-regulated in transgenic poplar trees and Arabidopsis atagp18 T-DNA mutant analyses, I showed roles for AGP18 in fiber cell shape and fiber secondary cell wall formation (Chapter 2). Moreover, the poplar PtAGP18 was able to complement the Arabidopsis atagp18 T-DNA mutants which displayed altered fiber shape and cell wall thickness, indicating that these two genes are functionally equivalent (Chapter 2). Analysis of the growth of Arabidopsis hypocotyls cultivated in darkness revealed that AGP18 is involved in cell expansion (Chapter 2). In parallel, I showed that the AGP9 affects xylem vessel differentiation and vessel cell expansion (Chapter 3). A role for AGP9 in cell expansion was also demonstrated with Arabidopsis agp9 mutant hypocotyls grown in the dark (Chapter 3). Furthermore, AGP14 appears to contribute to cell wall formation in poplar (Chapter 4). Taken together, the functional characterization of these AGPs suggests that AGP18 and AGP9 play roles in the development of fibers and vessels, respectively. However, further research is needed to delineate the exact cellular and molecular mechanisms through which AGPs contribute to secondary xylem development.
Lignin is a critical structural component of plants, providing vascular integrity and mechanical strength. Lignin precursors, monolignols, must be exported to the extracellular matrix where random oxidative coupling produces a complex lignin polymer. The objectives of this study were twofold: to determine the timing of lignification, with respect to programmed cell death during Arabidopsis thaliana primary xylem development, and to determine which cells are contributing to the lignification of tracheary elements and fibres. This thesis demonstrates that lignin deposition is not exclusively a post-mortem event, but also occurs prior to programmed cell death. Radiolabelled monolignols were not detected in the cytoplasm or vacuoles of tracheary elements or neighbours. To experimentally define which cells in lignifying tissues contribute to lignification in intact plants, a microRNA against CINNAMOYL CoA-REDUCTASE1, driven by the promoter from CELLULOSE SYNTHASE 7 (proCESA7:miRNA CCR1), was used to silence monolignol biosynthesis in cells developing secondary cell walls. When monolignol biosynthesis was knocked down specifically in the cells with thickened secondary cell walls, but not in the neighbouring cells, lignin was still deposited in the xylem secondary cell walls. This indicates that “good neighbour” cells are sufficient to produce lignin in the vascular bundles. Surprisingly, this was not the case in the interfascicular fibres, where a dramatic reduction in cell wall lignification demonstrates that these extra-xylary fibers undergo cell autonomous lignification. When a fibre-specific promoter (proAtPEROXIDASE64) was used to drive the miRNA, autonomous extraxylary fibre lignification was again observed, as was non-cell autonomous lignification between xylary fibres and neighbouring tracheary elements. These effects may have reflected compensatory mechanisms in response to lignin downregulation, so to demonstrate that discrete cell populations, such as xylem parenchyma, do contribute to lignification, genes encoding enzymes catalyzing the synthesis of novel monolignol conjugates were introduced into wild-type Arabidopsis using cell population-specific promoters. The detection of novel monolignol conjugates in the cell wall by chemical analysis and fluorescence microscopy supported the contribution of tracheary elements and fibres to lignification and also revealed that xylary parenchyma cells are producing monolignol substrates and acting as “good neighbours” to tracheary elements and xylary fibres during lignification.
No abstract available.
Master's Student Supervision (2010 - 2018)
Lignin, one of the three main components of the secondary cell wall, is an important phenolic biopolymer that provides strength and rigidity to the cell walls of tracheary elements and fibers in vascular plants. Lignin is composed of phenolic alcohol monomers called monolignols, which are synthesized in the cytoplasm. These monolignols are exported to the apoplast where they polymerize by random radical coupling following oxidation by laccases and peroxidases. Two laccases found in Arabidopsis thaliana, LAC4 and LAC17, were localized to secondary cell wall, and required for lignification of protoxylem tracheary elements. The localization of LAC4 and LAC17 to spiral secondary cell walls could be due to either: 1) the diffuse secretion of laccases followed by remobilization to the secondary wall, or 2) a reorientation of post-Golgi vesicle trafficking to secondary cell wall specific plasma membrane domains. Localization studies with LAC4-RFP driven by a constitutive promoter found laccases localized to all regions of the primary cell wall prior to differentiation, then the localization shifted into the helical secondary cell wall bands during protoxylem tracheary elements differentiation. This change in localization suggests there is a change in vesicle traffic during secretion of secondary cell wall components (such as laccases). Furthermore, Fluorescence Recovery After Photobleaching (FRAP) was used to determine if laccase localization in secondary cell walls was due to constraint by the secondary cell walls or exclusion from the primary cell wall. Laccases were also found to be immobile in secondary cell wall domains, but mobile when expressed ectopically in primary cell wall domains. Further drug and mutant FRAP studies found laccases remain immobile in the absence of secondary cell wall: cellulose, xylan, lignin and xylan/lignin. These results suggest laccases are not only anchored to secondary cell wall specific components but may be anchored to multiple components of the secondary cell wall or an unknown component of the secondary cell wall.
Lignin is a phenolic polymer that plays important roles in the structural integrity ofplants. Both peroxidases and laccases have been implicated in the polymerization of lignin, andmutant analyses have conclusively demonstrated a role for laccases in lignification ofArabidopsis thaliana stems. However, the oxidative enzymes that polymerize lignin inprotoxylem tracheary elements (TEs) have not been defined. Induction of the mastertranscription factor VASCULAR RELATED NAC-DOMAIN 7 (VND7) causes systemic transdifferentiationinto protoxylem TEs, providing an inducible-experimental model system to studyprotoxylem TE differentiation. The transcriptome of these lines has been well characterized, andtwo laccases, LAC4 and LAC17, are strongly expressed following induction of protoxylem TEdevelopment. To test if LAC4 and LAC17 are necessary for the lignification of protoxylem TEs,the inducible VND7 construct was transformed into the lac4-2/lac17 double mutant backgroundand fluorescently labeled monolignols were exogenously applied to differentiating protoxylemTEs. Labeled polymerized lignin was only detected in the wild-type protoxylem TEs, but not inlac4-2/lac17 protoxylem TEs. To test if laccases alone are sufficient to promote lignification, theconstitutive 35S promoter was used to drive either LAC4 or LAC17 in wild-type plants, resultingin strong ectopic lignification of primary cell walls upon application of fluorescently labeledmonolignols. Fluorescently tagged laccases were transformed into the inducible protoxylem TEssystem, where they specifically localize to the secondary, but not primary, cell walls ofprotoxylem tracheary elements. This research shows that LAC4 and LAC17 are necessary andsufficient for the lignification of secondary cell wall domains of protoxylem TEs and that theyare specifically localized to these domains.
- Organization of Xylan Production in the Golgi During Secondary Cell Wall Biosynthesis (2019)
Plant Physiology, 181 (2), 527--546
- Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation. (2018)
Proceedings of the National Academy of Sciences of the United States of America,
- Distribution, mobility, and anchoring of lignin-related oxidative enzymes in Arabidopsis secondary cell walls (2018)
Journal of Experimental Botany, 69 (8), 1849--1859
- Male functionality in Garcinia celebica L., a candidate ancestor species of mangosteen (G. mangostana L.) (2018)
- Patterned Deposition of Xylan and Lignin is Independent from that of the Secondary Wall Cellulose of Arabidopsis Xylem Vessels. (2018)
The Plant cell,
- The cell biology of secondary cell wall biosynthesis. (2018)
Annals of botany,
- The transport of monomers during lignification in plants: anything goes but how? (2018)
Current opinion in biotechnology,
- Defining the Diverse Cell Populations Contributing to Lignification in Arabidopsis Stems (2017)
Plant Physiology, 174 (2), 1028--1036
- Multiscale Structural Analysis of Plant ER–PM Contact Sites (2017)
Plant and Cell Physiology,
- Fine structure of the Arabidopsis stem cuticle: effects of fixation and changes over development (2016)
Planta, 244 (4), 843-851
- Free-Flow Electrophoresis of Plasma Membrane Vesicles Enriched by Two-Phase Partitioning Enhances the Quality of the Proteome from Arabidopsis Seedlings (2016)
Journal of Proteome Research, 15 (3), 900-913
- Histology and cell wall biochemistry of stone cells in the physical defence of conifers against insects (2016)
Plant, Cell and Environment, 39 (8), 1646-1661
- Stitching Organelles: Organization and Function of Specialized Membrane Contact Sites in Plants (2016)
Trends in Cell Biology, 26 (9), 705-717
- Engineering monolignol p-coumarate conjugates into poplar and arabidopsis lignins (2015)
Plant Physiology, 169 (4), 2992-3001
- Visualization of cellulose synthases in Arabidopsis secondary cell walls (2015)
Science, 350 (6257), 198-203
- Golgi- and Trans-Golgi Network-Mediated Vesicle Trafficking Is Required for Wax Secretion from Epidermal Cells (2014)
Plant Physiology, 164 (3), 1250-1260
- Manipulating lignin deposition (2014)
Canadian Journal of Plant Science, 94 (6), 1043-1049
- Acyl-lipid metabolism. (2013)
The Arabidopsis book / American Society of Plant Biologists, 11, e0161
- Cell Wall Polysaccharides are Mislocalized to the Vacuole in echidna Mutants (2013)
Plant and Cell Physiology, 54 (11), 1867-1880
- ECHIDNA-mediated post-Golgi trafficking of auxin carriers for differential cell elongation (2013)
Proceedings of the National Academy of Sciences of the United States of America, 110 (40), 16259-16264
- Neighboring parenchyma cells contribute to Arabidopsis xylem lignification, while lignification of interfascicular fibers is cell autonomous (2013)
Plant Cell, 25 (10), 3988-3999
- Patterning and lifetime of plasma membrane-localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells (2013)
Plant Physiology, 162 (2), 675-688
- Trans-Golgi network localized ECHIDNA/Ypt interacting protein complex is required for the secretion of cell wall polysaccharides in Arabidopsis (2013)
Plant Cell, 25 (7), 2633-2646
- Plant cell wall secretion and lipid traffic at membrane contact sites of the cell cortex (2012)
Protoplasma, 249 (SUPPL), 19-23
- The endo-1,4-beta-glucanase Korrigan exhibits functional conservation between gymnosperms and angiosperms and is required for proper cell wall formation in gymnosperms (2012)
New Phytologist, 193 (4), 1076-1087
- ABC transporters coordinately expressed during lignification of Arabidopsis stems include a set of ABCBs associated with auxin transport (2011)
Journal of Experimental Botany, 62 (6), 2063-2077
- Conserved Arabidopsis ECHIDNA protein mediates trans-Golgi-network trafficking and cell elongation (2011)
Proceedings of the National Academy of Sciences of the United States of America, 108 (19), 8048-8053
- Dynamic compartmentalization of SCAR/WAVE signaling scaffolds and active pools of ARP2/3 during polarized growth. (2011)
Molecular Biology of the Cell, 22
- Self-Immobilizing Fluorogenic Imaging Agents of Enzyme Activity (2011)
Angewandte Chemie-International Edition, 50 (1), 300-303
- Arabidopsis ABCG Transporters, Which Are Required for Export of Diverse Cuticular Lipids, Dimerize in Different Combinations (2010)
Plant Cell, 22 (9), 3066-3075
- ATP-Binding Cassette Transporter G26 Is Required for Male Fertility and Pollen Exine Formation in Arabidopsis (2010)
Plant Physiology, 154 (2), 678-690
- Secondary Cell Wall Deposition in Developing Secondary Xylem of Poplar (2010)
Journal of Integrative Plant Biology, 52 (2), 234-243
- SPIKE1 Signals Originate from and Assemble Specialized Domains of the Endoplasmic Reticulum (2010)
Current Biology, 20 (23), 2144-2149
- A unique program for cell death in xylem fibers of Populus stem (2009)
Plant Journal, 58 (2), 260-274
- Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface (2009)
Plant Cell, 21 (4), 1230-1238
- Plant cuticles shine: advances in wax biosynthesis and export (2009)
Current Opinion in Plant Biology, 12 (6), 721-727
- Analysis of the golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage (2008)
Plant Cell, 20 (6), 1623-1638
- Cortical microtubules mark the mucilage secretion domain of the plasma membrane in Arabidopsis seed coat cells (2008)
Planta, 227 (6), 1363-1375
- Identification of the wax ester synthase/acyl-coenzyme a:diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis (2008)
Plant Physiology, 148 (1), 97-107
- Perturbed Lignification Impacts Tree Growth in Hybrid Poplar-A Function of Sink Strength, Vascular Integrity, and Photosynthetic Assimilation (2008)
Plant Physiology, 148 (3), 1229-1237
- Plant ABC proteins - a unified nomenclature and updated inventory (2008)
Trends in Plant Science, 13 (4), 151-159
- Sealing plant surfaces: Cuticular wax formation by epidermal cells (2008)
Annual Review of Plant Biology, 59, 683-707
- Tracking monolignols during wood development in lodgepole pine (2008)
Plant Physiology, 147 (4), 1750-1760
- Use of Arabidopsis eceriferum mutants to explore plant cuticle biosynthesis. (2008)
Journal of visualized experiments : JoVE, (16)
- Biosynthesis and Transport of Plant Cuticular Waxes (2007)
Annual Plant Reviews, 23, 182-215
- Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion (2007)
Plant Journal, 52 (3), 485-498
- Composition of Plant Cuticular Waxes (2007)
Annual Plant Reviews, 23, 145-181
- Influence of poly(ethylene glycol) grafting density and polymer length on liposomes: Relating plasma circulation lifetimes to protein binding (2007)
Biochimica et Biophysica Acta - Biomembranes, 1768 (6), 1367-1377
- The cytochrome p450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of arabidopsis (2007)
Plant Physiology, 145 (3), 653-667
- The cell biology of wood formation: from cambial divisions to mature secondary xylem (2006)
Canadian Journal of Botany-Revue Canadienne De Botanique, 84 (4), 631-639
- Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis (2005)
Plant Physiology, 139 (4), 1649-1665
- First steps in understanding the export of lipids to the plant cuticle (2005)
Plant Biosystems, 139 (1), 65-68
- Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation (2005)
Plant Journal, 42 (5), 618-640
- Cellular changes associated with rest and quiescence in winter-dormant vascular cambium of Pinus contorta (2004)
Trees-Structure and Function, 18 (4), 373-380
- MUCILAGE-MODIFIED4 encodes a putative pectin biosynthetic enzyme developmentally regulated by APETALA2, TRANSPARENT TESTA GLABRA1, and GLABRA2 in the Arabidopsis seed coat (2004)
Plant Physiology, 134 (1), 296-306
- Plant cuticular lipid export requires an ABC transporter (2004)
Science, 306 (5696), 702-704
- Biosynthesis and secretion of plant cuticular wax (2003)
Progress in Lipid Research, 42 (1), 51-80
- Cellular machinery of wood production: differentiation of secondary xylem in Pinus contorta var. latifolia (2002)
Planta, 216 (1), 72-82
- Ultrastructure of vascular cambial cell cytokinesis in pine seedlings preserved by cryofixation and substitution (2002)
Protoplasma, 220 (1-2), 39-49
- Conjugative junctions in RP4-mediated mating of Escherichia coli (2000)
Journal of Bacteriology, 182 (10), 2709-2715
- Optimizing conditions for tobacco BY-2 cell cycle synchronization - Rapid communication (1998)
Protoplasma, 202 (3-4), 232-236
- Caffeine inhibits cell plate formation by disrupting membrane reorganization just after the vesicle fusion step (1996)
Protoplasma, 195 (1-4), 144-155
- CYTOKINESIS IN TOBACCO BY-2 AND ROOT-TIP CELLS - A NEW MODEL OF CELL PLATE FORMATION IN HIGHER-PLANTS (1995)
Journal of Cell Biology, 130 (6), 1345-1357
- DEVELOPMENTAL PLASTICITY OF THE GOLGI-APPARATUS (1995)
Journal of Cellular Biochemistry, , 439
- SILICON IN CELL-WALLS AND PAPILLAE OF CUCUMIS-SATIVUS DURING INFECTION BY SPHAEROTHECA-FULIGINEA (1994)
Physiological and Molecular Plant Pathology, 44 (4), 237-242
- THE EFFECTS OF SILICON SUPPLEMENTATION ON CUCUMBER FRUIT - CHANGES IN SURFACE CHARACTERISTICS (1993)
Annals of Botany, 72 (5), 433-440
- IMMUNOFLUORESCENT LOCALIZATION OF PLASMA-MEMBRANE H+-ATPASE IN BARLEY ROOTS AND EFFECTS OF K-NUTRITION (1992)
Plant Physiology, 99 (4), 1509-1514
- DISTRIBUTION OF SILICON IN CUCUMBER LEAVES DURING INFECTION BY POWDERY MILDEW FUNGUS (SPHAEROTHECA-FULIGINEA) (1991)
Canadian Journal of Botany-Revue Canadienne De Botanique, 69 (1), 140-146
- MOBILITY AND DEPOSITION OF SILICON IN CUCUMBER PLANTS (1991)
Plant Cell and Environment, 14 (5), 485-492
- THE INFLUENCE OF SILICON ON CYTOLOGICAL INTERACTIONS BETWEEN SPHAEROTHECA-FULIGINEA AND CUCUMIS-SATIVUS (1991)
Physiological and Molecular Plant Pathology, 39 (6), 403-414
- ENDOCYTOSIS IN ELONGATING ROOT-CELLS OF LOBELIA-ERINUS (1990)
Journal of Cell Science, 97, 157-165