Abstract
Eduard Strasburger, director of the Botany Institute and the Botanical Garden at the University of Bonn from 1881 to 1912, was one of the most admirable scientists in the field of plant biology, not just as the founder of modern plant cell biology but in addition as an excellent teacher who strongly believed in “education through science.” He contributed to plant cell biology by discovering the discrete stages of karyokinesis and cytokinesis in algae and higher plants, describing cytoplasmic streaming in different systems, and reporting on the growth of the pollen tube into the embryo sac and guidance of the tube by synergides. Strasburger raised many problems which are hot spots in recent plant cell biology, e.g., structure and function of the plasmodesmata in relation to phloem loading (Strasburger cells) and signaling, mechanisms of cell plate formation, vesicle trafficking as a basis for most important developmental processes, and signaling related to fertilization.
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Introduction
Eduard Strasburger’s life (1844–1912) and scientific work distinguishes him not just as the founder of modern plant cell biology but also as an excellent teacher who strongly believed in “education through science” and who, as a scientist, always took into consideration the applicability and transfer of knowledge to neighboring scientific fields like medicine and pharmacology, and even to industry. Therefore, he exercised his profession in a manner we today regard as a state-of-the-art performance, more than 100 years later.
He was born on 1st February 1844 in Warsaw, when the city was under Russian governance and when society in Lower Silesia was shaken by the preindustrial revolution (Weberaufstand: rage against the machine). At that time, Heinrich Heine, the German poet, published “Deutschland—Ein Wintermärchen” (Germany—winter fairy tale), denouncing the social economic situation in Germany in his typical ironic manner. In those days, higher education, notably science and research at universities, was clearly restricted to the upper class and exclusively to male individuals. Eduard Adolf Strasburger was the eldest son of the merchant Eduard Gottlieb Strasburger. His family was of German descent, enjoying life in existential security. Nevertheless, the industrial, social, and economic turmoil he came to witness shaped his lifestyle and attitudes, in particular his behavior related to his students and colleagues.
Studies, scientific roots and carrier, most important publications
After he finished high school (gymnasium) in Warsaw, he enrolled at the Sorbonne in Paris in 1862 to study science, continued in 1864 at Bonn University, and then moved on to Jena University. It was in Bonn, inspired by his teacher Hermann Schacht, that he realized the importance and power of microscopy for the study of plant biology. Even more important for Strasburger’s scientific thinking was Julius Sachs who, after his habilitation with physiologist Jan Evangeliste Purkyně at Prague (compare Žárský this issue), established researching and teaching experimental and sensory physiology of plants at the Agricultural Academy Bonn-Poppelsdorf. Here, young Strasburger began to see how function is related to structure and vice versa. In 1866, at the age of 22, he earned his PhD at Jena University under the supervision of Nathanael Pringsheim. His dissertation “Asplenium bulbiferum, ein Beitrag zur Entwicklung des Farnblattes mit besonderer Berücksichtigung der Spaltöffnungen und des Chlorophylls” reflects his mounting interest in developmental processes. No wonder that Ernst Haeckel, the famous German Darwinist, working at that time at Jena University in the field of comparative embryology of animals, became Strasburger’s most important teacher, friend, and colleague. Strasburger accompanied Haeckel on trips to Egypt and to the Red Sea.
Several trips to the Mediterranean area shaped his enthusiastic view for nature, biodiversity and life in general. His book “Streifzüge an der Riviera” (first edition 1895, Gustav Fischer, Jena), and even more so the second edition in 1904, illustrated by Louise Reusch, was an insightful compendium extracted from five journeys to different areas between Hyeres (France) and Cinque Terre (Italy), describing the fascinating life of plants in the area. Not only did he treat in masterly fashion the classic ancient works on the life and meaning of plants, e.g., of Aristoteles, Demokrites, Plinius, Vergilius, and others, but he also reported on historical events in the area and regional customs including ingredients and protocols for the production of different alcoholic beverages customary to the area. He also was fondly interested in the industrial use of plant products like oil, and even in perfumes from the Grasse area. Entertaining as well as educational, this compendium was at his time, and still is today, worth reading by everyone traveling along the Franco-Italian Mediterranean coast. Nevertheless, he was anxious to remark that his report was not meant as a traveling guide in the common sense “diese Streifzüge bezwecken nicht, einen Reiseführer zu ersetzen, sie sollen vielmehr dazu beitragen, die Naturschätze dieser einzig schönen Gegend zu heben, ihr Verständnis zu fördern und die Freude an ihren einzigartigen Reizen zu steigern” (from the foreword of Strasburger 1904).
In 1867, his dissertation on Asplenium bulbiferum has been published in Pringsheim’s Jahrbücher der wissenschaftlichen Botanik and was the basis for Strasburger’s habilitation and teaching at Warsaw University in the same year, i.e., at the age of 23 years. Already in 1869, he went back to Jena, and here, with the support of Haeckel, he was finally appointed as ordinarius for botany. In Jena, he performed and published several of his famous microscopic investigations related to the division of plant cells in a first (1875) and a second (1876) edition entitled “Über Zellbildung und Zelltheilung”, and in 1882 a third update on this topic under the title “Über den Theilungsvorgang der Zellkerne und das Verhältnis der Kerntheilung zur Zelltheilung” (Strasburger 1875, 1876, 1882).
In 1881, Eduard Strasburger moved to Bonn, where he became ordinarius of botany at the University of Bonn, as the successor of Johannes von Hanstein. Here, he dedicated himself to research and teaching for more than 30 years in the baroque Poppelsdorf Palace surrounded by the Botanical Garden (Fig. 1). In 1884, he published two important monographs. The first, which has since been re-edited numerous times, is: “Das Botanische Practicum” (Strasburger 1884a). In a volume of 664 pages including 182 xylographs, he presents information mainly on the anatomy of about 210 plant species. Four exhaustive registers related to the investigated plants, description of the scientific instruments used in the study, reagents, recipes, and experimental treatments of his study samples, and, finally, even some notes on general topics, turn the first edition into a bible for the science community of his time on plant anatomy, cytology, and cell biology. In the second book, “Neue Untersuchungen über den Befruchtungsvorgang bei den Phanerogamen als Grundlage für eine Theorie der Zeugung” (Strasburger 1884b), he presents comparative investigations of several plant families of ferns and gymnosperms related to the growth of pollen tubes toward the ovule and the process of fertilization. Herein, he presents his ideas of sexual reproduction and inheritance.
In 1894, together with his colleagues, Fritz Noll, Heinrich Schenck, and Andreas Franz Wilhelm Schimper, he founded the textbook Lehrbuch der Botanik für Hochschulen (1894). Later on, it was called “The Strasburger” or “The Four-Men-Book”, due to the number of authors. This monography has turned into a milestone for plant biologists of all generations since. On the forefront of plant science and exhaustive in scope, it is currently in its 36th edition, entitled “Strasburger—Lehrbuch der Botanik. Begründet von E. Strasburger” (Bresinsky et al. 2008).
Scientific highlights: methods–karyokinesis–cytokinesis–cytoplasmic streaming–fertilization
Methodological aspects
Successful microscopy depends at least on three parameters: the quality of the microscope, the qualification of the experimenter, and the quality of sample preparation. Concerning the quality of microscopes, Jena was the distinguished site for optical instruments made for microscopic investigations because this was the home of ZEISS and the domain of the physicist Ernst Abbe. As Eduard Strasburger proclaims in the preamble to his famous botany laboratory textbook: “Wir Mikroskopiker fühlen uns aber vor Allem dem Physiker Ernst Abbe verpflichtet, durch dessen rastlose Bestrebungen die jetzige Leistungsfähigkeit unserer Instrumente hauptsächlich erzielt wurde” (Strasburger 1884a). He used for example vacuum pumps to evacuate samples for better translucence, heatable object tables to perform experiments under the microscope, and eyepiece micrometers for measurements of cell size, cell wall thickness, etc. Thus, in Jena, started a tremendously successful industrial–scientific collaboration aimed at the improvement of mechano-optical instrumentation for the benefit of scientific progress. Ernst Abbe and Eduard Strasburger were the ingenious scientists behind this endeavor, demonstrating that, as in many other cases, joining forces is a better recipe for success than indulging in competition.
With respect to the pretreatment of tissue and the preparation of samples, Strasburger was the first botanist who used hardening of samples not only by alcohol, mostly absolute alcohol, but also by 1 % acetic acid, chromic, or picric acid. On the basis of Flemming’s protocols, published for animal cells, he used for the first time different staining procedures with plant material (Fig. 2), which was called hardening and tinction: “Die mikroskopische Tinctions-Technik macht so bedeutende Fortschritte, dass Untersuchungen, deren Resultate unter dem Einfluss von Tinctions-Methoden stehen, oft schon nach Ablauf weniger Jahre eine erneute Prüfung verlangen” (from the foreword to Strasburger 1884b). In 1877, at the botanical conference in Amsterdam, these fixation and tinction methods were criticized as artifacts. It was Anton de Bary who defended Strasburger’s results, related to the heredity of the nucleus, which he was able to demonstrate by the new tinction method.
By his hardening and tinction method, Strasburger was able to describe structures related to important functions in plants like nutrition uptake and sugar transport. He documented already modifications in the radial walls of endodermis cells as black deposits (Strasburger 1884a, b), later called Casparian strip, honoring Robert Caspary, a botanist in Bonn before Strasburger’s time. The formation and the function of this barrier structure controlling transport processes are still important research topics in plant biology (see for instance Schreiber 2010). He also discovered protein rich-cells (eiweißhaltige Zellen; Strasburger 1891), later called Strasburger cells, which are involved in phloem loading of gymnosperms. “Despite of more than 130 years of research (e.g., Kollmann and Schumacher 1964; Sauter et al. 1976; van Bel 1993), phloem loading is far from being understood in gymnosperms” (Liesche et al. 2011), as it is with the structure and function of plasmodesmata (Strasburger 1913; Lucas et al. 2009).
Karyokinesis—division of nucleus
For investigations related to karyokinesis, he used mainly two species: Tradescantia virginiana (Dicotyledonae) and Fritillaria imperialis (Monocotyledonae). From the former, he prepared stamen hairs (Fig. 3); from the latter, the first layer of developing endosperm from embryo sacs. By a comparison of different stages of nuclear divisions, he was able to describe the sequence and time course of karyokinesis. In principle, he was the first to determine the duration of phases during cell division. Today, textbook data (Weiler and Nover 2008) reporting the duration of the different nuclear division phases in cells of Tradescantia stamen hairs closely match Strasburger’s observations: total time, 200 min; anaphase, 15 min; and telophase, 30 min. He was able to experimentally delay these processes by lowering the temperature on the microscope stage (compare methods). By this experimental approach, he even shifted the mitotic rhythm from night to day. In addition, he described spindle-like structures and the positioning of chromatin material in the equatorial plate. Since he had no concept of chromosomes as individual entities of inheritance, he held the belief that chromatin material is arranged in a single, giant thread. But then he was the first to demonstrate by cytological staining as well as live observation the longitudinal splitting of this material and its separation into two daughter nuclei; thus, he had to reconsider his “single thread idea” and later dropped it. In 1888, the chromatin material was called chromosomes by Heinrich Wilhelm Waldeyer.
Meanwhile, the structures, molecules, and mechanisms involved in the process of mitosis/karyokinesis have been investigated intensively in animals, plants, and fungi, and this includes a detailed comparison with the equivalent process of division in the prokaryotes, plastids, and mitochondria (Wickstead and Gull 2007). Surprisingly, there is still a remarkable lack of knowledge in the field, in particular related to the process of chromosome segregation in flowering plants (Baskin and Cande 1990). To give an example: Cytoplasmic dynein dynactin, respectively, constituting macromolecular motor complexes in animal cells, are still in debate for cells in higher plants. Sequence analysis of the Arabidopsis genome has revealed that genes coding for dynein heavy chains are indeed absent from this dicotyledonous plant (Lawrence et al. 2001). As a consequence, flowering plants are thought to have evolved an alternative mechanism of chromosome segregation and organelle motility based on kinesin as components of the motor complexes rather than dynein (i.e., Bannigan et al. 2008; Vale 2003). However, just 1 year later, four dynein heavy-chain genes have been discovered in silico in the whole-genome shotgun sequence data of Oryza sativa (King 2002), indicating a major difference between monocots and dicots. Certainly, extended investigations are necessary by comparing species from the different evolutionary branches of the flowering plants to understand the meaning of this apparent dichotomy. In his investigations, a century ago, Strasburger was very much aware of the usefulness of such phylogenetic approaches (for recent research, compare Knoop and Müller 2009) because comparing the expression and variation of a certain cytological characteristic among the evolutionary branches of the plant kingdom helps separate family-specific traits from functionally important characteristics.
Cytokinesis—cell plate formation-cell division
Cell division, i.e., cytokinesis, in its various forms is one of Strasburger’s major research topics. His study objects ranged from algae to flowering plants, e.g., Spirogyra orthospira, Phaseolus multiflorus, T. virginiana, and many others. For Spirogyra, he describes in extenso the process of cell division (Fig. 4) by a ring-like, protoplasma-rich structure in the region of the division plane coinciding with the formation of a cell plate opposite to the ring-like structure. He further observed the progression of the cell plate, the dissection of the band-like chloroplast, and the final steps of cross wall material. This particular variant of cytokinesis has much later been recognized as an intermediate form between the centripetal contractile cytokinetic ring mechanism, generally employed in the animal kingdom, and the phragmoplast-based centrifugal cell plate mechanism, observed in all phanerogamous plants (Pickett-Heaps et al. 1999; Sawitzky and Grolig 1995).
With higher plants, Strasburger investigated different tissues and cell types from several species, e.g., epidermis cells (guard mother cells) from Iris pumila, young endosperm cells of P. multiflorus and F. imperialis, stamen hair cells of T. virginiana, and cambium cells and pollen mother cells of several conifers. Again, he was able to clearly describe in living and fixed material the formation of cell plates in detailed stages (Figs. 3 and 5): early formation of the ring-like structure, later coined pre-prophase band (Pickett-Heaps and Northcote 1966); formation of a barrel-shaped structure (phragmoplast; see Baker et al. 1968); and initiation of the new cell wall within this barrel-shaped structure by aggregation of protoplasmic particles (vesicles). Since then, these membraneous/vesiculous structures have been intensely studied beginning with the advent of fine structure research (i.e., Whaley and Mollenhauer 1963) and still today by in vivo fluorochrome labeling and GFP fusion techniques (Dhonukshe et al. 2006). Since the origin of these vesicles can now been tracked down, a new refined model for the assembly mechanism of the cell plate involving endomembrane recycling between the parental plasma membrane and the cell plate membrane has been formulated (Dhonukshe et al. 2007), challenging the established secretory vesicle model (Reichardt et al. 2007).
Eduard Strasburger also saw the docking of the new cell wall/cell plate at the predisposed mother cell wall (lateral walls). He even observed “seeking” movements of the late cell plate before the final docking. It is important to point out that he observed the process of cytokinesis not just in meristematic cells rich in protoplasm but also in vacuolated cells of the leaf epidermis and in vascular cambium. He described equal and unequal cell division, e.g., in guard cells, and, last not least, he was able to determine the exact thickness of 0.9 μm for the new cell wall.
It is one of the paradigms of cell biology that karyokinesis (i.e., mitosis) is followed by cytokinesis and that for the cells to be able to determine the plane of division is a very important integral part of it. A shift in the division plane, from transversal to longitudinal, from periclinal to anticlinal, or from equal to unequal, often marks the beginning of a new developmental sequence (Rasmussen et al. 2011). Strasburger had already observed many such examples. However, it is interesting to see that by his careful comparative approach looking at algae, lower plants, and higher plants, he could not help to note that there are strange exceptions to this rule.
When commenting on his observations in Phaseolus in comparison with those in Spirogyra and other algae, he wrote: “Hier (i.e. Phaseolus) wirken eben noch Zellkern und Zellprotoplasma im Geschäft der Zelltheilung zusammen, während sich bei Spirogyra Kerntheilung und Protoplasmatheilung voneinander bedeutend emancipirt haben” (from Strasburger 1875, p. 107). It is now an accepted view that mitosis and cytokinesis can become uncoupled, such as in some green algae (see for instance Mine et al. 2008) as well as higher plant tissues, such as the syncytial endosperm (Brown et al. 2003; Otegui et al. 2001; for a more comprehensive treatment of this aspect of Strasburger’s impact on cell theory, see Baluška et al. 2012).
Cytoplasmic streaming
Strasburger was extremely fascinated by the dynamic behavior of the protoplasm. For the century to come, his observations of cytoplasmic streaming in different algae like Spirogyra and Nitella; staminal hairs of flowering plants such as T. virginiana, Momordica elaterium, and some Lamiaceae; root hairs of Hydrocharis morsus-ranae; and mesophyll cells of Vallisneria spiralis have been followed, repeated, and refined by many researchers beginning with his successor, Hans Fitting (Fitting 1937), and subsequently picked up by others such as Robert Jarosch and his students (Jarosch 1960), Noburo Kamiya and his students (Kamiya 1962), and Reiko Nagai and her students (Ryu et al. 1995; see also Liebe and Menzel 1995), to name just a few (for a comprehensive review, see Shimmen and Yokota 2004). Watching Spirogyra under the microscope, Strasburger reported on tiny and massive streams of granulated protoplasm, in particular grains of different sizes. The largest grains he identified as starch grains, which sometimes stop movements or even change their direction of movement. When cell division starts, movable particles accumulate close to the peripheral ring-like structure (pre-prophase band). By dissecting cell threads of Spirogyra, he was even able to produce protoplasts and observe the vibrating movements of particles. He also described the stationary layer of the peripheral cytoplasma in Nitella internodal cells, hosting chlorophyll grains (chloroplasts), and the “Indifferenzstreifen” (indifferent zone) free of chloroplasts and separating two large streams of cytoplasm.
In staminal hairs, Strasburger differentiated between peripherally located hyaloplasm, with embedded microsomes, and central cytoplasm. He describes netlike plasma streams of variable thickness forming anastomoses and showing different streaming velocities. Even in the smallest streams, he observed bidirectional movements of particles, whereas nuclei were moving very slowly or not at all, mostly functioning as centers for attraction for the major cytoplasmic strands. In experiments with Vallisneria, he found out that the velocity of streaming was temperature-dependent and started after raising the temperature. As yet, he did not take into consideration light as an external trigger of cytoplasmic streaming (see Takagi and Nagai 1983). Strasburger also studied cytoplasmic streaming in root hairs, where he described the occurrence of very fast bulk streaming in an inverse fountain-like manner. Besides the unicellular rhizoid of the algae Chara (Sievers et al. 1991; Ackers et al. 1994), this cell type has become a favorite model system in plant cell biology and cell polarity (Baluška et al. 2000; Emons and Ketelaar 2009). Streaming, which has now been recognized as being based on the actin cytoskeleton, has become a major issue (see Voigt et al. 2005).
In the last century, investigations of cytoplasmic streaming were mainly related to the force-producing system which drives the movement of cellular organelles and smaller particles—in Strasburger’s terminology, microsomes (Grolig and Pierson 2000; Shimmen and Yokota 2004)—which has led to its mathematical modeling (Alt 1987). Our recent knowledge about the diversity of myosin molecular motors (Reichelt and Kendrick-Jones 2000; Sparks 2011) and filamentous tracks of actin (Meagher et al. 2000) goes back to these investigations. Most recent papers demonstrate the importance of the actomyosin system in vesicle trafficking involved in almost all developmental processes like polar growth of single cells (Hepler et al. 2001), endocytosis (Šamaj et al. 2005), signal transduction networks (Holweg and Nick 2004; Schlicht et al. 2008), and cellular long-distance transport (Verchot-Lubicz and Goldstein 2010). Nevertheless, even in the field of cytoplasmic streaming, many important gaps in current research remain unsolved (Pollack 2001; Verchot-Lubicz and Goldstein 2010).
Fertilization
In 2005, Elizabeth Lord, an established expert in the field, wrote: “the biology of the in vivo pollen tube cell remains somewhat of a mystery though, due to the technical difficulties encountered in observing pollen tubes in the style” (Lord 2005). So much more are Strasburger’s investigations to be admired. He observed the growth of pollen tubes, their entry into the style and finally into the embryo sac in members of more than 30 families of angiosperms using living (Fig. 6) as well as fixed material (Strasburger 1884b). He was able to differentiate between the vegetative nucleus and the two generative nuclei in the growing pollen tube. He described in detail the cells and nuclei of the embryo sac as well as processes, which eventually result in fertilization, the formation of the embryo and the endosperm. He already reported synergides, which might secrete substances that guide the pollen tube to the micropyle and egg cell, and that at least one of the synergides degenerates and disappears. By comparison with other fertilization processes in the plant kingdom, he came to the general conclusion that fertilization results from the copulation (Strasburger’s terminology) of nuclei of sperm and egg cell, nuclei are bearing the characteristic features of organisms, and the cytoplasm does not play a role in fertilization. He even saw an analogy between the cytoplasm of the pollen tube, the angiosperm vegetative cell, and the cilia of spermatozoids of lower plants, where the archegonial canal filled with cytoplasm and the beating flagella serve the same function as a vehicle for the passage of the generative nucleus.
Since Strasburger’s cunning experiments on pollen tubes, the mechanisms of pollination and fertilization in higher plants have become one of the most fascinating fields in plant development and evolution (Lord and Russell 2002), including problems of self-incompatibility and programmed cell death (Thomas and Franklin-Tong 2004), polar cell growth (Hepler et al. 2001), chemotropism on the basis of cell-to-cell signaling (Okuda et al. 2009), and initiation of the endosperm as a nutritive tissue without double fertilization (Nowack et al. 2006). Phylogenetic approaches, as always considered by Strasburger very important, might dissect further these important problems of the cell biology of fertilization.
Erroneous ideas: what can we learn from Strasburger?
Among the staggering details in Strasburger’s elaborate publications, there are some remarkable erroneous ideas. In his first books, he was convinced that chromatin material existed as single thread. Later on (Strasburger 1884b), he spoke of a segmented nuclear thread, but after segregation and the formation of new daughter nuclei, these segments appeared to him again as a single thread. Another problem is cytoplasmic inheritance, which he flatly denied. Nevertheless, Strasburger never hesitated to change his mind or his interpretation when he found results diverging from his previously published data. This non-dogmatic behavior is documented by his three publications in 1875, 1876, and 1882, when he frankly mentioned errors of the earlier editions: “Bei Durchsicht meiner früheren Präparate sah ich mich vielfach veranlasst, dieselben umzuzeichnen, oder auch durch andere zu ersetzen, und dieses…führte mich dahin, drei meiner älteren Tafeln durch vier neuere, correctere zu ersetzen” (from the foreword to Strasburger 1876). His motto of research and teaching was always: Science is a constant flow and mistakes will disappear in the constant flow!
His behavior against his colleagues and students is absolutely admirable. When he studied cell division in different species, he wrote: “Schon aus Pietät fühlte ich mich veranlasst, den Theilungsvorgang bei Cladophora zu studieren, derjenigen Pflanze, an der die Zellhteilung überhaupt 1835 durch v. Mohl zum ersten Mal verfolgt worden war (Strasburger 1875, p. 85), a sentence which documents Strasburger’s high appreciation of his famous colleague von Mohl.
Strasburger was an excellent lecturer. Every Friday, he presented his fascination for his scientific work in a lecture to the public. In 1891, elected as Rector Magnificus of the University of Bonn, he dedicated his inauguration lecture entitled “Das Protoplasma und die Reizbarkeit” to the properties of the cytoplasm that are still in the center of plant cell biology research to day (see for instance Volkmann and Baluška 1999; Šamaj et al. 2006; Zonia 2010).
For his students, he was not just an excellent teacher but also often like a father discussing individual problems during his laboratory visit even or, in particular, at the weekend. Even at the fin de siècle, his team was of international composition, in particular by students from the USA. One of them, Charles J. Chamberlain (1912), documents Strasburger’s thinking by excerpt of a handwritten letter (Fig. 7).
Strasburger died on 19th May 1912. His tomb at the cemetery in Bonn-Poppelsdorf (Fig. 8) is still a frequently visited place by botanists and cell biologists from all over the world.
References
Ackers D, Hejnowicz Z, Sievers A (1994) Variation in velocity of cytoplasmic streaming and gravity effect in Characean internodal cells measured by laser-Doppler-velocimetry. Protoplasma 179:61–71
Alt W (1987) Mathematical models in actin–myosin interaction. In: Wohlfarth-Bottermann KE (ed) Nature and function of cytoskeletal proteins in motility and transport. Fortschritte der Zoologie 34, pp 219–230
Baker K, Hepler PK, Jackson WT (1968) Microtubules and early stages of cell-plate formation in the endosperm of Haemanthus. J Cell Biol 38:437–446
Baluška F, Salaj J, Mathur J, Braun M, Jasper F, Šamaj J, Chua N-H, Barlow PW, Volkmann D (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227:618–632
Baluška F, Volkmann D, Menzel D, Barlow P (2012) Strasburger’s legacy to mitosis and cytokinesis and its relevance for the cell theory. Protoplasma. doi:10.1007/s00709-012-0404-8
Bannigan A, Lizotte-Waniewski M, Riley M, Baskin TI (2008) Emerging molecular mechanisms that power and regulate the anastral mitotic spindle of flowering plants. Cell Motil Cytoskeleton 65:1–11
Baskin TI, Cande WZ (1990) The structure and function of the mitotic spindle in flowering plants. Annu Rev Plant Biol 41:277–315
Bresinsky A, Körner Ch, Kadereit JW, Neuhaus G, Sonnewald U (2008) Strasburger—Lehrbuch der Botanik. Begründet von E. Strasburger, Spektrum Akademischer Verlag, Heidelberg
Brown RC, Lemmon BE, Nguyen H (2003) Events during the first four rounds of mitosis establish three developmental domains in the syncytial endosperm of Arabidopsis thaliana. Protoplasma 222:167–174
Chamberlain ChJ (1912) Eduard Strasburger. Bot Gaz 54:68–72
Dhonukshe P, Baluška F, Schlicht M, Šamaj J, Friml J, Gadella TWJ Jr (2006) Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 10:137–150
Dhonukshe P, Šamaj J, Baluška F, Friml J (2007) A unifying new model of cytokinesis for the dividing plant and animal cells. BioEssays 29:371–381
Emons AMC, Ketelaar T (2009) Intracellular organization: a prerequisite for root hair elongation and cell wall deposition. Plant Cell Monogr 12:27–44
Fitting H (1937) Beitrage zur Physiologie der Protoplasmaströmung in den Blättern von Vallisneria spiralis. Ber deutsch Bot Ges 55:255–261
Grolig F, Pierson ES (2000) Cytoplasmic streaming: from flow to track. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 165–190
Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187
Holweg C, Nick P (2004) Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. PNAS 101:10488–10493
Jarosch R (1960) Die dynamik im Characeen protoplasma. Phyton 15:43–66
Kamiya N (1962) Protoplasmic streaming. Encyclop Plant Physiol 17–2:981–1035
King SM (2002) Dyneins motor on in plants. Traffic 3:930–931
Knoop V, Müller K (2009) Gene und Stammbäume. Ein Handbuch zur molekularen Phylogenetik. Spektrum Akademischer Verlag, Heidelberg
Kollmann R, Schumacher W (1964) Über die Feinstruktur des Phloems von Metasequoia glyptostroboides und seine jahreszeitlichen Veränderungen. V. Die Differenzierung der Siebzellen im Verlauf einer Vegetationsperiode. Planta 63:155–190
Lawrence CJ, Morris NR, MeagherRB DRK (2001) Dyneins have run their course in plant lineage. Traffic 2:362–363
Liebe S, Menzel D (1995) Actomyosin-based motility of endoplasmic reticulum and chloroplasts in Vallisneria mesophyll cells. Biol Cell 85:207–222
Liesche J, Martens HJ, Schulz A (2011) Symplasmic transport and phloem loading in gymnosperm leaves. Protoplasma 248:181–190
Lord EM (2005) Adhesion and guidance in compatible pollination. J Exp Bot 54:47–54
Lord EM, Russell SD (2002) The mechanisms of pollination and fertilization in plants. Annu Rev Cell Dev Biol 18:81–105
Lucas WJ, Ham B-K, Kim J-Y (2009) Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–500
Meagher RB, McKinney EC, Kandasamy MK (2000) The significance of diversity in the plant actin gene family. Studies in Arabidopsis. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 3–27
Mine I, Menzel D, Okuda K (2008) Morphogenesis in giant-celled algae. Int Rev Cell Mol Biol 266:37–83
Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, Schnittger A (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38:63–67
Okuda S, Tsutsui H, Shiin K, Sprunck S, Takeuchi K, Yui R et al (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–361
Otegui MS, Mastronarde DN, Kang BH, Bednarek SY, Staehelin LA (2001) Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13:2033–2051
Pickett-Heaps JD, Northcote DH (1966) Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristem. J Cell Sci 1:109–120
Pickett-Heaps JD, Gunning BE, Brown RC, Lemmon BE, Cleary AL (1999) The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell. Am J Bot 86:153–172
Pollack GH (2001) Cells, gels and the engines of life. A new unifying approach to cell function. Ebner and Sons, Seattle
Rasmussen CG, Humphries JA, Smith LG (2011) Determination of symmetric and asymmetric division planes in plant cells. Annu Rev Plant Biol 62:387–409
Reichardt I, Stierhof Y-D, Mayer U, Richter S, Schwarz H, Schumacher K, Jürgens G (2007) Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Current Biol 17:2047–2053
Reichelt S, Kendrick-Jones J (2000) Myosins. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 29–44
Ryu JH, Takagi S, Nagai R (1995) Stationary organization of the actin cytoskeleton in Vallisneria: the role of stable microfilaments at the end walls. J Cell Sci 108:1531–1539
Šamaj J, Read ND, Volkmann D, Menzel D, Baluška F (2005) The endocytic network in plants. Trends Cell Biol 15:425–433
Šamaj J, Müller J, Beck M, Böhm N, Menzel D (2006) Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. Trends Plant Sci 11:594–600
Sauter JJ, Dörr I, Kollmann R (1976) The ultrastructure of Strasburger cells (= albuminous cells) in the secondary phloem of Pinus nigra var. austriaca (Hoess) Badoux. Protoplasma 88:31–49
Sawitzky H, Grolig F (1995) Phragmoplast of the green alga Spirogyra is functionally distinct from the higher plant phragmoplast. J Cell Biol 130:1359–1371
Schlicht M, Šamajová O, Schachtschnabel D, Mancuso S, Menzel D, Boland W, Baluška F (2008) Dorenone blocks polarized tip-growth of root hairs by interfering with the PIN2-mediated auxin transport network in the root apex. Plant J 55:709–717
Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15:546–553
Shimmen T, Yokota E (2004) Cytoplasmic streaming in plants. Curr Opin Cell Biol 16:68–72
Sievers A, Buchen B, Volkmann D, Hejnowicz Z (1991) Role of the cytoskeleton in gravity perception. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic, London, pp 169–182
Sparks I (2011) Recent advances in understanding plant myosin function: life in the fast lane. Mol Plant 4:805–812
Strasburger E (1875) Über Zellbildung und Zelltheilung. Hermann Dabis, Jena
Strasburger E (1876) Über Zellbildung und Zelltheilung, zweite verbesserte und vermehrte Auflage nebst Untersuchungen über Befruchtung. Hermann Dabis, Jena
Strasburger E (1882) Über den Theilungsvorgang der Zellkerne und das Verhältniss der Kerntheilung zur Zelltheilung. Max Cohen & Sohn, Bonn
Strasburger E (1884a) Das Botanische Practicum. Anleitung zum Selbststudium der mikroskopischen Botanik für Anfänger und Fortgeschrittnere. Gustav Fischer, Jena
Strasburger E (1884b) Neue Untersuchungen über den Befruchtungsvorgang bei den Phanerogamen als Grundlage für eine Theorie der Zeugung. Gustav Fischer, Jena
Strasburger E (1891) Ueber den Bau und die Verrichtung der Leitungsbahnen in den Pflanzen. Gustav Fischer, Jena
Strasburger E (1904) Streifzüge an der Riviera, zweite gänzlich umgearbeitete Auflage mit 87 farbigen Abbildungen. Gustav Fischer, Jena
Strasburger E (1913) Pflanzliche Zellen-und Gewebelehre. In: Von Wettstein R (ed) Zellen-und Gewebelehre, Morphologie und Entwicklunggeschichte. B.G. Teubner, Leipzig, pp 1–174
Strasburger E, Noll F, Schenck H, Schimper AFW (1894) Lehrbuch der Botanik für Hochschulen. Gustav Fischer, Jena
Takagi S, Nagai R (1983) Regulation of cytoplasmic streaming in Vallisneria mesophyll cells. J Cell Sci 62:385–405
Thomas SG, Franklin-Tong VE (2004) Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429:305–309
Vale RD (2003) The molecular motor toolbox for intracellular transport. Cell 112:467–480
Van Bel AJE (1993) Strategies of phloem loading. Annu Rev Plant Physiol Plant Mol Biol 44:253–281
Verchot-Lubicz J, Goldstein RE (2010) Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma 240:99–107
Voigt B, Timmers AC, Šamaj J, Hlavacka A, Ueda T, Preuss M, Nielsen E, Mathur J, Emans N, Stenmark H, Nakano A, Baluška F, Menzel D (2005) Actin-based motility of endosomes is linked to the polar tip growth of root hairs. Eur J Cell Biol 84:609–621
Volkmann D, Baluška F (1999) Actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 47:135–154
Weiler E, Nover L (2008) Allgemeine und molekulare Botanik. Begründet von Wilhelm Nultsch. Georg Thieme, Stuttgart
Whaley WG, Mollenhauer HH (1963) The Golgi apparatus and cell plate formation—a postulate. J Cell Biol 17:216
Wickstead B, Gull K (2007) Dyneins across eukaryotes: a comparative genomic analysis. Traffic 7:1708–1721
Zonia L (2010) Spatial and temporal integration of signalling networks regulating pollen tube growth. J Exp Bot 61:1939–1957
Acknowledgment
This paper was presented as an invited lecture at the 5th Conference of the Polish Society of Experimental Plant Biology. It served as introduction to the session “E. Strasburger Day—Cellular Level” which was organized by Profs. Beata Zagórska-Marek (Wrocław University, Poland) and Przemysław Wojtaszek (Adam Mickiewicz University, Poznań, Poland).
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Volkmann, D., Baluška, F. & Menzel, D. Eduard Strasburger (1844–1912): founder of modern plant cell biology. Protoplasma 249, 1163–1172 (2012). https://doi.org/10.1007/s00709-012-0406-6
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DOI: https://doi.org/10.1007/s00709-012-0406-6