Gravity: one of the driving forces for evolution

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1 Protoplasma (2006) 229: DOI /s PROTOPLASMA Printed in Austria Gravity: one of the driving forces for evolution D. Volkmann* and F. Baluška Institut für Zelluläre und Molekulare Botanik, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn Received July 15, 2005; accepted August 29, 2005; published online December 16, 2006 Springer-Verlag 2006 Summary. Mechanical load is 10 3 larger for land-living than for waterliving organisms. As a consequence, antigravitational material in form of compound materials like lignified cell walls in plants and mineralised bones in animals occurs in land-living organisms preferentially. Besides cellulose, pectic substances of plant cell walls seem to function as antigravitational material in early phases of plant evolution and development. A testable hypothesis including vesicular recycling processes into the tensegrity concept is proposed for both sensing of gravitational force and responding by production of antigravitational material at the cellular level. Keywords: Gravity; Evolution; Antigravitational material; Extracellular matrix; Cell wall; Tensegrity; Vesicular recycling. Introduction Life on Earth in its present diversity and complexity has developed under constantly changing environmental conditions. The gravitational force, however, is one of the most constant factors guiding and affecting the evolution of all organisms. Nevertheless, there is a small variation related to the position of organisms on the Earth s radius and also some mass-related variation in the gravitational impact exerted on organisms living in different media, such as water, soil, and air. Schematically, evolution can be described as a process occurring in a four-dimensional space, where the genotype and phenotype of organisms are the result of a complex network of environment, mutation, and selection. One of the most striking examples for this interconnected network is the change from the original nitric atmosphere of the early Earth into a partially oxygenic atmosphere by oxygen-producing cyanobacteria, which created totally * Correspondence and reprints: Institut für Zelluläre und Molekulare Botanik, Rheinische Friedrich-Wilhelms-Universität Bonn, Kirschallee 1, Bonn, Germany. unb110@uni-bonn.de new environmental conditions suitable for the subsequent evolution of more complex oxygen-consuming organisms. Environmental conditions provided by water versus land and consequences for organismal diversity The homogeneity of water versus the heterogeneity of land and air is related to temperature, the distribution of particles (mainly nutrients), radiation, and mechanical load. For each of these four parameters, the difference is moderate for the water habitat, whereas it is extreme for land and air. Thus, in order to occupy and survive on land, organisms had to solve severe problems related to temperature regulation, nutrient uptake, radiation protection, and resistance to mechanical load. In spite of the more or less constant gravitational force on Earth, mechanical load on organisms is approximately 1000 times larger on land than in water, due to large differences in density ( ). Increasing heterogeneity of the habitat conditions described above is strongly correlated with biodiversity. Just 5% of estimated plant species live in the water habitat salt as well as fresh water, whereas 95% evolved on land. Mechanical load resulting in antigravitational material might be, among others, an important factor in the evolutionary explosion of organisms into the new and extremely heterogeneous biotope land. Antigravitational strategies of multicellular land organisms Land plants have developed two basic strategies to withstand the extreme mechanical load acting on their bodies. The first is the balance between the internal force exerted by osmotically effective particles like small molecules or

2 144 D. Volkmann and F. Baluška: Gravity and evolution ions and the external force exerted by the cell wall, in more general terms the extracellular matrix. This balance between internal and external forces is already obvious in early land plants mainly mosses which form a relatively homogeneous group of plants in terms of their morphology and anatomy. The second strategy is based on a process analogous to the mineralisation of animal bones. In plants, this is based on the structural modification of the extracellular matrix by lignification which was first realized in more recent lower plants, such as clubmosses, horsetails, and pteridophytes, and finally evolved to highest effectiveness in gymnosperm and angiosperm trees, and grasses (Lewis 1999). It is therefore not surprising that plant biologists speak of the lignified plant backbone. In cereals, for example, the lignified antigravitational material is extremely effective insofar as the ratio of the diameter to the height of stalks is much smaller than that of the most admirable technical buildings in the world (Volkmann 2001: fig. 2). Lignification of cell walls under mechanical load occurs mainly at the periphery of the plant body. Moreover, in conducting tissue, lignification is common either at vascular thickenings or in cells surrounding vessels (Volkmann and Sievers 1992: fig. 3). Investigations of fossil land plants, like for instance Rhynia sp., indicate that the earliest vascular tissues were probably unlignified (Boyce et al. 2003). This would imply two distinct evolutionary steps towards lignification, a first under mechanical load on the plant body and a second under hydrostatic pressure in the conducting tissue. An impressive example of how mechanical load may change the morphology of organisms is available in snakes. These include water-living species and land-living species moving in a horizontal direction on the ground, as well as climbing species moving in a vertical direction on trees. Clear differences are obvious in skin, connecting tissues such as muscles, the bone skeleton, the position of the heart, blood vessels, and circulation (Lillywhite 1988). The evolution of the bone skeleton in animals, and finally its hardening by the process of mineralisation, was certainly one of the main factors allowing the survival of organisms and their increasing diversification on land (Kirsch and Gunga 2001: fig. 2). Antigravitational strategy in land plants Cell walls: pectins and hemicelluloses for cell wall dynamicity The extracellular matrix of most land plants, the cell wall (Carpita et al. 2001), is a complex compound material composed of cellulose, the most abundant natural product, hemicelluloses, pectins, and proteins. Pectins consisting of a range of different compounds are also responsible for proper hydration of cell walls and, thereby, supporting the balance between external and internal forces in land plants. Nevertheless, recent studies have revealed that pectins cross-linked with calcium and boron, as well as covalently cross-linked with xyloglucans, also have very important load-bearing structural functions (Ryden et al. 2003, Popper and Fry 2005). Importantly, the pectic-hemicellulosic component can fully replace the cellulosic network in cell walls (Schedletzky et al. 1990, Diaz-Cacho et al. 1999, Sabba et al. 1999, Encina et al. 2002). These cellulose-depleted and pectin-enriched cell walls also have elevated levels of structural proteins (Sabba et al. 1999, Manfield et al. 2004). On the other hand, pectin-devoid cell walls have not yet been described. All this suggests that the pectin network is the most ancient one and this was reinforced firstly by the cellulosic network and later also by lignins. Moreover, one can assume that the pectin networks were originally more flexible, becoming progressively crosslinked with increasing exposure to mechanical load. There are two major cross-linking agents calcium and boron. In contrast to cellulose and lignin, pectins and xyloglucans are internalised from cell walls back into the cytoplasm in meristematic and early postmitotic cells (Baluška et al. 2002). As they colocalize with recycling proteins (Šamaj et al. 2004), they are most likely also recycled back to cell walls via secretory endosomes (Baluška et al. 2002, Šamaj et al. 2005). This dynamicity of plant cell walls resembles the degradation of bones via endocytosis, as well as the internalisation of hyaluronan from the extracellular matrix of animal cells (Tammi et al. 2001). Plant cells can clearly fine-tune the mechanical properties of their cell walls, not only via secretory processes and enzymatic activities within cell walls but also via selective internalisation of pectins and xyloglucans. In addition to their role in coping with the mechanical stress associated with repositioning of plant organs under the influence of the gravity vector, these activities are also involved in processes such as stomata movements, pathogen response, and cell plate formation (Baluška et al. 2005a, b; Šamaj et al. 2005). Cell walls are initiated during plant cytokinesis when a primordial cell wall, known as the cell plate, is laid down. This is composed of ancient cell wall molecules such as recycling pectins and xyloglucans which are targeted to the cell plate via endosomes (Baluška et al. 2005a, b; Šamaj et al. 2005). Callose accumulates later, while cellulose synthesis starts only after the cell plate has docked at

3 D. Volkmann and F. Baluška: Gravity and evolution 145 the parent cell wall (Samuels et al. 1995). Intriguingly, this ontogenetic sequence of events fits nicely into the above-mentioned phylogenetic sequence when antigravitational substances became progressively stronger in their ability to resist the mechanical load placed on plant cells. Besides cell wall ontogenesis, this sequential increase of mechanically more robust antigravitational molecules is also obvious in plant organs where pectins and xyloglucan dominate in cells at their apices, while cellulose and lignins are formed in large amounts only in cells located more basally. Cell walls: cellulose-lignin composite for cell wall strength The most mechanically relevant cell wall components are cellulose and lignins, which both appeared in the later stages of evolution and arise later in plant development. As polymerisation products of phenylpropanes, lignins are the second most abundant natural products, forming robust supramacromolecular networks spreading throughout the whole plant body. The cellulose-xyloglucan-pectinlignin composite that is formed has extremely robust mechanical properties. Depending on the relative amounts of cellulose and lignins, this cell wall composite has the characteristics of extremely elastic glass fibres or noncompressible ferroconcrete, where cellulose fibres play a role analogous to iron acting against tension and the lignin networks react to compression like concrete. It is, Fig. 1. Compression wood in Pinus sp. after an accident. Photograph provided by Dr. Ulrike Friedrich (DLR, Köln/Bonn, Germany) therefore, not surprising that lignification always occurs at sites of highest mechanical load. In this respect, one of the most common phenomena is that of tension versus compression wood (Hejnowicz 1997). As is well known from situations such as those depicted in Fig. 1 for stems and twigs of trees under mechanical load, the composition of the cellulose-lignin complex differs in tissues under tension or compression, as well as in those under microgravity conditions (Hoson et al. 2003). The molecular basis of lignins was described in 1874 by Tiemann and Haarmann (1874). Nevertheless, the mechanism of lignification at the molecular and cellular level is far from completely understood, in spite of its extreme abundance and economical importance (Lewis 1999). Antigravitational strategy in animals: collagen-hydroxylapatite composite for dynamicity and strength of bones Like the plant cell wall, bones are also extremely dynamic structures which can be degraded and remodelled via endocytic processes (Vico et al. 1998). Osteoclasts are the major players, docking at bones and resorbing the bone matrix via endocytosis (Martin and Sims 2005). This process of bone resorption bears similarities to synaptic processes (Bhangu 2003, Spencer and Genever 2003). Intriguingly, endocytic internalization and recycling of cell wall pectins and xyloglucans is also accomplished at plant synapses in root apices (Baluška et al. 2005b). In addition to endosomal bone resorption by osteoclasts, other components of the animal extracellular matrix are also known to be internalised via endocytosis, e.g., hyaluronan and collagen (Tammi et al. 2001, Arora et al. 2005). In fact, there are other remote similarities between hyaluronan and pectins, for instance, their degradation fragments are known to have signalling roles. There are several analogies between the extracellular matrices of land-living plants and animals concerning their composition, their mechanical characteristics, and probably also their formation. The main component of bones is collagen, which is the most abundant protein in animals. Interestingly, collagen-like proteins have also been detected in plant cell walls (Ringli et al. 2001), and plant cell walls are also sensitive to collagenase treatments (Wojtaszek et al. 2005). Importantly, collagen is rich in proline, as are plant cell wall proteins (Showalter 1993, Cassab 1998). Further structural components of animal extracellular matrices are carbohydrates, such as hyaluronic acid, keratan sulfate, and chondroitin sulfate. The most important constituents, however, are the inorganic materials that act as a basis for bone mineralisation, i.e., hydroxylapatite (a complex of calcium

4 146 D. Volkmann and F. Baluška: Gravity and evolution Fig. 2. A Xyloglucans are abundant at the cross-walls (plant synapses) in the transition zone of the maize root apex. B Internalized xyloglucans accumulate within BFA-induced compartments after 2 h exposure to BFA, while almost no signal is visible at the cross-walls phosphate), calcium carbonate, and calcium silicate. Again, depending on the relative amounts of collagen and hydroxylapatite, the mechanical characteristics of the composite are analogous either to elastic glass fibres or to noncompressible ferroconcrete. In bones, the proteinaceous collagen fibres act against tension, whereas mineralisation by inorganic material prevents compression. As in plant lignification, mineralisation occurs mainly at sites of high mechanical load. The density of bones, based mainly on the level of mineral deposits (mineralisation), correlates positively with the mechanical load. Formation and maintenance of antigravitational material: Ingber s tensegrity concept and recycling processes driven by cytoskeletal proteins On the basis of the many analogies found in plants and animals concerning antigravitational material, it is reasonable to seek possible common mechanisms that might have evolved under the constant influence of gravitational force, in particular after leaving water and colonizing land. There are two concepts available which, when combined, might serve as a basis for an attractive and testable working hypothesis. In the 90s, Donald Ingber (1997, 2003) developed a theory of cellular mechanochemistry for cell cultures and animal cells which he called the tensegrity concept. The main components of his concept are adhesion domains composed of integral membrane proteins, i.e., integrins, located in the plasma membrane, associated proteins at the peripheral cytoplasm and interconnected cytoskeletal proteins extending into the cell interior, such as microtubules, intermediate and actin filaments, and the motor proteins kinesin and myosin. Changes in tension and/or compression at the plasma membrane domains induced by external forces like gravity or other mechanical forces may unbalance the tensegrity forces of the cell and trigger mechanotransduction chains via the FAK (focal adhesion kinase) ERK (extracellular signal regulated protein kinase) or the AC (adenylate cyclase) PKA (protein kinase A) pathways (Ingber 2003: figs. 1 and 3). Another idea associated with gravity-related growth in plants comes from recent work of plant cell biology. Geldner et al. (2001) showed the internalisation of transmembrane proteins like plasma membrane H -ATPase and proteins of the PIN family in Arabidopsis thaliana roots after unbalancing exocytotic and endocytotic events by application of brefeldin A (BFA). Using the same experimental approach for Zea mays roots, Baluška et al. (2002) demonstrated that, besides plasma membrane H - ATPase, cell wall components like unesterified rhamnogalacturonans are also internalised a few minutes after BFA treatment. In addition, a large number of molecules are known to undergo recycling processes at the plasma membrane, including several pectins (Figs. 2 and 3). This process depends on the actomyosin system (Šamaj et al. 2004) and might be involved in the exchange of information via hormones or transmitter substances through vesicular trafficking corresponding to events at synapses (Baluška et al. 2003). During long-term experiments investigating potato tuber formation under microgravity conditions, Cook Fig. 3. Scheme for endocytosis of pectins. Recycling of several pectin epitopes (2F4, 6D7, RGII. JIM5, LM5) and xyloglucans (XG) between the cell wall plasma membrane (CW/PM) and endosomes that aggregate into BFA-induced compartments in BFA-exposed root cells

5 D. Volkmann and F. Baluška: Gravity and evolution 147 and Croxdale (2003) did not find any effects on pectins and cell wall ultrastructure. On the other hand, short-term experiments under microgravity (Lisboa et al. 2002) have indicated that endocytosis might be altered in tobacco pollen tubes during tip growth, with the main changes occurring in the secretion of pectins. Thus, the balance between exocytotic versus endocytotic events might be important for developmental processes like cytokinesis (Baluška et al. 2005b, Dhonukshe et al. 2006), cell and organ polarity in relation to gravity (Baluška et al. 2005a), and morphogenesis (Šamaj et al. 2006). Working hypothesis and questions for the future Combining Ingber s tensegrity concept and actomyosindriven recycling processes, the following attractive and testable working hypothesis (Fig. 4) might be proposed: Mechanical load is perceived at the plasma membrane via mechanosensitive transmembrane complexes in cooperation with associated proteins, in particular, cytoskeletal elements. Changes in mechanical load disturb the balance of exocytotic versus endocytotic processes and thereby trigger changes in the flux of information-bearing molecules. These then instruct the assembly of antigravitational molecules and polymers. From this working hypothesis the following questions arise. Which molecules underlie recycling processes? Which are the information-bearing molecules? Are different mechanisms realized, e.g., for short-term graviresponses like gravitaxis and gravitropism in plants, and orientation of man in space? And the most general and important one: Are plasma membrane areas sensitive to tension and compression? Fig. 4. Working hypothesis for the interrelationship between gravity, intracellular factors like the cytoskeleton and plasma membrane, and the evolution of antigravitational material in organisms Unsolved by this approach, however, is the gravi-paradox that many of the organisms investigated so far are able to perceive gravitational forces in the range of 10 3 g in spite of the Earth s acceleration of 1 g (981 cm/s 2 ) acting constantly over millions of years. Could the density difference between water and air,, be important, which is just in the range of 10 3? Acknowledgments Our research is financially supported by the Deutsches Zentrum für Luftund Raumfahrt (DLR Köln/Bonn, Germany, Projects 50 WB 9995 and 50 WB 0434) and the European Space Agency (ESA/ESTEC, MAP Project AO ). F.B. receives partial support from the Slovak Academy of Sciences, Grant Agency VEGA (grant nr. 2/5085/25), Bratislava, Slovakia. Y. Sone (University of Osaka, Japan) kindly provided us with the anti-xg antibody. We thank A. Hlavacka for help with the figures. References Arora PD, Chan MWC, Anderson RA, Janmey PA, McCulloch CA (2005) Separate functions of gelsolin mediate sequential steps of collagen phagocytosis. Mol Biol Cell 16: Baluška F, Hlavacka A, Šamaj J, Palme K, Robinson DG, Matoh T, Mc- Curdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells: insights from brefeldin A-induced compartments. Plant Physiol 130: Baluška F, Šamaj J, Menzel D (2003) Polar transport of auxin: carriermediated flux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol 13: Baluška F, Volkmann D, Menzel D (2005a) Plant synapses: actin-based adhesion domains for cell-to-cell communication. Trends Plant Sci 10: Baluška F, Liners F, Hlavačka A, Schlicht M, Van Cutsem P, McCurdy D, Menzel D (2005b) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225: Bhangu PS (2003) Pre-synaptic vesicular glutamate release mechanisms in osteoblasts. J Musculoskelet Neuronal Interact 3: Boyce CK, Cody GD, Fogel ML, Hazen RM, Alexander CMO D, Knoll AH (2003) Chemical evidence for cell wall lignification and the evolution of tracheids in Early Devonian plants. Int J Plant Sci 164: Carpita NC, Tierney M, Campbell M (2001) Molecular biology of the plant cell wall: searching for the genes that define structure, architecture, and dynamics. Plant Mol Biol 47: 1 5 Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 49: Cook ME, Croxdale JG (2003) Ultrastructure of potato tubers formed in microgravity under controlled environmental conditions. J Exp Bot 54: Dhonukshe P, Baluška F, Hlavacka A, Schlicht M, Šamaj J, Friml J, Gadella TWJ Jr (2006) Endocytosed cell surface material is used for cell plate formation during plant cytokinesis. Dev Cell 10: Diaz-Cacho P, Moral R, Encina A, Acebes JL, Alvarez J (1999) Cell wall modification in bean (Phaseolus vulgaris) callus cultures tolerant to isoxaben. Physiol Plant 107: Encina A, Sevillano JM, Acebes JL, Alvarez J (2002) Cell wall modifications of bean (Phaseolus vulgaris) cell suspensions during habituation and dehabituation to dichlobenil. Physiol Plant 114:

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