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Shape change is a fundamental process occurring in biological tissues during embryonic development and regeneration of tissues and organs. This process is regulated by cells that are constrained within a complex environment of biochemical and physical cues. The spatial constraint due to geometry has a determining role on tissue mechanics and the spatial distribution of force patterns that, in turn, influences the organization of the tissue structure. An understanding of the underlying principles of tissue organization may have wide consequences for the understanding of healing processes and the development of organs and, as such, is of fundamental interest for the tissue engineering community.
This thesis aims to further our understanding of how the collective behaviour of cells is influenced by the 3D geometry of the environment. Previous research studying the role of geometry on tissue growth has mainly focused either on flat surfaces or on substrates where at least one of the principal curvatures is zero. In the present work, tissue growth from MC3T3-E1 pre-osteoblasts was investigated on surfaces of controlled mean curvature.
One key aspect of this thesis was the development of substrates of controlled mean curvature and their visualization in 3D. It was demonstrated that substrates of controlled mean curvature suitable for cell culture can be fabricated using liquid polymers and surface tension effects.
Using these substrates, it was shown that the mean surface curvature has a strong impact on the rate of tissue growth and on the organization of the tissue structure. It was thereby not only demonstrated that the amount of tissue produced (i.e. growth rates) by the cells depends on the mean curvature of the substrate but also that the tissue surface behaves like a viscous fluid with an equilibrium shape governed by the Laplace-Young-law. It was observed that more tissue was formed on highly concave surfaces compared to flat or convex surfaces.
Motivated by these observations, an analytical model was developed, where the rate of tissue growth is a function of the mean curvature, which could successfully describe the growth kinetics. This model was also able to reproduce the growth kinetics of previous experiments where tissues have been cultured in straight-sided prismatic pores.
A second part of this thesis focuses on the tissue structure, which influences the mechanical properties of the mature bone tissue. Since the extracellular matrix is produced by the cells, the cell orientation has a strong impact on the direction of the tissue fibres. In addition, it was recently shown that some cell types exhibit collective alignment similar to liquid crystals.
Based on this observation, a computational model of self-propelled active particles was developed to explore in an abstract manner how the collective behaviour of cells is influenced by 3D curvature. It was demonstrated that the 3D curvature has a strong impact on the self-organization of active particles and gives, therefore, first insights into the principles of self-organization of cells on curved surfaces.
Rubisco catalyses the first step of CO2 assimilation into plant biomass. Despite its crucial role, it is notorious for its low catalytic rate and its tendency to fix O2 instead of CO2, giving rise to a toxic product that needs to be recycled in a process known as photorespiration. Since almost all our food supply relies on Rubisco, even small improvements in its specificity for CO2 could lead to an improvement of photosynthesis and ultimately, crop yield. In this work, we attempted to improve photosynthesis by decreasing photorespiration with an artificial CCM based on a fusion between Rubisco and a carbonic anhydrase (CA).
A preliminary set of plants contained fusions between one of two CAs, bCA1 and CAH3, and the N- or C-terminus of RbcL connected by a small flexible linker of 5 amino acids. Subsequently, further fusion proteins were created between RbcL C-terminus and bCA1/CAH3 with linkers of 14, 23, 32, and 41 amino acids. The transplastomic tobacco plants carrying fusions with bCA1 were able to grow autotrophically even with the shortest linkers, albeit at a low rate, and accumulated very low levels of the fusion protein. On the other hand, plants carrying fusions with CAH3 were autotrophic only with the longer linkers. The longest linker permitted nearly wild-type like growth of the plants carrying fusions with CAH3 and increased the levels of fusion protein, but also of smaller degradation products.
The fusion of catalytically inactive CAs to RbcL did not cause a different phenotype from the fusions with catalytically active CAs, suggesting that the selected CAs were not active in the fusion with RbcL or their activity did not have an effect on CO2 assimilation. However, fusions to RbcL did not abolish RbcL catalytic activity, as shown by the autotrophic growth, gas exchange and in vitro activity measurements. Furthermore, Rubisco carboxylation rate and specificity for CO2 was not altered in some of the fusion proteins, suggesting that despite the defect in RbcL folding or assembly caused by the fusions, the addition of 60-150 amino acids to RbcL does not affect its catalytic properties. On the contrary, most growth defects of the plants carrying RbcL-CA fusions are related to their reduced Rubisco content, likely caused by impaired RbcL folding or assembly. Finally, we found that fusions with RbcL C-terminus were better tolerated than with the N-terminus, and increasing the length of the linker relieved the growth impairment imposed by the fusion to RbcL. Together, the results of this work constitute considerable relevant findings for future Rubisco engineering.
Calcium carbonate formation
(2017)
Chloroplast membranes have a unique composition characterized by very high contents of the galactolipids, MGDG and DGDG. Many studies on constitutive, galactolipid-deficient mutants revealed conflicting results about potential functions of galactolipids in photosynthetic membranes. Likely, this was caused by pleiotropic effects such as starvation artefacts because of impaired photosynthesis from early developmental stages of the plants onward. Therefore, an ethanol inducible RNAi-approach has been taken to suppress two key enzymes of galactolipid biosynthesis in the chloroplast, MGD1 and DGD1. Plants were allowed to develop fully functional source leaves prior to induction, which then could support plant growth. Then, after the ethanol induction, both young and mature leaves were investigated over time.
Our studies revealed similar changes in both MGDG- and DGDG-deficient lines, however young and mature leaves of transgenic lines showed a different response to galactolipid deficiency. While no changes of photosynthetic parameters and minor changes in lipid content were observed in mature leaves of transgenic lines, strong reductions in total chlorophyll content and in the accumulation of all photosynthetic complexes and significant changes in contents of various lipid groups occurred in young leaves. Microscopy studies revealed an appearance of lipid droplets in the cytosol of young leaves in all transgenic lines which correlates with significantly higher levels of TAGs. Since in young leaves the production of membrane lipids is lowered, the excess of fatty acids is used for storage lipids production, resulting in the accumulation of TAGs.
Our data indicate that both investigated galactolipids serve as structural lipids since changes in photosynthetic parameters were mainly the result of reduced amounts of all photosynthetic constituents. In response to restricted galactolipid synthesis, thylakoid biogenesis is precisely readjusted to keep the proper stoichiometry and functionality of the photosynthetic apparatus. Ultimately, the data revealed that downregulation of one galactolipid triggers changes not only in chloroplasts but also in the nucleus as shown by downregulation of nuclear encoded subunits of the photosynthetic complexes.
Conformational transition of peptide-functionalized cryogels enabling shape-memory capability
(2017)
Plant cells host two important organelles: mitochondria, known as the cell’s ‘powerhouse’, which act by converting oxygen and nutrients into ATP, and plastids, which perform photosynthesis. These organelles contain their own genomes that encode proteins required for gene expression and energy metabolism. Transformation technologies offer great potential for investigating all aspects of the physiology and gene expression of these organelles in vivo. In addition, organelle transformation can be a valuable tool for biotechnology and molecular plant breeding. Plastid transformation systems are well-developed for a few higher plants, however, mitochondrial transformation has so far only been reported for Saccharomyces cerevisiae and the unicellular alga Chlamydomonas reinhardtii.
Development of an efficient new selection marker for plastid transformation is important for several reasons, including facilitating supertransformation of the plastid genome for metabolic engineering purposes and for producing multiple knock-outs or site-directed mutagenesis of two unlinked genes. In this work, we developed a novel selection system for Nicotiana tabacum (tobacco) chloroplast transformation with an alternative marker. The marker gene, aac(6′)-Ie/aph(2′′)-Ia, was cloned into different plastid transformation vectors and several candidate aminoglycoside antibiotics were investigated as selection agents. Generally, the efficiency of selection and the transformation efficiency with aac(6′)-Ie/aph(2′′)-Ia as selectable marker in combination with the aminoglycoside antibiotic tobramycin was similarly high as that with the standard marker gene aadA and spectinomycin selection. Furthermore, our new selection system may be useful for the development of plastid transformation for new species, including cereals, the world’s most important food crops, and could also be helpful for the establishment of a selection system for mitochondrial transformation.
To date, all attempts to achieve mitochondrial transformation for higher plants have been unsuccessful. A mitochondrial transformation system for higher plants would not only provide a potential for studying mitochondrial physiology but could also provide a method to introduce cytoplasmic male sterility into crops to produce hybrid seeds. Establishing a stable mitochondrial transformation system in higher plants requires several steps including delivery of foreign DNA, stable integration of the foreign sequences into the mitochondrial genome, efficient expression of the transgene, a highly regenerable tissue culture system that allows regeneration of the transformed cells into plants, and finally, a suitable selection system to identify cells with transformed mitochondrial genomes. Among all these requirements, finding a good selection is perhaps the most important obstacle towards the development of a mitochondrial transformation system for higher plants. In this work, two selection systems were tested for mitochondrial transformation: kanamycin as a selection system in combination with the antibiotic-inactivating marker gene nptII, and sulfadiazine as a selection agent that inhibits the folic acid biosynthesis pathway residing in plant mitochondria in combination with the sul gene encoding an enzyme that is insensitive to inhibition by sulfadiazine. Nuclear transformation experiments were considered as proof of the specificity of the sulfadiazine selection system for mitochondria. We showed that an optimized sulfadiazine selection system, with the Sul protein targeted to mitochondria, is much more efficient than the previous sulfadiazine selection system, in which the Sul protein was targeted to the chloroplast. We also showed by systematic experiments that the efficiency of selection and nuclear transformation of the optimized sulfadiazine selection was higher compared to the standard kanamycin selection system. Finally, we also investigated the suitability of this selection system for nuclear transformation of the model alga Chlamydomonas reinhardtii, obtaining promising results. Although we designed several mitochondrial transformation vectors with different expression elements and integration sites in the mitochondrial genome based on the sulfadiazine system, and different tissue culture condition were also considered, we were not able to obtain mitochondrial transformation with this system. Nonetheless, establishing the sul gene as an efficient and specific selection marker for mitochondria addresses one of the major bottlenecks and may pave the way to achieve mitochondrial transformation in higher plants.