The role of genome and gene regulatory network canalization in the evolution of multi-trait polymorphisms and sympatric speciation

<p>Abstract</p> <p>Background</p> <p>Sexual reproduction has classically been considered as a barrier to the buildup of discrete phenotypic differentiation. This notion has been confirmed by models of sympatric speciation in which a fixed genetic architecture and a linear genotype phenotype mapping were assumed. In this paper we study the influence of a flexible genetic architecture and non-linear genotype phenotype map on differentiation under sexual reproduction.</p> <p>We use an individual based model in which organisms have a genome containing genes and transcription factor binding sites. Mutations involve single genes or binding sites or stretches of genome. The genome codes for a regulatory network that determines the gene expression pattern and hence the phenotype of the organism, resulting in a non-linear genotype phenotype map. The organisms compete in a multi-niche environment, imposing selection for phenotypic differentiation.</p> <p>Results</p> <p>We find as a generic outcome the evolution of discrete clusters of organisms adapted to different niches, despite random mating. Organisms from different clusters are distinct on the genotypic, the network and the phenotypic level. However, the genome and network differences are constrained to a subset of the genome locations, a process we call genotypic canalization. We demonstrate how this canalization leads to an increased robustness to recombination and increasing hybrid fitness. Finally, in case of assortative mating, we explain how this canalization increases the effectiveness of assortativeness.</p> <p>Conclusion</p> <p>We conclude that in case of a flexible genetic architecture and a non-linear genotype phenotype mapping, sexual reproduction does not constrain phenotypic differentiation, but instead constrains the genotypic differences underlying it. We hypothesize that, as genotypic canalization enables differentiation despite random mating and increases the effectiveness of assortative mating, sympatric speciation is more likely than is commonly suggested.</p

Undirected Sucrose Efflux Mitigation by the FT-Like SP6A Preferentially Enhances Tuber Resource Partitioning

The yield of harvestable plant organs depends on overall photosynthetic output and the subsequent distribution of the produced assimilates from source leaves across different sink organs. In this study, we aimed to obtain, using a two-sink transport model, mechanistic understanding of how the interplay between sink and pathway properties together determines sink resource partitioning. As a working example, we analyzed the partitioning of resources within potato plants, investigating the determinants of tuber sink yield. Our results indicated that, contrary to earlier studies, with a spatially explicit biophysically detailed model, transport pathway properties significantly affect sink resource partitioning within the physiologically relevant domain. Additionally, we uncovered that xylem flow, through its hydraulic coupling to the phloem, and sucrose efflux along the phloem, also significantly affected resource partitioning. For tubers, it is the cumulative disadvantage compared to sink leaves (distance, xylem flow, and sucrose efflux) that enable an undirected SP6A-mediated reduction of sucrose efflux to preferentially benefit tuber resource partitioning. Combined with the SP6A-mediated sink strength increase, undirected SP6A introduction significantly enhances tuber resource partitioning

Complementary roles for auxin and auxin signalling revealed by reverse engineering lateral root stable prebranch site formation

Priming is the process through which periodic elevations in auxin signalling prepattern future sites for lateral root formation, called prebranch sites. Thus far, the extent to which elevations in auxin concentration and/or auxin signalling are required for priming and prebranch site formation has remained a matter of debate. Recently, we discovered a reflux-and-growth mechanism for priming generating periodic elevations in auxin concentration that subsequently dissipate. Here, we reverse engineer a mechanism for prebranch site formation that translates these transient elevations into a persistent increase in auxin signalling, resolving the prior debate into a two-step process of auxin concentration-mediated initial signal and auxin signalling capacity-mediated memorization. A crucial aspect of the prebranch site formation mechanism is its activation in response to time-integrated rather than instantaneous auxin signalling. The proposed mechanism is demonstrated to be consistent with prebranch site auxin signalling dynamics, lateral inhibition, and symmetry-breaking mechanisms and perturbations in auxin homeostasis

What is quantitative plant biology?

Quantitative plant biology is an interdisciplinary field that builds on a long history of biomathematics and biophysics. Today, thanks to high spatiotemporal resolution tools and computational modelling, it sets a new standard in plant science. Acquired data, whether molecular, geometric or mechanical, are quantified, statistically assessed and integrated at multiple scales and across fields. They feed testable predictions that, in turn, guide further experimental tests. Quantitative features such as variability, noise, robustness, delays or feedback loops are included to account for the inner dynamics of plants and their interactions with the environment. Here, we present the main features of this ongoing revolution, through new questions around signalling networks, tissue topology, shape plasticity, biomechanics, bioenergetics, ecology and engineering. In the end, quantitative plant biology allows us to question and better understand our interactions with plants. In turn, this field opens the door to transdisciplinary projects with the society, notably through citizen science.Peer reviewe

Of mice and plants: Comparative developmental systems biology

Multicellular animals and plants represent independent evolutionary experiments with complex multicellular bodyplans. Differences in their life history, a mobile versus sessile lifestyle, and predominant embryonic versus postembryonic development, have led to the evolution of highly different body plans. However, also many intriguing parallels exist. Extension of the vertebrate body axis and its segmentation into somites bears striking resemblance to plant root growth and the concomittant prepatterning of lateral root competent sites. Likewise, plant shoot phyllotaxis displays similarities with vertebrate limb and digit patterning. Additionally, both plants and animals use complex signalling systems combining systemic and local signals to fine tune and coordinate organ growth across their body. Identification of these striking examples of convergent evolution provides support for the existence of general design principles: the idea that for particular patterning demands, evolution is likely to arrive at highly similar developmental patterning mechanisms. Furthermore, focussing on these parallels may aid in identifying core mechanistic principles, often obscured by the highly complex nature of multiscale patterning processes

What remains of the evidence for auxin feedback on PIN polarity patterns?

In light of recent findings, the feedback between auxin and PIN that plays a major role in models for self-organized auxin patterning requires revisiting

Joining forces: feedback and integration in plant development

Feedback and integration of information are of paramount importance for the robust functioning and dynamics of biological systems. In plant developmental biology, experimentation is increasingly combined with computational modeling to obtain a better understanding of how such regulatory interactions shape the systems’ behavior. Here we highlight experimental and modeling studies on feedback loops and integration mechanisms involved in plant development. These studies have substantially expanded our understanding of previously characterized gene regulatory networks (GRNs). In addition, they illustrate the pervasiveness of regulatory interactions between seemingly unrelated processes and levels of organization. Modelers in plant development will increasingly face the challenges of what level of detail, which processes and how many levels of organization to incorporate when trying to understand a particular process

Evolution of networks for body plan patterning; interplay of modularity, robustness and evolvability.

A major goal of evolutionary developmental biology (evo-devo) is to understand how multicellular body plans of increasing complexity have evolved, and how the corresponding developmental programs are genetically encoded. It has been repeatedly argued that key to the evolution of increased body plan complexity is the modularity of the underlying developmental gene regulatory networks (GRNs). This modularity is considered essential for network robustness and evolvability. In our opinion, these ideas, appealing as they may sound, have not been sufficiently tested. Here we use computer simulations to study the evolution of GRNs' underlying body plan patterning. We select for body plan segmentation and differentiation, as these are considered to be major innovations in metazoan evolution. To allow modular networks to evolve, we independently select for segmentation and differentiation. We study both the occurrence and relation of robustness, evolvability and modularity of evolved networks. Interestingly, we observed two distinct evolutionary strategies to evolve a segmented, differentiated body plan. In the first strategy, first segments and then differentiation domains evolve (SF strategy). In the second scenario segments and domains evolve simultaneously (SS strategy). We demonstrate that under indirect selection for robustness the SF strategy becomes dominant. In addition, as a byproduct of this larger robustness, the SF strategy is also more evolvable. Finally, using a combined functional and architectural approach, we determine network modularity. We find that while SS networks generate segments and domains in an integrated manner, SF networks use largely independent modules to produce segments and domains. Surprisingly, we find that widely used, purely architectural methods for determining network modularity completely fail to establish this higher modularity of SF networks. Finally, we observe that, as a free side effect of evolving segmentation and differentiation in combination, we obtained in-silico developmental mechanisms resembling mechanisms used in vertebrate development

Periodic lateral root priming : What makes it tick?

Conditioning small groups of root pericycle cells for future lateral root formation has a major impact on overall plant root architecture. This priming of lateral roots occurs rhythmically, involving temporal oscillations in auxin response in the root tip. During growth, this process generates a spatial pattern of prebranch sites, an early stage in lateral root formation characterized by a stably maintained high auxin response. To date, the molecular mechanism behind this rhythmicity has remained elusive. Some data implicate a cell-autonomous oscillation in gene expression, while others strongly support the importance of tissue-level modulations in auxin fluxes. Here, we summarize the experimental data on periodic lateral root priming. We present a theoretical framework that distinguishes between a priming signal and its subsequent memorization and show how major roles for auxin fluxes and gene expression naturally emerge from this framework. We then discuss three mechanisms that could potentially induce oscillations of auxin response: cell-autonomous oscillations, Turing-type patterning, and tissue-level oscillations in auxin fluxes, along with specific properties of lateral root priming that may be used to discern which type of mechanism is most likely to drive lateral root patterning. We conclude with suggestions for future experiments and modeling studies

Influence of diffuse fibrosis on wave propagation in human ventricular tissue

Aims: During ageing, after infarction, in cardiomyopathies and other cardiac diseases, the percentage of fibrotic (connective) tissue may increase from 6% up to 10-35%. The presence of increased amounts of connective tissue is strongly correlated with the occurrence of arrhythmias and sudden cardiac death. Methods and results: In this article, we investigate the role of diffuse fibrosis on wave propagation, arrhythmogenesis, and arrhythmia mechanism in human ventricular tissue using computer modelling. We show that diffuse fibrosis slows down wave propagation and increases tissue vulnerability to wave break and spiral wave formation. We also demonstrate that diffuse fibrosis increases the period of re-entrant arrhythmias and can suppress the restitution -induced transition from tachycardia to fibrillation. Conclusion: The latter suggests that mechanisms different from restitution-induced spiral break-up might be more likely to account for the onset of fibrillation in the presence of large amounts of diffuse fibrotic tissue