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Developmental programming is a major source of inter-individual variation that can tailor phenotypes to environmental conditions, including thermal conditions. While the underlying mechanisms of developmental plasticity are mostly unknown, there is growing evidence for the involvement of mitochondria in this process. Here, we investigate whether prenatal sound – increasingly recognised as an essential source of information for embryos – can program mitochondrial metabolism. In the arid-adapted zebra finch, prenatal exposure to “heat-calls”, produced by parents incubating at high temperatures, adaptively alters nestling growth in the heat. To test whether mitochondrial programming underlies this adaptive pattern, we measured red blood cell mitochondrial function in nestlings, exposed prenatally to either heat-calls or control-calls, and reared in contrasting thermal environments post-hatch. Exposure to high temperatures always reduced mitochondrial ATP production efficiency. However, as expected to reduce heat production and improve growth, prenatal exposure to heat-calls improved mitochondrial efficiency under mild heat conditions. By contrast, when exposed to an acute heat-challenge, LEAK respiration was higher in heat-call nestlings. Consistent with its role in reducing oxidative damage, LEAK under extreme heat was also higher in fast growing nestlings. These changes in mitochondrial function are consistent with the differential growth pattern induced by prenatal heat-calls. Our study therefore provides the first demonstration of mitochondrial acoustic sensitivity, and brings us closer to understanding the underpinning of acoustic developmental programming and avian strategies for heat adaptation.

SEB Annual Conference 2022

Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird

Discover the art of creating extraordinary science at SEB’s Annual Conference at Le Corum Conference Center     in Montpellier, France from 5 to  8 July 2022.

SEB’s Annual Conference is celebrated for creating the perfect composition of research, new discoveries and collaborative connections. Be creative and innovative by exchanging ideas and knowledge with masters of biology from all over the world.

2022 will find over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years.
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Please register for the conference by clicking on this link:

https://www.sebiology.org/events/seb-annual-conference-2022/registration.html

The site will be open for registered participants closer to the event.

2022 will find over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years - Montpellier, France

technical paper

While hypoxia (i.e. low dissolved oxygen level in water) events occur naturally, global change and human activities have exacerbated their strength and temporal fluctuations. As populations may not be able to escape the hypoxic conditions, especially in freshwater ponds, it is crucial to understand how organisms can adjust and adapt to these fluctuating environments. When directly exposed, individuals may be able to adjust their phenotypes through plasticity, but continued exposure to hypoxia over generations may require adaptation and evolution. As the mitochondrial metabolism is the key component that fuel aerobic functions, the individual capacity to respond to the environmental change in oxygen availability is likely to rely on mitochondrial functions. Using two populations of wild three-spined sticklebacks (Gasterosteus aculeatus) exposed to different levels of hypoxia conditions in their natural habitats and experimentally exposed to fluctuating hypoxia (20% air saturation during the night and 100% during the day), we investigated the fish metabolic plastic and evolutionary response.  We showed adaptation in fish growth and metabolic rate, fish exposed to hypoxia in their natural habitats possessing higher metabolic capacity, but limited evidence for plasticity to the experimental conditions. These responses were supported by the muscle mitochondrial metabolism, for which similar adaptation were observed. However, no differences were observed in the brain mitochondrial metabolism, suggesting tissue specific response to environmental changes. Overall, these results highlight the capacity of fish to adapt environmental changes across generations, relying on mitochondrial adaptation.

Fish metabolic response to freshwater hypoxia: plasticity and adaptation

Antarctic fish of the suborder Notothenioidei display remarkable metabolic adaptations to life in the Southern Ocean. These comprise very low, energy saving metabolic rates, higher mitochondrial densities, cold adapted enzymes, anti-freeze proteins and last but not least, the loss of hemoglobin in the icefishes (family Channichthyidae). Yet, those adaptations come at a premium and render Antarctic notothenioids especially vulnerable to a warming ocean. As the central players in aerobic energy metabolism, mitochondria and their acclimatory plasticity play an important role in buffering the effects of climate change and much depends on their thermal stability and acclimatory capacity. 
I will present an overview of recent studies on notothenioid mitochondrial and whole animal respiration under acute and chronic thermal exposure and explore the differences in thermal reaction norms, leak rates and thermal stability of the individual respiratory complexes in Antarctic nototheniids (N. rossii, N. coriiceps), trematomids (T. eulepidotus, T. loennbergii) and the haemoglobin-less channichthyids (C. hamatus, C. wilsoni).




Acclimation capacity and thermal sensitivity of notothenioid energy metabolism

Seedling de-etiolation involves massive change in genome expression, many light-responsive genes undergoing pioneering rounds of transcription within minutes. In previous studies we reported that Arabidopsis photomorphogenesis indeed associates with a ~3-fold increase of global RNA Polymerase II elongation activity in most cotyledon nuclei (1), which, together with more recent studies (2), suggests that light induces a switch from a relatively quiescent to a more active transcriptional status during the transition. Studies from others and us focusing on nuclear and chromatin dynamics also unveiled that de-etiolation involves genome-wide variations nuclear architecture and in chromatin hallmarks of transcription elongation status at thousands' protein-coding genes (1, 3-4), which are controlled by DET1 and other light signaling components (3). Yet, because of data normalization practices, the functional consequences of these multilevel adaptations of the chromatin status to an elevated transcriptional regime are not observed when analyzing transcriptomic profiles obtained with classical microarray or RNA-seq analyses. We therefore developed a new methodological setup enabling an absolute quantification of RNA-seq data to explore the functional impact of transcription intensification on gene expression. We will present how this approach can be used to assess to which extent, and for which genes, a global increase of RNA Pol 2 activity is reflected at the transcript level during photomorphogenesis. This new standpoint should help revisiting how signaling paths and chromatin machineries modulate plant genome expression in response to the environment.

References:
1- Bourbousse et al, PNAS (2015) 112(21) e2836-44
2- Godoy Herz, et al. Mol Cell (2019) PMID: 30661982
3- Nassrallah, Rougee et al, eLife (2018) e37892
4- Charron et al, Plant Cell (2009) 21:3732-48

Global increase of the nuclear transcriptional regime during Arabidopsis photomorphogenesis: a chromatin perspective

The basket of nuclear pore complex (NPC) is an assembly of flexible protein filaments and acts as a dynamic scaffold at the nucleoplasmic side that regulates various essential cellular processes, including nuclear transport, RNA processing, chromatin organization, and gene expression. However, the mechanisms behind the regulation are still poorly understood, especially in plants. Here, we identified a guanylate-binding protein (GBP)-like GTPase (GBPL3) as a specific component of the NPC basket in Arabidopsis. GBPL3 is located at the nuclear rim and confers robust physical and genetic interactions with various NPC and nucleoskeleton constituents. Proximity labeling proteomics experiment suggests that GBPL3 is predominantly distributed at the NPC basket and that it is intimately associated with chromatin remodelers, transcription regulators, and RNA processing machinery. Importantly, we found that GBPL3 promotes the formation of biomolecular condensates at the NPC basket, which is capable of recruiting its interactors. Loss of GBPL3 led to severely stunted plant growth, aberrant transcription of abiotic and biotic stress-related genes, and retention of total mRNA in the nucleus. These results suggest that GBPL3 is a plant-specific NPC basket component and can recruit transcription and RNA processing machinery through condensate formation to modulate gene expression and subsequent RNA processing, which is required for plant growth and stress responses.

GBPL3 is a novel plant nucleoporin that recruits RNA processing and transcription machinery at the nuclear basket by promoting condensates formation

Plants must cope with the highly dynamic nature of light to survive and thrive, a process referred to as acclimation. Although acclimation to different light intensities has been well studied, there has been little research into the effects of dynamic lighting regimes on this process. Natural fluctuating light in field grown crops, can limit photosynthesis through slow stomatal opening in response to increasing light, whilst slow stomatal closure can erode water use efficiency (McAusland et al, 2016). It has been reported that both biochemical and stomata limitation on photosynthesis can lead to wheat yield losses of upto 21% (Taylor and Long, 2017).Previously dynamic growth light has been shown to effect the photosynthetic abilities of Arabidopsis thaliana, reducing maximum photosynthetic capacity and light absorption and altering light use efficiency along with changes in photoprotection (Vialet-Chabrand et al., 2017). To understand changes in gene expression resulting from acclimation to fluctuating light, Whole Genome Bisulfite Sequencing (WGBS) was utilised to examine changes in DNA methylation. Genome-wide changes were noted, with differentially methylated regions observed across a range of protein coding genes, transposable elements, and non-coding RNAs, as well as multiple regulatory sequences. RNAseq analysis demonstrated that some of these genes with changed methylation state impacted transcription, although many more changes in transcript levels were noted beyond the WGBS data. This could provide a new set of gene targets for improved photosynthetic efficiency and ultimately crop yield, which could be incorporated into on-going crop breeding programmes.

The Ups and Downs of Being an Outdoor Plant

Decision making have hitherto been investigated almost exclusively in multicellular neural organisms. Yet, evidence for decision making  have been described in single celled organisms such as acellular slime molds. In the last 20 years, slime molds have become a model system, with multiple experiments seeking to reproduce behavioural predictions from neuroscience, animal behaviour and psychology In this talk, I will  focus on decision making in slime molds and explore various frameworks: nutritional geometry, speed versus accuracy trade-off, magnitude-sensitive reaction times, Weber's law and social influence.  Hopefully by the end of my talk, you will be convinced that slime molds are an ideal model system in which to investigate fundamental mechanisms underlying the ground-floor of decision making abilities. 

Problem solving in acellular slime molds

Extensive efforts have revealed genetic programs plants use to control their development in response to the environment. Much less is known about how the output of these programs is impacted by the multicellular context they operate within. In order to better understand how collections of cells in plants process information, we are taking a computational perspective of development and examining parallels between these naturally evolved biological organisms and engineered computational systems. More specifically, whether the control principles of distributed computation apply to plants. In an effort to address this, we are viewing plant organs as integrated systems of interacting cells, and mapping intercellular connectivity into networks. This provides a quantitative approach to understanding cellular patterning, while mapping the multicellular “circuitry” plants use to perform computation. By integrating these topological templates with mathematical models describing the genetic programs that operate within individual cells, the impact of each cell organization and communication on developmental outputs is being examined. This is providing insight into the extent to which development is controlled beyond intracellular genetic mechanisms.  

Information processing in plant organs

Fate decisions in developing tissues involve cells transitioning between a set of discrete cell states. Geometric models, often referred to as Waddington landscapes, are an appealing way to describe differentiation dynamics and developmental decisions. We consider the differentiation of neural and mesodermal cells from pluripotent mouse embryonic stem cells exposed to different combinations and durations of signalling factors. We developed a principled statistical approach using flow cytometry data to quantify differentiating cell states. Then, using a framework based on Catastrophe Theory and approximate Bayesian computation, we constructed the corresponding dynamical landscape. The result was a quantitative model that accurately predicted the proportions of neural and mesodermal cells differentiating in response to specific signalling regimes. Taken together, the approach we describe is broadly applicable for the quantitative analysis of differentiation dynamics and for determining the logic of developmental cell fate decisions.

Gene-free landscape models for development

Capturing the rules governing developmental decisions in multicellular organisms is key to study cellular functions, including  reprogramming of cell differentiation and function. To understand how different genes coordinately regulate developmental decisions towards cell function, we used a multi-scale hybrid model integrating ordinary differential equations (ODEs) and agent-based modeling. This model allowed us to gain a deeper understanding in the coordinate function of key developmental genes, including WUSCHEL-RELATED HOMEOBOX 5 (WOX5) and SHORTROOT (SHR), to regulate stem cell divisions. We predicted cell-type-specific expression dynamics of SHR, SCARECROW, WOX5, AN3 and CYCLIND6;1, and showed an interdependency between CEI and QC divisions. At present, we know these stem cell populations divide, differentiate and display functions in response to relative positional information. A major challenge is to accurately capture the multicellular 3 dimensional (3D) microenvironment. To further study systemic behavior of these stem cells within a defined microenvironment, we established the framework of 3D bioprinting with plant cells to study cell viability, cell division, and cell identity. Within our designed microenvironment, the deposited Arabidopsis and soybean cells re-entered the cell cycle, which led to the formation of microcalli. Furthermore, we showed that the identity of isolated cells of Arabidopsis roots expressing endodermal markers maintained longer periods of time. We believe that the 3D bioprinting framework paves the way for a general use of 3D bioprinting for studying the rules governing developmental decisions.

Coordinated regulation of gene expression among stem cells

The plant hormone gibberellin (GA) is involved in many developmental processes, however, how GA is distributed within plant tissues is not yet understood. In this talk, we present a multi-cellular mathematical model for GA transport within the Arabidopsis root. We consider both passive and facilitated modes of transport through the symplast and the apoplast. In particular, we model the effects of the NPF cytoplasm importers, localised in different layers of the root. In addition, we consider the effect of a vacuole as a possible storage mechanism for GA within each cell and model the role of transport across the tonoplast. We assume an effective GA source coming from the stele and constant degradation rate of GA within the whole root. We also present results on the values of the various transporter permeabilities, estimated from a model and oocyte experimental data. We discuss the governing equations and show numerical results predicting the spatial and temporal distribution of GA. Our results provide insights into the role of the vacuole in regulating the amount of GA in the cell, and how this contributes to GA distributions and cellular decision making.

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Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird

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