Mechanisms underlying insect freeze tolerance

Freeze tolerance – the ability to survive internal ice formation – has evolved repeatedly in insects, facilitating survival in environments with low temperatures and/or high risk of freezing. Surviving internal ice formation poses several challenges because freezing can cause cellular dehydration and mechanical damage, and restricts the opportunity to metabolise and respond to environmental challenges. While freeze‐tolerant insects accumulate many potentially protective molecules, there is no apparent ‘magic bullet’ – a molecule or class of molecules that appears to be necessary or sufficient to support this cold‐tolerance strategy. In addition, the mechanisms underlying freeze tolerance have been minimally explored. Herein, we frame freeze tolerance as the ability to survive a process: freeze‐tolerant insects must withstand the challenges associated with cooling (low temperatures), freezing (internal ice formation), and thawing. To do so, we hypothesise that freeze‐tolerant insects control the quality and quantity of ice, prevent or repair damage to cells and macromolecules, manage biochemical processes while frozen/thawing, and restore physiological processes post‐thaw. Many of the molecules that can facilitate freeze tolerance are also accumulated by other cold‐ and desiccation‐tolerant insects. We suggest that, when freezing offered a physiological advantage, freeze tolerance evolved in insects that were already adapted to low temperatures or desiccation, or in insects that could withstand small amounts of internal ice formation. Although freeze tolerance is a complex cold‐tolerance strategy that has evolved multiple times, we suggest that a process‐focused approach (in combination with appropriate techniques and model organisms) will facilitate hypothesis‐driven research to understand better how insects survive internal ice formation.     

Functional impairment of MSC induced by transient warming events: Correlation with loss of adhesion and altered cell size

Background

We recently showed that transient warming effects decreased the functional and adhesion properties of mesenchymal stromal cells (MSC) while post-thaw viability remained high. In an attempt to better predict functional impairment of cryopreserved MSC, we further analysed the correlation between viability, immunosuppressive activity and adhesion of cells exposed or not to warming events.

The ex vivo toll-like receptor 7 tolerance induction in donor lymphocytes prevents murine acute graft-versus-host disease

Background aims

Acute graft-versus-host disease (aGVHD) remains a major cause of morbidity and mortality after allogeneic hematopoietic stem cell transplantation, mediated by alloreactive donor T cells. Toll-like receptors (TLRs), a family of conserved pattern-recognition receptors (PRRs), represent key players in donors' T-cell activation during aGVHD; however, a regulatory, tolerogenic role for certain TLRs has been recognized in a different context. We investigated whether the ex vivo–induced TLR-2,-4,-7 tolerance in donor cells could prevent alloreactivity in a mismatched transplantation model.

Seed germination and antioxidant pattern in Lavandula multifida (Lamiaceae): A comparison between core and peripheral populations

We evaluated the environmental adaptability of Lavandula multifida L., a plant species presents in the Western Mediterranean Basin with a threatened peripheral population in Southern Italy. Germination capacity, activities of some hydrolyzing enzymes associated with germination and antioxidative pathway of Calabrian L. multifida were quantified in comparison with a Spanish core population. The Calabrian population showed a lower germination ability and it can be related to the small size of the population and associated inbreeding depression. Difference between two populations in enzymatic assays and antioxidative pattern during germination and early seedling development may in part explain a different ability of these two populations to respond to external cues and a diverse environmental adaptability. The study on germination strategies of isolated populations is important to define possible programmes to preserve genetic biodiversity of autochthon plants populations.     

Water availability,fundamental niches and realized niches: A case study from the Cape flora

The ability of plants to survive drought or waterlogging constitutes an important niche parameter, which might be particularly significant in explaining species coexistence in the species‐rich and seasonally dry Cape Floristic Region of South Africa. However, the degree of physiological adaptation and specialization to these eco‐hydrological parameters (the fundamental niche) cannot be readily inferred from correlative studies based on species distributions and spatial variation in environmental parameters (the realized niche). We used an ex situ greenhouse experiment to compare the fundamental hydrological niches (different mean annual precipitation, rainfall seasonality and soil drainage) of six eco‐hydrologically divergent African Restionaceae species. Juvenile plants were subjected to six different watering treatments, ranging from no watering to waterlogging, to determine drought and waterlogging susceptibility and optimal growth conditions. We used the rate of biomass accumulation and survival rate as response measures. We found that species from dry and mesic (but well‐drained) habitats had optimal or near‐optimal growth at benign conditions (under which most restio species grow well). All species performed worse when droughted and died when not watered. Species from dry habitats tended to perform better (assessed in growth) than species from wet habitats under droughting. Species from wet habitats performed best when waterlogged, whereas species from dry habitats performed very poorly when waterlogged – thus showing that realized and fundamental niches covaried at the wet end of the hydrological gradient. We conclude that eco‐hydrological parameters are part of the fundamental niche, and fundamental and realized species niches are approximately correlated along them. The distribution of wet habitat species appears not to reflect their drought tolerance, suggesting that it may not be predicted by bioclimatic variables, but rather by soil drainage characteristics.     

A unified framework of plant adaptive strategies to drought: Crossing scales and disciplines

Plant adaptation to drought has been extensively studied at many scales from ecology to molecular biology across a large range of model species. However, the conceptual frameworks underpinning the definition of plant strategies, and the terminology used across the different disciplines and scales are not analogous. ‘Drought resistance’ for instance refers to plant responses as different as the maintenance of growth and productivity in crops, to the survival and recovery in perennial woody or grassland species. Therefore, this paper aims to propose a unified conceptual framework of plant adaptive strategies to drought based on a revised terminology in order to enhance comparative studies. Ecological strategies encapsulate plant adaptation to multidimensional variation in resource variability but cannot account for the dynamic and short‐term responses to fluctuations in water availability. Conversely, several plant physiological strategies have been identified along the mono‐dimensional gradient of water availability in a given environment. According to a revised terminology, dehydration escape, dehydration avoidance, dehydration tolerance, dormancy, and desiccation tolerance are clearly distinguishable. Their sequential expression is expressed as water deficit increases while cavitation tolerance is proposed here to be a major hydraulic strategy underpinning adaptive responses to drought of vascular plants. This continuum of physiological strategies can be interpreted in the context of the ecological trade‐off between water‐acquisition vs. water‐conservation, since growth maintenance is associated with fast water use under moderate drought while plant survival after growth cessation is associated with slow water use under severe drought. Consequently, the distinction between ‘drought resistance’ and ‘drought survival’, is emphasized as crucial to ensure a correct interpretation of plant strategies since ‘knowing when not to grow’ does not confer ‘drought resistance’ but may well enhance ‘drought survival’. This framework proposal should improve cross‐fertilization between disciplines to help tackle the increasing worldwide challenges that drought poses to plant adaptation.     

Assessing the sensitivity of bivalve populations to global warming using an individual‐based modelling approach

Climate change exposes benthic species populations in coastal ecosystems to a combination of different stressors (e.g., warming, acidification and eutrophication), threatening the sustainability of the ecological functions they provide. Thermal stress appears to be one of the strongest drivers impacting marine ecosystems, acting across a wide range of scales, from individual metabolic performances to geographic distribution of populations. Accounting for and integrating the response of species functional traits to thermal stress is therefore a necessary step in predicting how populations will respond to the warming expected in coming decades. Here, we developed an individual‐based population model using a mechanistic formulation of metabolic processes within the framework of the dynamic energy budget theory. Through a large number of simulations, we assessed the sensitivity of population growth potential to thermal stress and food conditions based on a climate projection scenario (Representative Concentration Pathway; RCP8.5: no reduction of greenhouse gas emissions). We focused on three bivalve species with contrasting thermal tolerance ranges and distinct distribution ranges along 5,000 km of coastline in the NE Atlantic: the Pacific oyster (Magallana gigas), and two mussel species: Mytilus edulis and Mytilus galloprovincialis. Our results suggest substantial and contrasting changes within species depending on local temperature and food concentration. Reproductive phenology appeared to be a core process driving the responses of the populations, and these patterns were closely related to species thermal tolerances. The nonlinear relationship we found between individual life‐history traits and response at the population level emphasizes the need to consider the interactions resulting from upscaling across different levels of biological organisation. These results underline the importance of a process‐based understanding of benthic population response to seawater warming, which will be necessary for forward planning of resource management and strategies for conservation and adaptation to environmental changes.     

Effective tolerance based on resource reallocation is a virus‐specific defence in Arabidopsis thaliana

Plant viruses often harm their hosts, which have developed mechanisms to prevent or minimize the effects of virus infection. Resistance and tolerance are the two main plant defences to pathogens. Although resistance to plant viruses has been studied extensively, tolerance has received much less attention. Theory predicts that tolerance to low‐virulent parasites would be achieved through resource reallocation from growth to reproduction, whereas tolerance to high‐virulent parasites would be attained through shortening of the pre‐reproductive period. We have shown previously that the tolerance of Arabidopsis thaliana to Cucumber mosaic virus (CMV), a relatively low‐virulent virus in this host, accords to these predictions. However, whether other viruses trigger the same response, and how A. thaliana copes with highly virulent virus infections remains unexplored. To address these questions, we challenged six A. thaliana wild genotypes with five viruses with different genomic structures, life histories and transmission modes. In these plants, we quantified virus multiplication, virulence, and the effects of infection on plant growth and reproduction, and on the developmental schedule. Our results indicate that virus multiplication varies according to the virus × host genotype interaction. Conversely, effective tolerance is observed only on CMV infection, and is associated with resource reallocation from growth to reproduction. Tolerance to the other viruses is observed only in specific host–virus combinations and, at odds with theoretical predictions, is linked to longer pre‐reproductive periods. These findings only partially agree with theoretical predictions, and contribute to a better understanding of pathogenic processes in plant–virus interactions.     

Engineering heat tolerance in potato by temperature‐dependent expression of a specific allele of HEAT‐SHOCK COGNATE 70

For many commercial potato cultivars, tuber yield is optimal at average daytime temperatures in the range of 14–22 °C. Further rises in ambient temperature can reduce or completely inhibit potato tuber production, with damaging consequences for both producer and consumer. The aim of this study was to use a genetic screen based on a model tuberization assay to identify quantitative trait loci (QTL) associated with enhanced tuber yield. A candidate gene encoding HSc70 was identified within one of the three QTL intervals associated with elevated yield in a Phureja–Tuberosum hybrid diploid potato population (06H1). A particular HSc70 allelic variant was linked to elevated yield in the 06H1 progeny. Expression of this allelic variant was much higher than other alleles, particularly on exposure to moderately elevated temperature. Transient expression of this allele in Nicotiana benthamiana resulted in significantly enhanced tolerance to elevated temperature. An TA repeat element was present in the promoter of this allele, but not in other HSc70 alleles identified in the population. Expression of the HSc70 allelic variant under its native promoter in the potato cultivar Desiree resulted in enhanced HSc70 expression at elevated temperature. This was reflected in greater tolerance to heat stress as determined by improved yield under moderately elevated temperature in a model nodal cutting tuberization system and in plants grown from stem cuttings. Our results identify HSc70 expression level as a significant factor influencing yield stability under moderately elevated temperature and identify specific allelic variants of HSc70 for the induction of thermotolerance via conventional introgression or molecular breeding approaches.