Challenges during diapause and anhydrobiosis: Mitochondrial bioenergetics and desiccation tolerance

Hand, Steven C.; Moore, Daniel; Patil, Yuvraj

doi:10.1002/iub.1953

Cited by 19 publications

(14 citation statements)

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“…During anhydrobiosis, tissue water can decrease to less than 2% (Crowe and Madin 1974), which imposes substantial challenges for defending the functionality of biological structures (Crowe et al 1997;Clegg 1973, 1978). One key strategy for desiccation tolerance in many anhydrobiotes is the accumulation of protective molecules such as late embryogenesis abundant (LEA) proteins, heat-shock proteins, and stabilizing organic solutes (Clegg 2005(Clegg , 2011Crowe et al 1998Crowe et al , 2005Hand et al 2011Hand et al , 2018Tan and MacRae 2018;Tapia and Koshland 2014;Tunnacliffe and Wise 2007). The present study focuses on AfrLEA6, a group 6 LEA protein also referred to as a seed maturation protein (SMP).…”

Section: Introductionmentioning

confidence: 99%

Structural properties and cellular expression of AfrLEA6, a group 6 late embryogenesis abundant protein from embryos of Artemia franciscana

LeBlanc

Janis

et al. 2019

Cell Stress and Chaperones

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Late embryogenesis abundant (LEA) proteins are intrinsically disordered proteins (IDPs) commonly found in anhydrobiotic organisms and are frequently correlated with desiccation tolerance. Herein we report new findings on AfrLEA6, a novel group 6 LEA protein from embryos of Artemia franciscana. Assessment of secondary structure in aqueous and dried states with circular dichroism (CD) reveals 89% random coil in the aqueous state, thus supporting classification of AfrLEA6 as an IDP. Removal of water from the protein by drying or exposure to trifluoroethanol (a chemical de-solvating agent) promotes a large gain in secondary structure of AfrLEA6, predominated by α-helix and exhibiting minimal β-sheet structure. We evaluated the impact of physiological concentrations (up to 400 mM) of the disaccharide trehalose on the folding of LEA proteins in solution. CD spectra for AfrLEA2, AfrLEA3m, and AfrLEA6 are unaffected by this organic solute noted for its ability to drive protein folding. AfrLEA6 exhibits its highest concentration in vivo during embryonic diapause, drops acutely at diapause termination, and then declines during development to undetectable values at the larval stage. Maximum cellular titer of AfrLEA6 was 10-fold lower than for AfrLEA2 or AfrLEA3, both group 3 LEA proteins. Acute termination of diapause with H 2 O 2 (a far more effective terminator than desiccation in this Great Salt Lake, UT, population) fostered a rapid 38% decrease in AfrLEA6 content of embryos. While the ultimate mechanism of diapause termination is unknown, disruption of key macromolecules could initiate physiological signaling events necessary for resumption of development and metabolism.

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Section: Introductionmentioning

confidence: 99%

Structural properties and cellular expression of AfrLEA6, a group 6 late embryogenesis abundant protein from embryos of Artemia franciscana

LeBlanc

Janis

et al. 2019

Cell Stress and Chaperones

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“…The location of genes of well-known effectors of anhydrobiosis within ARIds provides further evidence of this connection. LEA proteins of Group 3, whose genes are co-located with PvLil genes, are extensively studied in a wide variety of organisms, demonstrating both the association with water deficit and experimentally verified effects, such as reducing surface-induced aggregation of proteins, protection and stabilizing the lipid bilayers and mitochondria, increasing cytoplasmic conductivity of cells, reinforcing sugar glasses 9,[25][26][27][28] . The latter include the transition from an intrinsically disordered to a structured state on dehydration, the reinforcement of trehalose-based glassy matrix and direct protection of proteins against desiccation-induced aggregation demonstrated for PvLEA22 protein 14,15 .…”

Section: Discussionmentioning

confidence: 99%

“…In many cases, the genes with a key involvement in the acquisition of desiccation tolerance are represented in a genome by multiple copies, and it seems that duplication of essential genes in the evolutionary process is a single-species attribute of P. vanderplanki 17 . In the P. vanderplanki genome, 27 Lea genes (PvLea) were identified, and the majority of them are localized in a single genomic cluster. In this cluster we also found 13 tandemly located paralogous genes that have no known orthologues in other species.…”

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confidence: 99%

New group of transmembrane proteins associated with desiccation tolerance in the anhydrobiotic midge Polypedilum vanderplanki

Voronina

Несмелов

Kondratyeva

et al. 2020

Sci Rep

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Larvae of the sleeping chironomid Polypedilum vanderplanki are known for their extraordinary ability to survive complete desiccation in an ametabolic state called "anhydrobiosis". The unique feature of P. vanderplanki genome is the presence of expanded gene clusters associated with anhydrobiosis. While several such clusters represent orthologues of known genes, there is a distinct set of genes unique for P. vanderplanki. These include Lea-Island-Located (LIL) genes with no known orthologues except two of LeA genes of P. vanderplanki, PvLea1 and PvLea3. However, PvLIL proteins lack typical features of LEA such as the state of intrinsic disorder, hydrophilicity and characteristic LEA_4 motif. They possess four to five transmembrane domains each and we confirmed membrane targeting for three PvLILs. Conserved amino acids in PvLIL are located in transmembrane domains or nearby. PvLEA1 and PvLEA3 proteins are chimeras combining LEA-like parts and transmembrane domains, shared with PvLIL proteins. We have found that PvLil genes are highly upregulated during anhydrobiosis induction both in larvae of P. vanderplanki and P. vanderplanki-derived cultured cell line, Pv11. Thus, PvLil are a new intriguing group of genes that are likely to be associated with anhydrobiosis due to their common origin with some LeA genes and their induction during anhydrobiosis. Anhydrobiosis is the ability of an organism to survive complete desiccation in the ametabolic state. Animals able to enter anhydrobiosis at least at some life stages are found in four invertebrate phyla, namely tardigrades, rotifers, nematodes and arthropods 1,2. Damaging effects of desiccation in these animals are mitigated via interplay of numerous protective mechanisms, including the formation of biological glass (vitrification), "molecular shield" and anti-aggregation activity of some proteins and enhanced antioxidant activity 3-5. Intrinsically disordered proteins (IDP's) frequently participate at least in some of the protective mechanisms related to desiccation tolerance 5-9. Anhydrobiotic animals share also such features as a small size which is typically less than 5 mm and an absence of internal skeletons, at least on anhydrobiotic life stages. This may be related to physical stresses associated with body shrinking during water loss 10. Larvae of the sleeping chironomid Polypedilum vanderplanki (Diptera) reaching 7 mm in length are the largest and the most complex organisms able to enter anhydrobiosis 11. This midge inhabits semi-arid rocks in Nigeria, and its larvae represent the only stage of the life cycle that is capable of enduring the desiccation at the onset of the dry season 12 .

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“…This is coupled with constitutive immune expression being costly to generate and maintain [14][15][16][17], especially during periods of low nutritional intake [18,19]. Diapausing organisms are also at greater risk of desiccation and require mechanisms to reduce water loss [20][21][22].…”

Section: Introductionmentioning

confidence: 99%

Mating induces selective immune priming which is maintained throughout bumblebee queen diapause

Colgan

Finlay

Brown

et al. 2019

Preprint

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Background: Understanding the mechanisms by which organisms adapt to unfavourable conditions is a fundamental question in ecology and evolutionary biology. One such mechanism is diapause, a period of dormancy typically found in nematodes, fish, crustaceans and insects. This state is a key life-history event characterised by arrested development, suppressed metabolism and increased stress tolerance and allows an organism to avoid prolonged periods of harsh and inhospitable environmental conditions. For some species, diapause is preceded by mating which can have a profound effect on female behaviour, physiology and key biological processes, including immunity. However, our understanding of how mating impacts long-term immunity and whether these effects persist throughout diapause is currently limited. To address this, we explored molecular changes in the haemolymph of the ecologically important pollinator, the buff-tailed bumblebee Bombus terrestris . B. terrestris queens mate prior to entering diapause, a non-feeding period of arrested development that can last 6-9 months. Using mass-spectrometry-based proteomics, we quantified changes in the pre-diapause queen haemolymph after mating, as well as the subsequent protein expression of mated queens during and post-diapause. Results: Our analysis identified distinct proteome profiles associated with diapause preparation, maintenance and termination. More specifically, mating pre-diapause was shown to increase the abundance of antimicrobial peptides, key effectors of the immune system. Furthermore, we identified the elevated abundance of these proteins to be maintained throughout diapause. This finding was in contrast to a general reduction in immune proteins during diapause suggestive of selective immune priming and expression during diapause. Diapause also affected the expression of proteins involved in cuticular maintenance, olfaction, as well as proteins of unknown function, which may have roles in diapause regulation. Conclusions: Our results provide clear molecular evidence for the consequences and benefits of mating at the immune level through the selective increased abundance of antimicrobial peptides that are sustained throughout diapause. In addition, our results provide novel insights into the molecular mechanisms by which bumblebees prepare for, survive, and recover from diapause, insights that may have implications for our general understanding of these processes in other insect groups.

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Challenges during diapause and anhydrobiosis: Mitochondrial bioenergetics and desiccation tolerance

Cited by 19 publications

References 76 publications

Structural properties and cellular expression of AfrLEA6, a group 6 late embryogenesis abundant protein from embryos of Artemia franciscana

Structural properties and cellular expression of AfrLEA6, a group 6 late embryogenesis abundant protein from embryos of Artemia franciscana

New group of transmembrane proteins associated with desiccation tolerance in the anhydrobiotic midge Polypedilum vanderplanki

Mating induces selective immune priming which is maintained throughout bumblebee queen diapause

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