Multiple genes contribute to anhydrobiosis (tolerance to extreme desiccation) in the nematode Panagrolaimus superbus

Evangelista, Cláudia Carolina Silva; Guidelli, Giovanna Vieira; Borges, Gustavo; Araujo, Thaís Fenz; Souza, Tiago Alves Jorge de; Neves, Ubiraci Pereira da Costa; Tunnacliffe, Alan; Pereira, Tiago Campos

doi:10.1590/1678-4685-gmb-2017-0030

Cited by 14 publications

(23 citation statements)

References 68 publications

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“…In particular, Pratylenchus spp. can adopt a strategy known as anhydrobiosis that allows the juvenile and adult stages to survive periods without plant hosts or severe dry, cold, or hot conditions [27,28]. During anhydrobiosis, metabolism and life processes are slowed down, but Pratylenchus spp.…”

Section: Introductionmentioning

confidence: 99%

Functional Variation of Two Novel Cellulases, Pv-eng-5 and Pv-eng-8, and the Heat Shock 90 Gene, Pv-hsp-90, in Pratylenchus vulnus and Their Expression in Response to Different Temperature Stress

Fanelli

Troccoli

Luca

2018

IJMS

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Functional characterization of two novel endoglucanase genes, Pv-eng-5 and Pv-eng-8, of the root-lesion nematode Pratylenchus vulnus was carried out. In situ-hybridization experiments revealed that Pv-eng-8 transcript was localized in the pharyngeal glands. Silencing of Pv-eng-5 and Pv-eng-8 resulted in a significant reduction of expression level (52% and 67%, respectively). Furthermore, the silencing of Pv-eng-8 determined a reduction (41%) in nematode reproduction, suggesting that treated nematodes are much less able to process food. Surprisingly, no significant difference on reproduction rate was observed with Pv-eng-5 dsRNA nematodes, suggesting a neofunctionalization of Pv-eng-5 despite the high similarity with nematode endoglucanases. Pratylenchus species are poikilothermic organisms showing close relationships with the environmental temperature. The effects of different temperature ranges revealed that the reproductive potential of P. vulnus increased with increasing temperature from 23 °C to 28 °C, but no reproduction was observed at 33 °C. In real time, increasing temperature from 23 °C to 28 °C the heat shock gene Pv-hsp-90 was differentially expressed in adult stages, while the levels of the effector genes Pv-eng-1 and Pv-eng-8 in females showed no significant differences compared to those observed at 23 °C, only in males Pv-eng-8 level decreased (45%). The upregulation of Pv-hsp-90 in both adult stages suggests a protective mechanism in order to cope with unfavorable environmental conditions.

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Section: Introductionmentioning

confidence: 99%

Functional Variation of Two Novel Cellulases, Pv-eng-5 and Pv-eng-8, and the Heat Shock 90 Gene, Pv-hsp-90, in Pratylenchus vulnus and Their Expression in Response to Different Temperature Stress

Fanelli

Troccoli

Luca

2018

IJMS

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“…4). The potential contribution of calcium signalings to anhydrobiosis was also suggested in tardigrades and nematodes 67,68 . In the anhydrobiotic tardigrade, Hypsibius dujardini, a calmodulin inhibitor (J-8) and a calcium release modulator (2-APB) reduced the survival rate after rehydration, but the inhibitors against CaN and CaMK had no effect on the anhydrobiotic ability.…”

Section: Discussionmentioning

confidence: 88%

“…Given that calmodulin regulates the gating of calcium ion channel in endoplasmic reticulum and mitochondrion as well as the signaling pathways 69,70 , the J-8 and 2-APB treatments may disrupt calcium storage in the organelles rather than calcium signalings, leading to malfunction of those intracellular organelles 71,72 . RNAi-based screening using the nematode Panagrolaimus superbus, showed that knockdown of “CAMK/CAMKL/MELK protein kinase” decreased the survival rate after rehydration 68 , whereas the contribution of CaN - NFAT pathway or CREB on the anhydrobiotic ability was not assessed. Our detailed experiments show that the CaM - CaN - NFAT pathway activation confers the tolerance to both trehalose incubation and desiccation on Pv11 cells, while the CaM - CaMK - CREB pathway activation gives only desiccation tolerance (Figs.…”

Section: Discussionmentioning

confidence: 99%

Cas9-mediated Genome Editing Reveals a Significant Contribution of Calcium Signaling Pathways to Anhydrobiosis in Pv11

Miyata

Fuse

Tokumoto

et al. 2020

Preprint

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Pv11 is an insect cell line established from the midge Polypedilum vanderplanki that exhibits an extreme desiccation tolerance known as anhydrobiosis. Pv11 has also an anhydrobiotic ability which is induced by trehalose treatment. Here we report the successful construction of the genome editing system for Pv11 cells and its application for identifying the signaling pathways in the anhydrobiosis. Using the Cas9-mediated gene knock-in system, we established GCaMP3-stably expressing Pv11 cells to monitor intracellular Ca2+ mobilization. Intriguingly, trehalose treatment evoked a transient increase of cytosolic Ca2+ concentration, and further experiments indicated the contribution of the calmodulin - calcineurin - NFAT pathway to the tolerance for trehalose treatment as well as the desiccation tolerance, while the calmodulin - calmodulin Kinase - CREB pathway conferred only the desiccation tolerance on Pv11 cells. Thus, our results show the critical contribution of the trehalose-induced Ca2+ surge to the anhydrobiosis and the temporal different roles of each signaling pathway.

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“…However, such a sample requires strong precautions to minimize the possibility of contamination 23,38,42 . After rigorous filtering of possible contaminants as described above, we generated a 153. appears to be a common mechanism in anhydrobiosis, not one that is limited to tardigrades 43,44 . In addition, we identified several genes in stress signaling pathways, i.e., genes involved in stress signaling pathways.…”

Section: Discussionmentioning

confidence: 99%

Multiomics study of a heterotardigrade,Echinisicus testudo, suggests convergent evolution of anhydrobiosis-related proteins in Tardigrada

Murai

Yagi-Utsumi

Tomita

et al. 2020

Preprint

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Many limno-terrestrial tardigrades can enter an ametabolic state upon desiccation, in which the animals can withstand extreme environments. To date, studies of the molecular mechanism have predominantly investigated the class Eutardigrada, and that in the Heterotardigrada, remains elusive. To this end, we report a multiomics study of the heterotardigrade Echiniscus testudo, which is one of the most desiccation-tolerant species. None of the previously identified tardigrade-specific anhydrobiosis-related genes was conserved, while the loss and expansion of existing pathways were partly shared. Furthermore, we identified two families of novel abundant heat-soluble proteins and the proteins exhibited structural changes from random coil to α-helix as the water content decreased in vitro. These characteristics are analogous to those of anhydrobiosis-related protein in eutardigrades, while there is no conservation at the sequence level. Our results suggest that Heterotardigrada have partly shared but distinct anhydrobiosis machinery compared with Eutardigrada, possibly due to convergent evolution within Tardigrada.

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Multiple genes contribute to anhydrobiosis (tolerance to extreme desiccation) in the nematode Panagrolaimus superbus

Cited by 14 publications

References 68 publications

Functional Variation of Two Novel Cellulases, Pv-eng-5 and Pv-eng-8, and the Heat Shock 90 Gene, Pv-hsp-90, in Pratylenchus vulnus and Their Expression in Response to Different Temperature Stress

Functional Variation of Two Novel Cellulases, Pv-eng-5 and Pv-eng-8, and the Heat Shock 90 Gene, Pv-hsp-90, in Pratylenchus vulnus and Their Expression in Response to Different Temperature Stress

Cas9-mediated Genome Editing Reveals a Significant Contribution of Calcium Signaling Pathways to Anhydrobiosis in Pv11

Multiomics study of a heterotardigrade,Echinisicus testudo, suggests convergent evolution of anhydrobiosis-related proteins in Tardigrada

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