113 Crickets: Spring 2012
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For cold-acclimated crickets relative to warm-acclimated crickets, shifts in expression are either upregulated orange , downregulated blue , or unchanged grey. A complete list of differentially-expressed genes in the Malpighian tubules is provided in Additional file 2 : Spreadsheet S1. Cold acclimation led to variable expression of multiple cytoskeletal genes, increased expression of two apoptosis genes, and decreased expression of one gene involved in autophagosome formation. Similar to the hindgut, cold-acclimated Malpighian tubules also exhibited increased expression of hsp 70 and downregulation of hsp 67B , and both up- and downregulation of multiple repair and antioxidant genes including those encoding putative cytochrome Ps and glutathione-S-transferases.
Multiple kinase genes were upregulated in cold-acclimated Malpighian tubules similar to the hindgut in addition to a relatively large decrease 6. Altered expression of circadian genes following cold acclimation were also similar to that of the hindgut, and juvenile hormone expression was reduced nearly fold. Selected upregulated genes in the Malpighian tubules following cold acclimation whose putative function in relation to cold tolerance is discussed in the text. For a full list of the upregulated Malpighian tubule genes, see Additional file 2 : Spreadsheet S1.
Selected downregulated genes in the Malpighian tubules following cold acclimation whose putative function in relation to cold tolerance is discussed in the text. For a full list of the downregulated Malpighian tubule genes, see Additional file 2 : Spreadsheet S1. Similar to patterns in the hindgut, more KEGG pathways were downregulated than were upregulated in cold-acclimated Malpighian tubules Fig. Many of the 20 upregulated pathways were involved in signaling, and most of the 47 downregulated pathways related to metabolism. Unlike in the hindgut, NKA, tropomyosin, or myosin heavy chain components of this pathway were not upregulated in Malpighian tubules.
Cold-acclimated Gryllus pennsylvanicus exhibited modified expression of a range of genes, the functions of which were broadly consistent with differentially-regulated genes associated with cold acclimation and rapid cold-hardening in Drosophila [ 56 , 58 , 80 ]. In crickets, genes involved in stress response, protein folding, and repair were prominent in cold acclimated hindguts, while cold acclimation in the Malpighian tubules was associated with shifts in transport-related genes.
In both tissues, cold acclimation was accompanied by altered expression of genes encoding components of the membrane and extracellular space. Only one gene with known function in insect water homeostasis — that encoding atrial natriuretic peptide-converting enzyme — was upregulated in the hindgut following cold acclimation. Although some aquaporins have been associated with insect freeze tolerance [ 83 — 85 ], their role in cold acclimation among chill-susceptible insects is unknown, and none of the water-transporting insect aquaporins [ 86 ] were differentially-expressed in the hindgut or Malpighian tubules with cold acclimation.
Most of these gene expression changes were observed in the hindgut. Although all of these transport enzymes contribute to primary urine production by the Malpighian tubules [ 88 ], cold-acclimated Malpighian tubules only exhibited downregulation of genes encoding V-ATPase and CAs 1 and 9. Downregulation of CA9 membrane-bound , CA1 cytosolic , and V-ATPase in the Malpighian tubules during cold acclimation could therefore have an antidiuretic effect, perhaps defending hemolymph volume in the cold.
Indeed, cold-acclimated G. However, it is unclear how NKA activity changes in D. Cold acclimation was associated with altered expression of cell and tissue structure-related genes e. In addition to possible roles in providing protons for ion transport, CA9 may have roles in cellular adhesion [ 99 ], proliferation, and differentiation at least in mammals [ ].
Thus, CA9 downregulation in hindgut and Malpighian tubules during cold acclimation may affect epithelial transport by increasing cellular adhesion and epithelial tightness. Tissue-specific post-translational modification of CA9 is an important means of regulating CA9 activity [ ], which would not be captured in a transcriptome comparison such as the present study. Cold-acclimated crickets had altered expression of hindgut cellular adhesion components associated with both adherens and septate junctions, which comprise the bulk of paracellular connections in the rectal pad [ 31 , — ], and are closely related [ ].
Cold acclimation was also associated with differential expression of genes encoding actin-membrane anchors, which could influence cell junction characteristics or cell shape. We hypothesise that altered actin-membrane anchoring could reduce tension, shearing damage, or unwanted stretch-activation of membrane-bound ion channels [ 4 , ] when the gut is distended by water migration during cold exposure.
Some gap and tight junction components were also altered during cold acclimation. These will likely modify ion and water recycling between the cytoplasm and paracellular channels [ , ], and selectivity of absorption [ , ]. After cold acclimation, we also observed shifts in the expression of multiple Malpighian tubule genes involving the cytoskeleton and cell junctions e. Whether these structural changes affect ion and water balance requires some assessment of Malpighian tubule permeability following cold acclimation.
Cold-attributed oxidative stress, disruption of homeostasis and signaling, protein mis-folding, and loss of membrane and cytoskeletal integrity may all contribute to chilling injury and mortality in chill-susceptible insects [ 12 , 15 , — ]. Cold acclimation was associated with upregulation of putative apoptosis genes e. We hypothesize that the ability to clear cold-damaged cells or cell components is likely increased in cold-acclimated crickets.
Polymorphisms or shifts in the expression of genes associated with apoptosis and autophagy appear to be common to the rapid cold-hardening process [ 56 ], and response to dehydration [ , ] in other insects. The cytoskeleton depolymerises at low temperatures in fish, mammals, and insects [ 6 , 7 , , ], and damage to the cytoskeleton could well be associated with chilling injury in insects.
Water loss — which occurs during cold exposure in chill-susceptible species — appears to drive shifts in cytoskeletal gene expression in other insects [ ]. Together, this suggests enhanced polymerisation and stabilization of actin and microtubules. Cytoskeleton-related genes were also upregulated in cold-acclimated Culex pipiens [ 8 ], Delia antiqua [ 7 ], alfalfa Medicago sativa [ 4 ], and D. Cold exposure appears to cause oxidative stress [ 16 , , ], and cold acclimation is associated with increased activity or expression of antioxidants e.
We observed increased expression of some putative DNA repair, and glutathione-S-transferase genes in both the hindgut and Malpighian tubules after cold acclimation and decreased expression in some of these genes, which we attribute to decreased reactive oxygen species production in the cold [ 16 , ]. Insects often upregulate antioxidant expression during rewarming [ 16 , 46 , ], so it is possible that a larger suite of antioxidants may become relevant if expression is also modified after cold exposure.
Cold acclimation was associated with increased expression of hsp 70 in both tissues as well as hsp 90 in the hindgut. Heat shock proteins have a range of cellular-protective roles including as protein chaperones, and could therefore protect against a many aspects of thermal stress and maintain cellular integrity and therefore perhaps epithelial function during and after cold exposure. In cold-acclimated D.
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Membrane remodelling is likely an important aspect of cold acclimation [ 2 , , ], and a large proportion of differentially-expressed GO cellular components in the cold-acclimated Malpighian tubules and hindgut were membrane-associated. Changes in membrane composition and fluidity with cold acclimation have not been explored in G.
Loss of signal transduction in the cold is a proposed mechanism of chill coma, and recent evidence suggests that paralysis during cold exposure results from direct inhibitory effects of low temperature on neuromuscular function [ 24 , 25 , 61 , , ]. The expression of some signal transduction and neurotransmission genes e.
Perhaps of greater interest were vesicle localization and fusion genes such as dynamin which mediates membrane-vesicle fusion , NSF a vesicle-fusing ATPase , AP2 involved in vesicle endocytosis , and syntaxin 1A which promotes vesicle-membrane docking , all of which were upregulated with cold acclimation.
Vesicle-membrane localization is important for both neurotransmission and recruitment of ion transporters the latter of which could directly affect ion homeostasis in the cold [ ] , and is likely slowed in the cold. Cold acclimation appears to affect the expression of some genes associated with circadian rhythm, storage and metabolism, development, and phosphorylation.
Differential expression of circadian genes was likely a result of the cold e. The expression of hindgut genes encoding vitellogenin a yolk protein precursor was drastically lower with cold acclimation, and this also occurs in cold-acclimated D. We have assembled the first transcriptome of Gryllus pennsylvanicus and our tissue-specific comparative approach yielded precise mechanistic hypotheses about the cold acclimation process. Remodeling of the cytoskeleton and adherens junctions and potentially tight junctions may mitigate paracellular leak of water and ions in both the hindgut and Malpighian tubules.
Cold-acclimated crickets may prevent direct chilling injury by stabilizing the actin cytoskeleton and by changing the way in which actin anchors to the membrane.
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To repair chilling injuries, cold-acclimated insects may increase expression of antioxidant, DNA repair, apoptosis, autophagy, and chaperone genes. Candidate mechanisms of cold acclimation in Gryllus pennsylvanicus. Summary of G. DOCX 12 kb. Spreadsheet S1. Complete list of genes differentially regulated in the hindgut and Malpighian tubules MTs following cold acclimation. CPM, counts per million; FC, fold-change. XLSX kb.
Spreadsheet S2. List of GO terms that were differentially represented in the hindgut and Malpighian tubules MTs following cold acclimation. Read counts of contigs associated with each GO term were summed for cold- and warm-acclimated crickets.
XLSX 82 kb. All authors read and approved the final manuscript. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Lauren E. Des Marteaux, Phone: , Email: ac. Alexander H McKinnon, Email: ac. Hiroko Udaka, Email: moc.
Jantina Toxopeus, Email: ac. Brent J. Sinclair, Email: ac. National Center for Biotechnology Information , U. BMC Genomics. Published online May 8. Sinclair 1. Des Marteaux. Author information Article notes Copyright and License information Disclaimer. Corresponding author.
Received Aug 18; Accepted Apr This article has been cited by other articles in PMC. Additional file 2: Spreadsheet S1.
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Additional file 3: Spreadsheet S2. Abstract Background Cold tolerance is a key determinant of temperate insect distribution and performance. Results We assembled a G. Conclusions This is the first G. Electronic supplementary material The online version of this article doi Background Most insects are chill-susceptible, such that their thermal performance and survival are limited in the cold at temperatures well above the freezing point [ 1 ]. Methods Insect rearing Our colony of G. De novo transcriptome assembly and annotation We removed Illumina adapter sequences and discarded sequences shorter than 15 nucleotides or containing unknown bases using the Galaxy web service [ 63 ].
Gene expression analyses We used normalized read counts of genes in warm- and cold-acclimated hindgut and Malpighian tubule libraries for differential gene expression analyses using the edgeR Bioconductor package [ 71 ] in R v3.