Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
- Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, United Kingdom
- Gurdon Institute, University of Cambridge, United Kingdom
- Van Andel Institute, United States
- Department of Molecular Genetics, University of Toronto, Canada
- Department of Biology, Duke University, United States
- Department of Molecular Biosciences, Northwestern University, United States
- Wellcome Sanger Institute, Wellcome Genome Campus, United Kingdom
- Center for Genomic and Computational Biology, Duke University, United States
- Department of Genetics, University of Cambridge, United Kingdom
Figures
Figure 1 with 1 supplement
Intergenerational adaptations to multiple stresses are evolutionarily conserved in multiple species of Caenorhabditis.
(A) Phylogenetic tree of the Elegans group of Caenorhabditis species adapted from Stevens et al., 2020. Scale represents substitutions per site. (B) Percent of wild-type C. elegans (N2), C. kamaaina …
-
Figure 1—source data 1
Statistics source data for Figure 1.
- https://cdn.elifesciences.org/articles/73425/elife-73425-fig1-data1-v2.xlsx
Figure 1—figure supplement 1
Intergenerational responses to environmental stress are conserved in wild isolates of Caenorhabditis species.
(A) Percent of wild-type C. elegans (N2) and C. briggsae (JU1348) animals surviving after 24 hr on plates seeded with P. vranovensis BIGb0446. Data presented as mean values ± s.d. n = 3 experiments …
Figure 2 with 1 supplement
Parental exposure to P. vranovensis and osmotic stress have overlapping effects on offspring gene expression across multiple species.
(A) Average fold change of 7587 single-copy ortholog genes in F1 progeny of C. elegans and C. briggsae parents fed P. vranovensis BIGb0446 when compared to parents fed E. coli HB101. Average fold …
Figure 2—figure supplement 1
Differences in developmental timing are insufficient to explain a majority of the observed differences in gene expression in the offspring of stressed parents.
(A) PCA of gene expression from Boeck et al., 2016 compared to RNA-seq data reported in the study. Time points of development are in minutes, t60 = 60 min postfertilization. (B) Percentage of genes …
Figure 3
Intergenerational adaptations to stress are stress-specific and have deleterious tradeoffs.
(A) Percent of wild-type C. elegans mobile and developing at 500 mM NaCl after 24 hr. Data presented as mean values ± s.d. n = 3 experiments of >100 animals. (B) Percent of wild-type C. elegans …
-
Figure 3—source data 1
Statistics source data for Figure 3.
- https://cdn.elifesciences.org/articles/73425/elife-73425-fig3-data1-v2.xlsx
Figure 4 with 1 supplement
Many of the intergenerational effects of parental exposure to bacterial pathogens on offspring gene expression are pathogen specific.
(A) Percent of wild-type C. elegans that developed to the L4 larval stage after 48 hr of feeding on Pseudomonas sp. 15C5. Data presented as mean values ± s.d. n = 3 experiments of >100 animals. (B) …
-
Figure 4—source data 1
Statistics source data for Figure 4.
- https://cdn.elifesciences.org/articles/73425/elife-73425-fig4-data1-v2.xlsx
Figure 4—figure supplement 1
Parental exposure to Aeromonas sp. BIGb0469 and S. plymuthica BUR1537 does not protect offspring from P. vranovensis.
Percent of wild-type C. elegans (N2) animals surviving after 24 hr on plates seeded with P. vranovensis BIGb0446. Data presented as mean values ± s.d. n = 3 experiments of >100 animals. * p < 0.05, …
Tables
Table 1
Complete list of genes that exhibited a greater than twofold change in expression in the F1 progeny of parents exposed to P. vranovensis or osmotic stress in all four species tested.
| Genes that change in F1 progeny of all species exposed to P. vranovensis | Predicted function |
|---|---|
| C18A11.1 | Unknown |
| R13A1.5 | Unknown |
| D1053.3 | Unknown |
| pmp-5 | ATP-binding activity and ATPase-coupled transmembrane transporter activity, ortholog of human ABCD4 |
| C39E9.8 | Unknown |
| nit-1 | Nitrilase ortholog – predicted to enable hydrolase activity |
| lips-10 | Lipase related |
| srr-6 | Serpentine receptor, class R |
| Y51B9A.6 | Predicted to enable transmembrane transporter activity |
| gst-33 | Glutathione S-transferase |
| ptr-8 | Patched domain containing, ortholog of human PTCHD1, PTCHD3, and PTCHD4 |
| ZC443.1 | Predicted to enable D-threo-aldose 1-dehydrogenase activity |
| cri-2 | Conserved regulator of innate immunity, ortholog of human TIMP2 |
| Y42G9A.3 | Unknown |
| ttr-21 | Transthyretin-related, involved in response to Gram-negative bacteria |
| F45E4.5 | Involved in defense against Gram-negative bacteria |
| C42D4.1 | Domain of unknown function DUF148 |
| asp-14 | Predicted to enable aspartic-type endopeptidase activity. Involved in innate immune response |
| cyp-32B1 | Cytochrome P450 family. Ortholog of human CYP4V2 |
| nas-10 | Predicted to enable metalloendopeptidase activity and zinc ion-binding activity |
| W01F3.2 | Unknown |
| nhr-11 | Nuclear hormone receptor |
| F26G1.2 | Unknown |
| F48E3.2 | Predicted to enable transmembrane transporter activity |
| hpo-26 | Unknown, hypersensitive to pore forming toxin |
| R05H10.1 | Unknown |
| C08E8.4 | Involved in innate immune response |
| C11G10.1 | Unknown |
| Y73F4A.2 | Unknown, DOMON domain containing |
| bigr-1 | Predicted to enable hydrolase activity |
| nlp-33 | Neuropeptide like, involved in innate immune response |
| far-3 | Predicted to enable lipid-binding activity |
| Genes that change in F1 progeny of all species exposed to both osmotic stress and P. vranovensis | |
| C30B5.6 | Unknown |
| hphd-1 | Predicted to enable hydroxyacid–oxoacid transhydrogenase activity. Ortholog of human ADHFE1 |
| C42D4.3 | Unknown, DB module and domain of unknown function DB |
| Genes that change in F1 progeny of all species exposed to osmotic stress | |
| ttr-15 | Transthyretin-like family |
| F08F3.4 | Predicted to enable catalytic activity. Involved in innate immune response.Ortholog of human TDH |
Table 2
Complete list of genes that exhibited a consistent and greater than twofold change in expression in the F1 progeny of parents exposed to P. vranovensisor osmotic stress in only species that intergenerationally adapted to stress.
Genes listed for P. vranovensis were identified by comparing genes that change consistently in C. elegans and C. kamaaina, but not C. briggsae. Genes listed for osmotic stress were identified by …
| Genes that change consistently in F1 progeny of only species that adapt to P. vranovensis | Predicted function |
|---|---|
| daf-18 | Lipid phosphatase, homologous to human PTEN tumor suppressor |
| gst-38 | Glutathione S-transferase |
| H04M03.3 | Predicted to enable oxidoreductase activity. |
| oops-1 | Oocyte partner of SPE-11 |
| F09G8.10 | Unknown |
| glb-1 | Globin -related |
| F57H12.6 | Unknown |
| elo-6 | Predicted to enable transferase activity, transferring acyl groups, ortholog of human ELOVL3 and ELOVL6 |
| cpr-5 | Predicted to enable cysteine-type peptidase activity |
| xpo-2 | Exportin involved in nuclear export, ortholog of human CSE1L |
| cysl-1 | Cysteine synthase known to be involved in adaptation to P. vranovensis |
| rhy-1 | Regulator of HIF-1 known to be involved in adaptation to P. vranovensis |
| cdc-25.1 | Homolog of human CDC25 phosphatase |
| imb-1 | Importin beta family, ortholog of human KPNB1 |
| VZK882L.2 | Unknown |
| cysl-2 | Cysteine synthase known to be involved in adaptation to P. vranovensis |
| cyk-7 | Involved in intercellular bridge organization |
| Genes that change consistently in F1 progeny of only species that adapt to osmotic stress | |
| T05F1.9 | Unknown |
| grl-21 | Unknown, Ground-like domain containing |
| gpdh-1 | Glycerol-3-phosphate dehydrogenase known to be involved in osmotic stress resposne |
| T22B7.3 | Amidinotransferase, ortholog of human DDAH1 and DDAH2 |
Table 3
Details of N. parisii doses employed.
| N. parisii dose | Plate concentration (spores/cm2) | Millions of spores used | |
|---|---|---|---|
| 6 cm plate | 10 cm plate | ||
| Low | ~32,000 | 2.5 | |
| High | ~88,000 | 2.5 | |
Additional files
-
Supplementary file 1
List of 7587 single-copy orthologous genes conserved among C. elegans, C. briggsae, C. kamaaina, and C. tropicalis.
- https://cdn.elifesciences.org/articles/73425/elife-73425-supp1-v2.xlsx
-
Supplementary file 2
Expression of single-copy orthologous genes in F1 progeny of animals exposed to P. vranovensis.
- https://cdn.elifesciences.org/articles/73425/elife-73425-supp2-v2.xlsx
-
Supplementary file 3
Expression of single-copy orthologous genes in F1 progeny of animals exposed to osmotic stress.
- https://cdn.elifesciences.org/articles/73425/elife-73425-supp3-v2.xlsx
-
Supplementary file 4
Expression of single-copy orthologous genes in F3 progeny of animals exposed to P. vranovensis and osmotic stress.
- https://cdn.elifesciences.org/articles/73425/elife-73425-supp4-v2.xlsx
-
Supplementary file 5
List of bacteria isolated from United Kingdom.
- https://cdn.elifesciences.org/articles/73425/elife-73425-supp5-v2.xlsx
-
Supplementary file 6
PCR sequences of Pseudomonas 15C5 16 S rRNA and rpoD.
- https://cdn.elifesciences.org/articles/73425/elife-73425-supp6-v2.txt
-
Supplementary file 7
Expression of single-copy orthologous genes in F1 progeny of C. elegans exposed to P. vranovensis, Pseudomonas sp. 15C5, Serratia plymuthica BUR1537, or Aeromonas sp. BIGb0469.
- https://cdn.elifesciences.org/articles/73425/elife-73425-supp7-v2.xlsx
-
Transparent reporting form
- https://cdn.elifesciences.org/articles/73425/elife-73425-transrepform1-v2.pdf
