Steroid hormone pathways coordinate developmental diapause and olfactory remodeling in Pristionchus pacificus
Abstract Developmental and behavioral plasticity allow animals to prioritize alternative genetic programs during fluctuating environments. Behavioral remodeling may be acute in animals that interact with host organisms, since reproductive adults and the developmentally arrested larvae often have dif...
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| Veröffentlicht in: | Genetics (Austin) 2021-06, Vol.218 (2) |
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| creator | Carstensen, Heather R Villalon, Reinard M Banerjee, Navonil Hallem, Elissa A Hong, Ray L |
| description | Abstract
Developmental and behavioral plasticity allow animals to prioritize alternative genetic programs during fluctuating environments. Behavioral remodeling may be acute in animals that interact with host organisms, since reproductive adults and the developmentally arrested larvae often have different ethological needs for chemical stimuli. To understand the genes that coordinate the development and host-seeking behavior, we used the entomophilic nematode Pristionchus pacificus to characterize dauer-constitutive mutants (Daf-c) that inappropriately enter developmental diapause to become dauer larvae. We found two Daf-c loci with dauer-constitutive and cuticle exsheathment phenotypes that can be rescued by the feeding of Δ7-dafachronic acid, and that are dependent on the conserved canonical steroid hormone receptor Ppa-DAF-12. Specifically at one locus, deletions in the sole hydroxysteroid dehydrogenase (HSD) in P. pacificus resulted in Daf-c phenotypes. Ppa-hsd-2 is expressed in the canal-associated neurons (CANs) and excretory cells whose homologous cells in Caenorhabditis elegans are not known to be involved in the dauer decision. While in wildtype only dauer larvae are attracted to host odors, hsd-2 mutant adults show enhanced attraction to the host beetle pheromone, along with ectopic activation of a marker for putative olfactory neurons, Ppa-odr-3. Surprisingly, this enhanced odor attraction acts independently of the Δ7-DA/DAF-12 module, suggesting that Ppa-HSD-2 may be responsible for several steroid hormone products involved in coordinating the dauer decision and host-seeking behavior in P. pacificus. |
| doi_str_mv | 10.1093/genetics/iyab071 |
| format | Article |
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Developmental and behavioral plasticity allow animals to prioritize alternative genetic programs during fluctuating environments. Behavioral remodeling may be acute in animals that interact with host organisms, since reproductive adults and the developmentally arrested larvae often have different ethological needs for chemical stimuli. To understand the genes that coordinate the development and host-seeking behavior, we used the entomophilic nematode Pristionchus pacificus to characterize dauer-constitutive mutants (Daf-c) that inappropriately enter developmental diapause to become dauer larvae. We found two Daf-c loci with dauer-constitutive and cuticle exsheathment phenotypes that can be rescued by the feeding of Δ7-dafachronic acid, and that are dependent on the conserved canonical steroid hormone receptor Ppa-DAF-12. Specifically at one locus, deletions in the sole hydroxysteroid dehydrogenase (HSD) in P. pacificus resulted in Daf-c phenotypes. Ppa-hsd-2 is expressed in the canal-associated neurons (CANs) and excretory cells whose homologous cells in Caenorhabditis elegans are not known to be involved in the dauer decision. While in wildtype only dauer larvae are attracted to host odors, hsd-2 mutant adults show enhanced attraction to the host beetle pheromone, along with ectopic activation of a marker for putative olfactory neurons, Ppa-odr-3. Surprisingly, this enhanced odor attraction acts independently of the Δ7-DA/DAF-12 module, suggesting that Ppa-HSD-2 may be responsible for several steroid hormone products involved in coordinating the dauer decision and host-seeking behavior in P. pacificus.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1093/genetics/iyab071</identifier><identifier>PMID: 33963848</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Adults ; Animal behavior ; Animals ; Attraction ; Behavior ; Behavioral plasticity ; Chemical stimuli ; Cholestenes - metabolism ; Coleoptera - metabolism ; Coleoptera - parasitology ; Developmental and Behavioral Genetics ; Diapause ; Diapause - genetics ; Gene Expression Regulation, Developmental ; Genetic Loci ; Genetic programs ; Genetics ; Helminth Proteins - genetics ; Helminth Proteins - metabolism ; Homology ; Host searching behavior ; Host-Seeking Behavior ; Hydroxysteroids ; Larva ; Larvae ; Loci ; Metabolic Networks and Pathways - genetics ; Mutants ; Mutation ; Nematodes ; Neuroethology ; Neurons ; Neurons - metabolism ; Odorants ; Odors ; Olfactory neurons ; Phenotypes ; Pheromones - metabolism ; Pristionchus pacificus ; Receptors, Steroid - genetics ; Receptors, Steroid - metabolism ; Rhabditida - genetics ; Rhabditida - growth & development ; Smell - genetics ; Steroids</subject><ispartof>Genetics (Austin), 2021-06, Vol.218 (2)</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. All rights reserved. For permissions, please email: journals.permissions@oup.com 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. All rights reserved. For permissions, please email: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-12addfdff7761771c3027643a79f6035eff97ec170f0bf7ad2bdb251560b586d3</citedby><cites>FETCH-LOGICAL-c526t-12addfdff7761771c3027643a79f6035eff97ec170f0bf7ad2bdb251560b586d3</cites><orcidid>0000-0003-1870-8659 ; 0000-0003-0260-3174</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,1584,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33963848$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Sundaram, M</contributor><creatorcontrib>Carstensen, Heather R</creatorcontrib><creatorcontrib>Villalon, Reinard M</creatorcontrib><creatorcontrib>Banerjee, Navonil</creatorcontrib><creatorcontrib>Hallem, Elissa A</creatorcontrib><creatorcontrib>Hong, Ray L</creatorcontrib><title>Steroid hormone pathways coordinate developmental diapause and olfactory remodeling in Pristionchus pacificus</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>Abstract
Developmental and behavioral plasticity allow animals to prioritize alternative genetic programs during fluctuating environments. Behavioral remodeling may be acute in animals that interact with host organisms, since reproductive adults and the developmentally arrested larvae often have different ethological needs for chemical stimuli. To understand the genes that coordinate the development and host-seeking behavior, we used the entomophilic nematode Pristionchus pacificus to characterize dauer-constitutive mutants (Daf-c) that inappropriately enter developmental diapause to become dauer larvae. We found two Daf-c loci with dauer-constitutive and cuticle exsheathment phenotypes that can be rescued by the feeding of Δ7-dafachronic acid, and that are dependent on the conserved canonical steroid hormone receptor Ppa-DAF-12. Specifically at one locus, deletions in the sole hydroxysteroid dehydrogenase (HSD) in P. pacificus resulted in Daf-c phenotypes. Ppa-hsd-2 is expressed in the canal-associated neurons (CANs) and excretory cells whose homologous cells in Caenorhabditis elegans are not known to be involved in the dauer decision. While in wildtype only dauer larvae are attracted to host odors, hsd-2 mutant adults show enhanced attraction to the host beetle pheromone, along with ectopic activation of a marker for putative olfactory neurons, Ppa-odr-3. Surprisingly, this enhanced odor attraction acts independently of the Δ7-DA/DAF-12 module, suggesting that Ppa-HSD-2 may be responsible for several steroid hormone products involved in coordinating the dauer decision and host-seeking behavior in P. pacificus.</description><subject>Adults</subject><subject>Animal behavior</subject><subject>Animals</subject><subject>Attraction</subject><subject>Behavior</subject><subject>Behavioral plasticity</subject><subject>Chemical stimuli</subject><subject>Cholestenes - metabolism</subject><subject>Coleoptera - metabolism</subject><subject>Coleoptera - parasitology</subject><subject>Developmental and Behavioral Genetics</subject><subject>Diapause</subject><subject>Diapause - genetics</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genetic Loci</subject><subject>Genetic programs</subject><subject>Genetics</subject><subject>Helminth Proteins - genetics</subject><subject>Helminth Proteins - metabolism</subject><subject>Homology</subject><subject>Host searching behavior</subject><subject>Host-Seeking Behavior</subject><subject>Hydroxysteroids</subject><subject>Larva</subject><subject>Larvae</subject><subject>Loci</subject><subject>Metabolic Networks and Pathways - genetics</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Nematodes</subject><subject>Neuroethology</subject><subject>Neurons</subject><subject>Neurons - metabolism</subject><subject>Odorants</subject><subject>Odors</subject><subject>Olfactory neurons</subject><subject>Phenotypes</subject><subject>Pheromones - metabolism</subject><subject>Pristionchus pacificus</subject><subject>Receptors, Steroid - genetics</subject><subject>Receptors, Steroid - metabolism</subject><subject>Rhabditida - genetics</subject><subject>Rhabditida - growth & development</subject><subject>Smell - genetics</subject><subject>Steroids</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1r3DAQhkVIadK095yKIJdC2UYflmRfAiH0CwItJD0LWRrtKtiSI8kp--_rsJuQ9tLTDMwzDzO8CJ1S8omSjp-vIUINtpyHremJogfomHYNXzHJ6eGL_gi9KeWOECI70b5GR5x3krdNe4zGmwo5BYc3KY8pAp5M3fw224JtStmFaCpgBw8wpGmEWM2AXTCTmQtgEx1Ogze2przFGcbkYAhxjUPEP3MoNaRoN3NZnDb4YOfyFr3yZijwbl9P0K8vn2-vvq2uf3z9fnV5vbKCybqizDjnnfdKSaoUtZwwJRtuVOcl4QK87xRYqognvVfGsd71TFAhSS9a6fgJuth5p7kfwdnl8GwGPeUwmrzVyQT99ySGjV6nB90yJngjFsGHvSCn-xlK1WMoFobBREhz0UywhgtFWrqgZ_-gd2nOcXlvoVSnGqGaR4rsKJtTKRn88zGU6Mcs9VOWep_lsvL-5RPPC0_hLcDHHZDm6f-6P82DsNI</recordid><startdate>20210624</startdate><enddate>20210624</enddate><creator>Carstensen, Heather R</creator><creator>Villalon, Reinard M</creator><creator>Banerjee, Navonil</creator><creator>Hallem, Elissa A</creator><creator>Hong, Ray L</creator><general>Oxford University Press</general><general>Genetics Society of America</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1870-8659</orcidid><orcidid>https://orcid.org/0000-0003-0260-3174</orcidid></search><sort><creationdate>20210624</creationdate><title>Steroid hormone pathways coordinate developmental diapause and olfactory remodeling in Pristionchus pacificus</title><author>Carstensen, Heather R ; Villalon, Reinard M ; Banerjee, Navonil ; Hallem, Elissa A ; Hong, Ray L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-12addfdff7761771c3027643a79f6035eff97ec170f0bf7ad2bdb251560b586d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adults</topic><topic>Animal behavior</topic><topic>Animals</topic><topic>Attraction</topic><topic>Behavior</topic><topic>Behavioral plasticity</topic><topic>Chemical stimuli</topic><topic>Cholestenes - metabolism</topic><topic>Coleoptera - metabolism</topic><topic>Coleoptera - parasitology</topic><topic>Developmental and Behavioral Genetics</topic><topic>Diapause</topic><topic>Diapause - genetics</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genetic Loci</topic><topic>Genetic programs</topic><topic>Genetics</topic><topic>Helminth Proteins - genetics</topic><topic>Helminth Proteins - metabolism</topic><topic>Homology</topic><topic>Host searching behavior</topic><topic>Host-Seeking Behavior</topic><topic>Hydroxysteroids</topic><topic>Larva</topic><topic>Larvae</topic><topic>Loci</topic><topic>Metabolic Networks and Pathways - genetics</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Nematodes</topic><topic>Neuroethology</topic><topic>Neurons</topic><topic>Neurons - metabolism</topic><topic>Odorants</topic><topic>Odors</topic><topic>Olfactory neurons</topic><topic>Phenotypes</topic><topic>Pheromones - metabolism</topic><topic>Pristionchus pacificus</topic><topic>Receptors, Steroid - genetics</topic><topic>Receptors, Steroid - metabolism</topic><topic>Rhabditida - genetics</topic><topic>Rhabditida - growth & development</topic><topic>Smell - genetics</topic><topic>Steroids</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Carstensen, Heather R</creatorcontrib><creatorcontrib>Villalon, Reinard M</creatorcontrib><creatorcontrib>Banerjee, Navonil</creatorcontrib><creatorcontrib>Hallem, Elissa A</creatorcontrib><creatorcontrib>Hong, Ray L</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>University Readers</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Carstensen, Heather R</au><au>Villalon, Reinard M</au><au>Banerjee, Navonil</au><au>Hallem, Elissa A</au><au>Hong, Ray L</au><au>Sundaram, M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Steroid hormone pathways coordinate developmental diapause and olfactory remodeling in Pristionchus pacificus</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2021-06-24</date><risdate>2021</risdate><volume>218</volume><issue>2</issue><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><abstract>Abstract
Developmental and behavioral plasticity allow animals to prioritize alternative genetic programs during fluctuating environments. Behavioral remodeling may be acute in animals that interact with host organisms, since reproductive adults and the developmentally arrested larvae often have different ethological needs for chemical stimuli. To understand the genes that coordinate the development and host-seeking behavior, we used the entomophilic nematode Pristionchus pacificus to characterize dauer-constitutive mutants (Daf-c) that inappropriately enter developmental diapause to become dauer larvae. We found two Daf-c loci with dauer-constitutive and cuticle exsheathment phenotypes that can be rescued by the feeding of Δ7-dafachronic acid, and that are dependent on the conserved canonical steroid hormone receptor Ppa-DAF-12. Specifically at one locus, deletions in the sole hydroxysteroid dehydrogenase (HSD) in P. pacificus resulted in Daf-c phenotypes. Ppa-hsd-2 is expressed in the canal-associated neurons (CANs) and excretory cells whose homologous cells in Caenorhabditis elegans are not known to be involved in the dauer decision. While in wildtype only dauer larvae are attracted to host odors, hsd-2 mutant adults show enhanced attraction to the host beetle pheromone, along with ectopic activation of a marker for putative olfactory neurons, Ppa-odr-3. Surprisingly, this enhanced odor attraction acts independently of the Δ7-DA/DAF-12 module, suggesting that Ppa-HSD-2 may be responsible for several steroid hormone products involved in coordinating the dauer decision and host-seeking behavior in P. pacificus.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>33963848</pmid><doi>10.1093/genetics/iyab071</doi><orcidid>https://orcid.org/0000-0003-1870-8659</orcidid><orcidid>https://orcid.org/0000-0003-0260-3174</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Oxford University Press Journals; MEDLINE; Alma/SFX Local Collection; EZB Electronic Journals Library |
| subjects | Adults Animal behavior Animals Attraction Behavior Behavioral plasticity Chemical stimuli Cholestenes - metabolism Coleoptera - metabolism Coleoptera - parasitology Developmental and Behavioral Genetics Diapause Diapause - genetics Gene Expression Regulation, Developmental Genetic Loci Genetic programs Genetics Helminth Proteins - genetics Helminth Proteins - metabolism Homology Host searching behavior Host-Seeking Behavior Hydroxysteroids Larva Larvae Loci Metabolic Networks and Pathways - genetics Mutants Mutation Nematodes Neuroethology Neurons Neurons - metabolism Odorants Odors Olfactory neurons Phenotypes Pheromones - metabolism Pristionchus pacificus Receptors, Steroid - genetics Receptors, Steroid - metabolism Rhabditida - genetics Rhabditida - growth & development Smell - genetics Steroids |
| title | Steroid hormone pathways coordinate developmental diapause and olfactory remodeling in Pristionchus pacificus |
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