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Differential regulation of host plant adaptive genes in Pieris butterflies exposed to a range of glucosinolate profiles in their host plants
Specialist herbivores have often evolved highly sophisticated mechanisms to counteract defenses mediated by major plant secondary-metabolites. Plant species of the herbivore host range often display high chemical diversity and it is not well understood how specialist herbivores respond to this chemi...
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| Published in: | Scientific reports 2019-05, Vol.9 (1), p.7256, Article 7256 |
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| creator | Okamura, Yu Sato, Ai Tsuzuki, Natsumi Sawada, Yuji Hirai, Masami Yokota Heidel-Fischer, Hanna Reichelt, Michael Murakami, Masashi Vogel, Heiko |
| description | Specialist herbivores have often evolved highly sophisticated mechanisms to counteract defenses mediated by major plant secondary-metabolites. Plant species of the herbivore host range often display high chemical diversity and it is not well understood how specialist herbivores respond to this chemical diversity.
Pieris
larvae overcome toxic products from glucosinolate hydrolysis, the major chemical defense of their Brassicaceae hosts, by expressing nitrile-specifier proteins (NSP) in their gut. Furthermore,
Pieris
butterflies possess so-called major allergen (MA) proteins, which are multi-domain variants of a single domain major allergen (SDMA) protein expressed in the guts of Lepidopteran larvae. Here we show that
Pieris
larvae fine-tune NSP and MA gene expression depending on the glucosinolate profiles of their Brassicaceae hosts. Although the role of MA is not yet fully understood, the expression levels of NSP and MA in larvae that fed on plants whose glucosinolate composition varied was dramatically changed, whereas levels of SDMA expression remained unchanged. In addition, we found a similar regulation pattern among these genes in larvae feeding on
Arabidopsis
mutants with different glucosinolate profiles. Our results demonstrate that
Pieris
larvae appear to use different host plant adaptive genes to overcome a wide range of glucosinolate profiles in their host plants. |
| doi_str_mv | 10.1038/s41598-019-43703-8 |
| format | article |
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Pieris
larvae overcome toxic products from glucosinolate hydrolysis, the major chemical defense of their Brassicaceae hosts, by expressing nitrile-specifier proteins (NSP) in their gut. Furthermore,
Pieris
butterflies possess so-called major allergen (MA) proteins, which are multi-domain variants of a single domain major allergen (SDMA) protein expressed in the guts of Lepidopteran larvae. Here we show that
Pieris
larvae fine-tune NSP and MA gene expression depending on the glucosinolate profiles of their Brassicaceae hosts. Although the role of MA is not yet fully understood, the expression levels of NSP and MA in larvae that fed on plants whose glucosinolate composition varied was dramatically changed, whereas levels of SDMA expression remained unchanged. In addition, we found a similar regulation pattern among these genes in larvae feeding on
Arabidopsis
mutants with different glucosinolate profiles. Our results demonstrate that
Pieris
larvae appear to use different host plant adaptive genes to overcome a wide range of glucosinolate profiles in their host plants.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-019-43703-8</identifier><identifier>PMID: 31076616</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>101/58 ; 38/91 ; 631/158/2452 ; 631/158/670 ; 631/181/2481 ; Adaptation, Biological - genetics ; Allergens ; Allergens - genetics ; Animals ; Arabidopsis - genetics ; Brassicaceae ; Butterflies & moths ; Butterflies - genetics ; Chemical defense ; Ericaceae - genetics ; Gene expression ; Gene regulation ; Genes, Plant - genetics ; Glucosinolates - genetics ; Herbivores ; Host plants ; Host range ; Humanities and Social Sciences ; Larva - genetics ; Larvae ; Metabolites ; multidisciplinary ; Plant species ; Science ; Science (multidisciplinary)</subject><ispartof>Scientific reports, 2019-05, Vol.9 (1), p.7256, Article 7256</ispartof><rights>The Author(s) 2019</rights><rights>The Author(s) 2019. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c511t-d0c141fba883dc0b35edcb1ed8a2ce8dd30bbd4798dcc2be30b6aafd986dcc473</citedby><cites>FETCH-LOGICAL-c511t-d0c141fba883dc0b35edcb1ed8a2ce8dd30bbd4798dcc2be30b6aafd986dcc473</cites><orcidid>0000-0002-6691-6500 ; 0000-0001-9821-7731</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2222924995/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2222924995?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31076616$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Okamura, Yu</creatorcontrib><creatorcontrib>Sato, Ai</creatorcontrib><creatorcontrib>Tsuzuki, Natsumi</creatorcontrib><creatorcontrib>Sawada, Yuji</creatorcontrib><creatorcontrib>Hirai, Masami Yokota</creatorcontrib><creatorcontrib>Heidel-Fischer, Hanna</creatorcontrib><creatorcontrib>Reichelt, Michael</creatorcontrib><creatorcontrib>Murakami, Masashi</creatorcontrib><creatorcontrib>Vogel, Heiko</creatorcontrib><title>Differential regulation of host plant adaptive genes in Pieris butterflies exposed to a range of glucosinolate profiles in their host plants</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Specialist herbivores have often evolved highly sophisticated mechanisms to counteract defenses mediated by major plant secondary-metabolites. Plant species of the herbivore host range often display high chemical diversity and it is not well understood how specialist herbivores respond to this chemical diversity.
Pieris
larvae overcome toxic products from glucosinolate hydrolysis, the major chemical defense of their Brassicaceae hosts, by expressing nitrile-specifier proteins (NSP) in their gut. Furthermore,
Pieris
butterflies possess so-called major allergen (MA) proteins, which are multi-domain variants of a single domain major allergen (SDMA) protein expressed in the guts of Lepidopteran larvae. Here we show that
Pieris
larvae fine-tune NSP and MA gene expression depending on the glucosinolate profiles of their Brassicaceae hosts. Although the role of MA is not yet fully understood, the expression levels of NSP and MA in larvae that fed on plants whose glucosinolate composition varied was dramatically changed, whereas levels of SDMA expression remained unchanged. In addition, we found a similar regulation pattern among these genes in larvae feeding on
Arabidopsis
mutants with different glucosinolate profiles. Our results demonstrate that
Pieris
larvae appear to use different host plant adaptive genes to overcome a wide range of glucosinolate profiles in their host plants.</description><subject>101/58</subject><subject>38/91</subject><subject>631/158/2452</subject><subject>631/158/670</subject><subject>631/181/2481</subject><subject>Adaptation, Biological - genetics</subject><subject>Allergens</subject><subject>Allergens - genetics</subject><subject>Animals</subject><subject>Arabidopsis - genetics</subject><subject>Brassicaceae</subject><subject>Butterflies & moths</subject><subject>Butterflies - genetics</subject><subject>Chemical defense</subject><subject>Ericaceae - genetics</subject><subject>Gene expression</subject><subject>Gene regulation</subject><subject>Genes, Plant - genetics</subject><subject>Glucosinolates - genetics</subject><subject>Herbivores</subject><subject>Host plants</subject><subject>Host range</subject><subject>Humanities and Social Sciences</subject><subject>Larva - genetics</subject><subject>Larvae</subject><subject>Metabolites</subject><subject>multidisciplinary</subject><subject>Plant species</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNp9Uctu1TAQtRCIVqU_wKKyxDrUjyTX3lSqCqWVKsEC1pZjj3NdpXZqOxX8Ax9d36aUy4bZ2J4558x4DkLvKflICRenuaWdFA2hsmn5hvBGvEKHjLRdwzhjr_fuB-g451tSo2OypfItOuCUbPqe9ofo9yfvHCQIxesJJxiXSRcfA44Ob2MueJ50KFhbPRf_AHiEABn7gL95SD7jYSkFkpt8zcLPOWawuESscdJhhJ3KOC0mZh9iFQY8p-j8tEqULfi01yW_Q2-cnjIcP59H6Mfl5-8XV83N1y_XF-c3jekoLY0lhrbUDVoIbg0ZeAfWDBSs0MyAsJaTYbDtRgprDBugPnutnZWir4l2w4_Q2ao7L8Nd5dbfJz2pOfk7nX6pqL36txL8Vo3xQfVdXRzvqsCHZ4EU7xfIRd3GJYU6s2I1JGul3KHYijIp5pzAvXSgRO1MVKuJqpqonkxUopJO9md7ofyxrAL4Csi1VHec_vb-j-wjdbWteA</recordid><startdate>20190510</startdate><enddate>20190510</enddate><creator>Okamura, Yu</creator><creator>Sato, Ai</creator><creator>Tsuzuki, Natsumi</creator><creator>Sawada, Yuji</creator><creator>Hirai, Masami Yokota</creator><creator>Heidel-Fischer, Hanna</creator><creator>Reichelt, Michael</creator><creator>Murakami, Masashi</creator><creator>Vogel, Heiko</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6691-6500</orcidid><orcidid>https://orcid.org/0000-0001-9821-7731</orcidid></search><sort><creationdate>20190510</creationdate><title>Differential regulation of host plant adaptive genes in Pieris butterflies exposed to a range of glucosinolate profiles in their host plants</title><author>Okamura, Yu ; Sato, Ai ; Tsuzuki, Natsumi ; Sawada, Yuji ; Hirai, Masami Yokota ; Heidel-Fischer, Hanna ; Reichelt, Michael ; Murakami, Masashi ; Vogel, Heiko</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c511t-d0c141fba883dc0b35edcb1ed8a2ce8dd30bbd4798dcc2be30b6aafd986dcc473</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>101/58</topic><topic>38/91</topic><topic>631/158/2452</topic><topic>631/158/670</topic><topic>631/181/2481</topic><topic>Adaptation, Biological - 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Plant species of the herbivore host range often display high chemical diversity and it is not well understood how specialist herbivores respond to this chemical diversity.
Pieris
larvae overcome toxic products from glucosinolate hydrolysis, the major chemical defense of their Brassicaceae hosts, by expressing nitrile-specifier proteins (NSP) in their gut. Furthermore,
Pieris
butterflies possess so-called major allergen (MA) proteins, which are multi-domain variants of a single domain major allergen (SDMA) protein expressed in the guts of Lepidopteran larvae. Here we show that
Pieris
larvae fine-tune NSP and MA gene expression depending on the glucosinolate profiles of their Brassicaceae hosts. Although the role of MA is not yet fully understood, the expression levels of NSP and MA in larvae that fed on plants whose glucosinolate composition varied was dramatically changed, whereas levels of SDMA expression remained unchanged. In addition, we found a similar regulation pattern among these genes in larvae feeding on
Arabidopsis
mutants with different glucosinolate profiles. Our results demonstrate that
Pieris
larvae appear to use different host plant adaptive genes to overcome a wide range of glucosinolate profiles in their host plants.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31076616</pmid><doi>10.1038/s41598-019-43703-8</doi><orcidid>https://orcid.org/0000-0002-6691-6500</orcidid><orcidid>https://orcid.org/0000-0001-9821-7731</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 101/58 38/91 631/158/2452 631/158/670 631/181/2481 Adaptation, Biological - genetics Allergens Allergens - genetics Animals Arabidopsis - genetics Brassicaceae Butterflies & moths Butterflies - genetics Chemical defense Ericaceae - genetics Gene expression Gene regulation Genes, Plant - genetics Glucosinolates - genetics Herbivores Host plants Host range Humanities and Social Sciences Larva - genetics Larvae Metabolites multidisciplinary Plant species Science Science (multidisciplinary) |
| title | Differential regulation of host plant adaptive genes in Pieris butterflies exposed to a range of glucosinolate profiles in their host plants |
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