Two hybrid histidine kinases, TcsB and the phytochrome FphA, are involved in temperature sensing in Aspergillus nidulans
Summary The adaptation of microorganisms to different temperatures is an advantage in habitats with steadily changing conditions and raises the question about temperature sensing. Here we show that in the filamentous fungus Aspergillus nidulans, the hybrid histidine kinase TcsB and phytochrome are i...
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Veröffentlicht in: | Molecular microbiology 2019-12, Vol.112 (6), p.1814-1830 |
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container_title | Molecular microbiology |
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creator | Yu, Zhenzhong Ali, Arin Igbalajobi, Olumuyiwa Ayokunle Streng, Christian Leister, Kai Krauß, Norbert Lamparter, Tilman Fischer, Reinhard |
description | Summary
The adaptation of microorganisms to different temperatures is an advantage in habitats with steadily changing conditions and raises the question about temperature sensing. Here we show that in the filamentous fungus Aspergillus nidulans, the hybrid histidine kinase TcsB and phytochrome are involved in temperature‐induced gene transcription. Temperature‐activated phytochrome fed the signal into the HOG MAP kinase pathway. There is evidence that the photoreceptor phytochrome fulfills a temperature sensory role in plants and bacteria. The effects in plants are based on dark reversion from the active form of phytochrome, Pfr, to the inactive form, Pr. Elevated temperature leads to higher dark reversion rates, and hence, temperature sensing depends on light. In A. nidulans and in Alternaria alternata, the temperature response was light‐independent. In order to understand the primary temperature response of phytochrome, we performed spectral analyses of recombinant FphA from both fungi. Spectral properties after heat stress resembled the spectrum of free biliverdin, suggesting conformational changes and a softening of the binding pocket of phytochrome, possibly mimicking photoactivation. We propose a novel function for fungal phytochrome as temperature sensor.
Phytochrome has been extensively characterized as red‐light sensor in plants. Recently, it was also discovered in bacteria and fungi. In Aspergillus nidulans and Alternaria alternata, phytochrome is tightly connected to the central stress‐sensing signaling HOG MAP kinase pathway. Here we show that in both fungi, phytochrome plays a dual role in light and in temperature sensing. The temperature‐sensing function of phytochrome was independent of light. We speculate that temperature sensing could be the ancient function of phytochromes. |
doi_str_mv | 10.1111/mmi.14395 |
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The adaptation of microorganisms to different temperatures is an advantage in habitats with steadily changing conditions and raises the question about temperature sensing. Here we show that in the filamentous fungus Aspergillus nidulans, the hybrid histidine kinase TcsB and phytochrome are involved in temperature‐induced gene transcription. Temperature‐activated phytochrome fed the signal into the HOG MAP kinase pathway. There is evidence that the photoreceptor phytochrome fulfills a temperature sensory role in plants and bacteria. The effects in plants are based on dark reversion from the active form of phytochrome, Pfr, to the inactive form, Pr. Elevated temperature leads to higher dark reversion rates, and hence, temperature sensing depends on light. In A. nidulans and in Alternaria alternata, the temperature response was light‐independent. In order to understand the primary temperature response of phytochrome, we performed spectral analyses of recombinant FphA from both fungi. Spectral properties after heat stress resembled the spectrum of free biliverdin, suggesting conformational changes and a softening of the binding pocket of phytochrome, possibly mimicking photoactivation. We propose a novel function for fungal phytochrome as temperature sensor.
Phytochrome has been extensively characterized as red‐light sensor in plants. Recently, it was also discovered in bacteria and fungi. In Aspergillus nidulans and Alternaria alternata, phytochrome is tightly connected to the central stress‐sensing signaling HOG MAP kinase pathway. Here we show that in both fungi, phytochrome plays a dual role in light and in temperature sensing. The temperature‐sensing function of phytochrome was independent of light. We speculate that temperature sensing could be the ancient function of phytochromes.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.14395</identifier><identifier>PMID: 31556180</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Aspergillus nidulans ; Biliverdin ; Detection ; Fungi ; Heat stress ; Heat tolerance ; High temperature ; Histidine ; Histidine kinase ; Kinases ; Light effects ; MAP kinase ; Microorganisms ; Mimicry ; Photoactivation ; Reversion ; Temperature ; Temperature sensors ; Transcription</subject><ispartof>Molecular microbiology, 2019-12, Vol.112 (6), p.1814-1830</ispartof><rights>2019 John Wiley & Sons Ltd</rights><rights>2019 John Wiley & Sons Ltd.</rights><rights>Copyright © 2019 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3885-c3f5e644a5fc1c7729d771c6f56a92ce7805dc5867b43906fdbbcd87ca0718753</citedby><cites>FETCH-LOGICAL-c3885-c3f5e644a5fc1c7729d771c6f56a92ce7805dc5867b43906fdbbcd87ca0718753</cites><orcidid>0000-0002-6704-2569</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmmi.14395$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmmi.14395$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31556180$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yu, Zhenzhong</creatorcontrib><creatorcontrib>Ali, Arin</creatorcontrib><creatorcontrib>Igbalajobi, Olumuyiwa Ayokunle</creatorcontrib><creatorcontrib>Streng, Christian</creatorcontrib><creatorcontrib>Leister, Kai</creatorcontrib><creatorcontrib>Krauß, Norbert</creatorcontrib><creatorcontrib>Lamparter, Tilman</creatorcontrib><creatorcontrib>Fischer, Reinhard</creatorcontrib><title>Two hybrid histidine kinases, TcsB and the phytochrome FphA, are involved in temperature sensing in Aspergillus nidulans</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
The adaptation of microorganisms to different temperatures is an advantage in habitats with steadily changing conditions and raises the question about temperature sensing. Here we show that in the filamentous fungus Aspergillus nidulans, the hybrid histidine kinase TcsB and phytochrome are involved in temperature‐induced gene transcription. Temperature‐activated phytochrome fed the signal into the HOG MAP kinase pathway. There is evidence that the photoreceptor phytochrome fulfills a temperature sensory role in plants and bacteria. The effects in plants are based on dark reversion from the active form of phytochrome, Pfr, to the inactive form, Pr. Elevated temperature leads to higher dark reversion rates, and hence, temperature sensing depends on light. In A. nidulans and in Alternaria alternata, the temperature response was light‐independent. In order to understand the primary temperature response of phytochrome, we performed spectral analyses of recombinant FphA from both fungi. Spectral properties after heat stress resembled the spectrum of free biliverdin, suggesting conformational changes and a softening of the binding pocket of phytochrome, possibly mimicking photoactivation. We propose a novel function for fungal phytochrome as temperature sensor.
Phytochrome has been extensively characterized as red‐light sensor in plants. Recently, it was also discovered in bacteria and fungi. In Aspergillus nidulans and Alternaria alternata, phytochrome is tightly connected to the central stress‐sensing signaling HOG MAP kinase pathway. Here we show that in both fungi, phytochrome plays a dual role in light and in temperature sensing. The temperature‐sensing function of phytochrome was independent of light. We speculate that temperature sensing could be the ancient function of phytochromes.</description><subject>Aspergillus nidulans</subject><subject>Biliverdin</subject><subject>Detection</subject><subject>Fungi</subject><subject>Heat stress</subject><subject>Heat tolerance</subject><subject>High temperature</subject><subject>Histidine</subject><subject>Histidine kinase</subject><subject>Kinases</subject><subject>Light effects</subject><subject>MAP kinase</subject><subject>Microorganisms</subject><subject>Mimicry</subject><subject>Photoactivation</subject><subject>Reversion</subject><subject>Temperature</subject><subject>Temperature sensors</subject><subject>Transcription</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp1kU1r3DAQhkVoSTZpD_0DRdBLA9lEH6sPH7eh-YCEXrbQm5ClcazElh3JTrr_vko37aHQOcwMLw8vw7wIfaDklJY66_twSle8EntoQbkUS1YJ_QYtSCXIkmv24wAd5nxPCOVE8n10wKkQkmqyQD83zwNut3UKHrchT8GHCPghRJshn-CNy1-wjR5PLeCx3U6Da9PQA74Y2_UJtglwiE9D9wS-LHiCfoRkp7noGWIO8e5FXuei3oWumzOOwc-djfkdetvYLsP713mEvl983ZxfLW--XV6fr2-WjmstSm8EyNXKisZRpxSrvFLUyUZIWzEHShPhndBS1eUBRDa-rp3XylmiqFaCH6HPO98xDY8z5Mn0ITvoyg0wzNkwVmm6UlrLgn76B70f5hTLdYZxximjXNBCHe8ol4acEzRmTKG3aWsoMS9xmBKH-R1HYT--Os51D_4v-ef_BTjbAc-hg-3_nczt7fXO8heTZ5Si</recordid><startdate>201912</startdate><enddate>201912</enddate><creator>Yu, Zhenzhong</creator><creator>Ali, Arin</creator><creator>Igbalajobi, Olumuyiwa Ayokunle</creator><creator>Streng, Christian</creator><creator>Leister, Kai</creator><creator>Krauß, Norbert</creator><creator>Lamparter, Tilman</creator><creator>Fischer, Reinhard</creator><general>Blackwell Publishing Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-6704-2569</orcidid></search><sort><creationdate>201912</creationdate><title>Two hybrid histidine kinases, TcsB and the phytochrome FphA, are involved in temperature sensing in Aspergillus nidulans</title><author>Yu, Zhenzhong ; Ali, Arin ; Igbalajobi, Olumuyiwa Ayokunle ; Streng, Christian ; Leister, Kai ; Krauß, Norbert ; Lamparter, Tilman ; Fischer, Reinhard</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3885-c3f5e644a5fc1c7729d771c6f56a92ce7805dc5867b43906fdbbcd87ca0718753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Aspergillus nidulans</topic><topic>Biliverdin</topic><topic>Detection</topic><topic>Fungi</topic><topic>Heat stress</topic><topic>Heat tolerance</topic><topic>High temperature</topic><topic>Histidine</topic><topic>Histidine kinase</topic><topic>Kinases</topic><topic>Light effects</topic><topic>MAP kinase</topic><topic>Microorganisms</topic><topic>Mimicry</topic><topic>Photoactivation</topic><topic>Reversion</topic><topic>Temperature</topic><topic>Temperature sensors</topic><topic>Transcription</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yu, Zhenzhong</creatorcontrib><creatorcontrib>Ali, Arin</creatorcontrib><creatorcontrib>Igbalajobi, Olumuyiwa Ayokunle</creatorcontrib><creatorcontrib>Streng, Christian</creatorcontrib><creatorcontrib>Leister, Kai</creatorcontrib><creatorcontrib>Krauß, Norbert</creatorcontrib><creatorcontrib>Lamparter, Tilman</creatorcontrib><creatorcontrib>Fischer, Reinhard</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yu, Zhenzhong</au><au>Ali, Arin</au><au>Igbalajobi, Olumuyiwa Ayokunle</au><au>Streng, Christian</au><au>Leister, Kai</au><au>Krauß, Norbert</au><au>Lamparter, Tilman</au><au>Fischer, Reinhard</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Two hybrid histidine kinases, TcsB and the phytochrome FphA, are involved in temperature sensing in Aspergillus nidulans</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2019-12</date><risdate>2019</risdate><volume>112</volume><issue>6</issue><spage>1814</spage><epage>1830</epage><pages>1814-1830</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
The adaptation of microorganisms to different temperatures is an advantage in habitats with steadily changing conditions and raises the question about temperature sensing. Here we show that in the filamentous fungus Aspergillus nidulans, the hybrid histidine kinase TcsB and phytochrome are involved in temperature‐induced gene transcription. Temperature‐activated phytochrome fed the signal into the HOG MAP kinase pathway. There is evidence that the photoreceptor phytochrome fulfills a temperature sensory role in plants and bacteria. The effects in plants are based on dark reversion from the active form of phytochrome, Pfr, to the inactive form, Pr. Elevated temperature leads to higher dark reversion rates, and hence, temperature sensing depends on light. In A. nidulans and in Alternaria alternata, the temperature response was light‐independent. In order to understand the primary temperature response of phytochrome, we performed spectral analyses of recombinant FphA from both fungi. Spectral properties after heat stress resembled the spectrum of free biliverdin, suggesting conformational changes and a softening of the binding pocket of phytochrome, possibly mimicking photoactivation. We propose a novel function for fungal phytochrome as temperature sensor.
Phytochrome has been extensively characterized as red‐light sensor in plants. Recently, it was also discovered in bacteria and fungi. In Aspergillus nidulans and Alternaria alternata, phytochrome is tightly connected to the central stress‐sensing signaling HOG MAP kinase pathway. Here we show that in both fungi, phytochrome plays a dual role in light and in temperature sensing. The temperature‐sensing function of phytochrome was independent of light. We speculate that temperature sensing could be the ancient function of phytochromes.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>31556180</pmid><doi>10.1111/mmi.14395</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-6704-2569</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aspergillus nidulans Biliverdin Detection Fungi Heat stress Heat tolerance High temperature Histidine Histidine kinase Kinases Light effects MAP kinase Microorganisms Mimicry Photoactivation Reversion Temperature Temperature sensors Transcription |
title | Two hybrid histidine kinases, TcsB and the phytochrome FphA, are involved in temperature sensing in Aspergillus nidulans |
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