Photoexcited Cryptochrome 1 Interacts With SPCHLESS to Regulate Stomatal Development in Arabidopsis

ABSTRACT Stomata are epidermal openings that facilitate plant−atmosphere gas and water exchange during photosynthesis, respiration and water evaporation. SPEECHLESS (SPCH) is a master basic helix‐loop‐helix (bHLH) transcription factor that determines the initiation of stomatal development. It is kno...

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Veröffentlicht in:Plant, cell and environment cell and environment, 2025-01, Vol.48 (1), p.286-296
Hauptverfasser: Chen, Li, Cao, Xiaoli, Li, Yupeng, Liu, Minqing, Liu, Yao, Guan, Yan, Ruan, Jiaqi, Mao, Zhilei, Wang, Wenxiu, Yang, Hong‐Quan, Guo, Tongtong
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container_end_page 296
container_issue 1
container_start_page 286
container_title Plant, cell and environment
container_volume 48
creator Chen, Li
Cao, Xiaoli
Li, Yupeng
Liu, Minqing
Liu, Yao
Guan, Yan
Ruan, Jiaqi
Mao, Zhilei
Wang, Wenxiu
Yang, Hong‐Quan
Guo, Tongtong
description ABSTRACT Stomata are epidermal openings that facilitate plant−atmosphere gas and water exchange during photosynthesis, respiration and water evaporation. SPEECHLESS (SPCH) is a master basic helix‐loop‐helix (bHLH) transcription factor that determines the initiation of stomatal development. It is known that blue light promotes stomatal development through the blue light photoreceptor cryptochromes (CRYs, CRY1 and CRY2). Whether CRYs regulate stomatal development through directly modulating SPCH is unknown. Here, we demonstrate by biochemical studies that CRY1 physically interacts with SPCH in a blue light‐dependent manner. Genetic studies show that SPCH acts downstream of CRY1 to promote stomatal development in blue light. Furthermore, we show that CRY1 enhances the DNA‐binding activity of SPCH and promotes the expression of its target genes in blue light. These results suggest that the mechanism by which CRY1 promotes stomatal development involves positive regulation of the DNA‐binding activity of SPCH, which is likely mediated by blue light‐induced CRY1−SPCH interaction. The precise regulation of SPCH DNA‐binding activity by CRY1 may allow plants to optimize stomatal density and pattern according to ambient light conditions. Summary statement Blue light photoreceptor CRY1 directly interacts with SPCH in a blue light‐dependent manner to promote its DNA‐binding activity, leading to enhanced expression of SPCH‐target genes and eventual stomatal development in Arabidopsis.
doi_str_mv 10.1111/pce.15123
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SPEECHLESS (SPCH) is a master basic helix‐loop‐helix (bHLH) transcription factor that determines the initiation of stomatal development. It is known that blue light promotes stomatal development through the blue light photoreceptor cryptochromes (CRYs, CRY1 and CRY2). Whether CRYs regulate stomatal development through directly modulating SPCH is unknown. Here, we demonstrate by biochemical studies that CRY1 physically interacts with SPCH in a blue light‐dependent manner. Genetic studies show that SPCH acts downstream of CRY1 to promote stomatal development in blue light. Furthermore, we show that CRY1 enhances the DNA‐binding activity of SPCH and promotes the expression of its target genes in blue light. These results suggest that the mechanism by which CRY1 promotes stomatal development involves positive regulation of the DNA‐binding activity of SPCH, which is likely mediated by blue light‐induced CRY1−SPCH interaction. The precise regulation of SPCH DNA‐binding activity by CRY1 may allow plants to optimize stomatal density and pattern according to ambient light conditions. Summary statement Blue light photoreceptor CRY1 directly interacts with SPCH in a blue light‐dependent manner to promote its DNA‐binding activity, leading to enhanced expression of SPCH‐target genes and eventual stomatal development in Arabidopsis.</description><identifier>ISSN: 0140-7791</identifier><identifier>ISSN: 1365-3040</identifier><identifier>EISSN: 1365-3040</identifier><identifier>DOI: 10.1111/pce.15123</identifier><identifier>PMID: 39253954</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - growth &amp; development ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Basic Helix-Loop-Helix Transcription Factors - genetics ; Basic Helix-Loop-Helix Transcription Factors - metabolism ; Binding ; blue light ; Cryptochromes ; Cryptochromes - genetics ; Cryptochromes - metabolism ; Deoxyribonucleic acid ; DNA ; environment ; Evaporation ; Gene expression ; Gene Expression Regulation, Plant ; Gene regulation ; Light ; light signalling ; photoreceptor ; photoreceptors ; Photosynthesis ; Plant Stomata - growth &amp; development ; Plant Stomata - metabolism ; Plant Stomata - physiology ; Plant Stomata - radiation effects ; Protein Binding ; SPEECHLESS (SPCH) ; Stomata ; stomatal development ; transcription factors ; Water exchange</subject><ispartof>Plant, cell and environment, 2025-01, Vol.48 (1), p.286-296</ispartof><rights>2024 John Wiley &amp; Sons Ltd.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c2763-e47ab5eacaa544500cfb2882a08a0f6718fffadbc7fdde31e9e488528394a5893</cites><orcidid>0000-0003-0462-3929 ; 0000-0002-8988-3000 ; 0009-0002-9679-955X ; 0009-0007-9204-309X ; 0000-0001-6215-2665 ; 0009-0005-4292-8362</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%2Fpce.15123$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpce.15123$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39253954$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Li</creatorcontrib><creatorcontrib>Cao, Xiaoli</creatorcontrib><creatorcontrib>Li, Yupeng</creatorcontrib><creatorcontrib>Liu, Minqing</creatorcontrib><creatorcontrib>Liu, Yao</creatorcontrib><creatorcontrib>Guan, Yan</creatorcontrib><creatorcontrib>Ruan, Jiaqi</creatorcontrib><creatorcontrib>Mao, Zhilei</creatorcontrib><creatorcontrib>Wang, Wenxiu</creatorcontrib><creatorcontrib>Yang, Hong‐Quan</creatorcontrib><creatorcontrib>Guo, Tongtong</creatorcontrib><title>Photoexcited Cryptochrome 1 Interacts With SPCHLESS to Regulate Stomatal Development in Arabidopsis</title><title>Plant, cell and environment</title><addtitle>Plant Cell Environ</addtitle><description>ABSTRACT Stomata are epidermal openings that facilitate plant−atmosphere gas and water exchange during photosynthesis, respiration and water evaporation. SPEECHLESS (SPCH) is a master basic helix‐loop‐helix (bHLH) transcription factor that determines the initiation of stomatal development. It is known that blue light promotes stomatal development through the blue light photoreceptor cryptochromes (CRYs, CRY1 and CRY2). Whether CRYs regulate stomatal development through directly modulating SPCH is unknown. Here, we demonstrate by biochemical studies that CRY1 physically interacts with SPCH in a blue light‐dependent manner. Genetic studies show that SPCH acts downstream of CRY1 to promote stomatal development in blue light. Furthermore, we show that CRY1 enhances the DNA‐binding activity of SPCH and promotes the expression of its target genes in blue light. These results suggest that the mechanism by which CRY1 promotes stomatal development involves positive regulation of the DNA‐binding activity of SPCH, which is likely mediated by blue light‐induced CRY1−SPCH interaction. The precise regulation of SPCH DNA‐binding activity by CRY1 may allow plants to optimize stomatal density and pattern according to ambient light conditions. 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development</subject><subject>Plant Stomata - metabolism</subject><subject>Plant Stomata - physiology</subject><subject>Plant Stomata - radiation effects</subject><subject>Protein Binding</subject><subject>SPEECHLESS (SPCH)</subject><subject>Stomata</subject><subject>stomatal development</subject><subject>transcription factors</subject><subject>Water exchange</subject><issn>0140-7791</issn><issn>1365-3040</issn><issn>1365-3040</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqN0U1r2zAYB3BRVpr05dAvMAS7rAe3eo2tY_GyJRBoaDZ6NLL8uHGxLU-St-XbT23SHgaD6iIQP_6Snj9Cl5Rc07huBgPXVFLGj9CU8plMOBHkA5oSKkiSpopO0Kn3T4TEg1SdoAlXTHIlxRSZ9dYGC39ME6DCudsNwZqtsx1gipd9AKdN8PihCVu8WeeL1XyzwcHie3gcWx0Ab4LtdNAt_gK_oLVDB33ATY9vnS6byg6-8efouNath4vDfoZ-fJ1_zxfJ6u7bMr9dJYalM56ASHUpQRutpRCSEFOXLMuYJpkm9SylWV3XuipNWlcVcAoKRJZJlnEltMwUP0Of97mDsz9H8KHoGm-gbXUPdvQFp1KwmYqzeQclTKQ0PiPST__QJzu6Pn4kKq7iTCl7vvtqr4yz3juoi8E1nXa7gpLiuaQillS8lBTtx0PiWHZQvcnXViK42YPfTQu7_ycV63y-j_wLkeeaNg</recordid><startdate>202501</startdate><enddate>202501</enddate><creator>Chen, Li</creator><creator>Cao, Xiaoli</creator><creator>Li, Yupeng</creator><creator>Liu, Minqing</creator><creator>Liu, Yao</creator><creator>Guan, Yan</creator><creator>Ruan, Jiaqi</creator><creator>Mao, Zhilei</creator><creator>Wang, Wenxiu</creator><creator>Yang, Hong‐Quan</creator><creator>Guo, Tongtong</creator><general>Wiley Subscription Services, Inc</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>7QP</scope><scope>7ST</scope><scope>C1K</scope><scope>SOI</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-0462-3929</orcidid><orcidid>https://orcid.org/0000-0002-8988-3000</orcidid><orcidid>https://orcid.org/0009-0002-9679-955X</orcidid><orcidid>https://orcid.org/0009-0007-9204-309X</orcidid><orcidid>https://orcid.org/0000-0001-6215-2665</orcidid><orcidid>https://orcid.org/0009-0005-4292-8362</orcidid></search><sort><creationdate>202501</creationdate><title>Photoexcited Cryptochrome 1 Interacts With SPCHLESS to Regulate Stomatal Development in Arabidopsis</title><author>Chen, Li ; 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development</topic><topic>Plant Stomata - metabolism</topic><topic>Plant Stomata - physiology</topic><topic>Plant Stomata - radiation effects</topic><topic>Protein Binding</topic><topic>SPEECHLESS (SPCH)</topic><topic>Stomata</topic><topic>stomatal development</topic><topic>transcription factors</topic><topic>Water exchange</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Li</creatorcontrib><creatorcontrib>Cao, Xiaoli</creatorcontrib><creatorcontrib>Li, Yupeng</creatorcontrib><creatorcontrib>Liu, Minqing</creatorcontrib><creatorcontrib>Liu, Yao</creatorcontrib><creatorcontrib>Guan, Yan</creatorcontrib><creatorcontrib>Ruan, Jiaqi</creatorcontrib><creatorcontrib>Mao, Zhilei</creatorcontrib><creatorcontrib>Wang, Wenxiu</creatorcontrib><creatorcontrib>Yang, Hong‐Quan</creatorcontrib><creatorcontrib>Guo, Tongtong</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium &amp; 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SPEECHLESS (SPCH) is a master basic helix‐loop‐helix (bHLH) transcription factor that determines the initiation of stomatal development. It is known that blue light promotes stomatal development through the blue light photoreceptor cryptochromes (CRYs, CRY1 and CRY2). Whether CRYs regulate stomatal development through directly modulating SPCH is unknown. Here, we demonstrate by biochemical studies that CRY1 physically interacts with SPCH in a blue light‐dependent manner. Genetic studies show that SPCH acts downstream of CRY1 to promote stomatal development in blue light. Furthermore, we show that CRY1 enhances the DNA‐binding activity of SPCH and promotes the expression of its target genes in blue light. These results suggest that the mechanism by which CRY1 promotes stomatal development involves positive regulation of the DNA‐binding activity of SPCH, which is likely mediated by blue light‐induced CRY1−SPCH interaction. The precise regulation of SPCH DNA‐binding activity by CRY1 may allow plants to optimize stomatal density and pattern according to ambient light conditions. Summary statement Blue light photoreceptor CRY1 directly interacts with SPCH in a blue light‐dependent manner to promote its DNA‐binding activity, leading to enhanced expression of SPCH‐target genes and eventual stomatal development in Arabidopsis.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>39253954</pmid><doi>10.1111/pce.15123</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-0462-3929</orcidid><orcidid>https://orcid.org/0000-0002-8988-3000</orcidid><orcidid>https://orcid.org/0009-0002-9679-955X</orcidid><orcidid>https://orcid.org/0009-0007-9204-309X</orcidid><orcidid>https://orcid.org/0000-0001-6215-2665</orcidid><orcidid>https://orcid.org/0009-0005-4292-8362</orcidid></addata></record>
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subjects Arabidopsis
Arabidopsis - genetics
Arabidopsis - growth & development
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
Binding
blue light
Cryptochromes
Cryptochromes - genetics
Cryptochromes - metabolism
Deoxyribonucleic acid
DNA
environment
Evaporation
Gene expression
Gene Expression Regulation, Plant
Gene regulation
Light
light signalling
photoreceptor
photoreceptors
Photosynthesis
Plant Stomata - growth & development
Plant Stomata - metabolism
Plant Stomata - physiology
Plant Stomata - radiation effects
Protein Binding
SPEECHLESS (SPCH)
Stomata
stomatal development
transcription factors
Water exchange
title Photoexcited Cryptochrome 1 Interacts With SPCHLESS to Regulate Stomatal Development in Arabidopsis
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