ORE1 stabilizes PIF4 protein through a UBP12-dependent regulatory module in thermomorphogenesis

ORE1 stabilizes PIF4 protein through a UBP12-dependent regulatory module in thermomorphogenesis | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article ORE1 stabilizes PIF4 protein through a UBP12-dependent regulatory module in thermomorphogenesis Nam-Hai Chua, Su-Hyun Park, Teck Lim Moo This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-8242956/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted You are reading this latest preprint version Abstract Understanding how plants integrate developmental programs with temperature-responsive growth remains a central challenge in thermal biology. Here, we uncover a previously unrecognized mechanism by which a canonical senescence regulator directly governs thermomorphogenesis in Arabidopsis. We show that ORESARA1 (ORE1), best known for orchestrating leaf senescence, plays an indispensable role in warm temperature-induced elongation growth. Mutant plants of ore1 display significantly reduced hypocotyl and petiole elongation and attenuated induction of the thermoresponsive genes IAA19 and YUC8. ORE1 acts upstream of PHYTOCHROME INTERACTING FACTOR 4 (PIF4), the central transcriptional hub for thermomorphogenesis, not by altering its transcript abundance but by stabilizing PIF4 protein specifically under warmth. ORE1 physically interacts with PIF4 in the nucleus and enhances its deubiquitination. We further identify the deubiquitinase UBP12 as a critical component of this pathway: UBP12 is required for PIF4 accumulation and thermomorphogenic growth, yet PIF4 does not bind UBP12 directly. Instead, our biochemical and genetic analyses support a model in which ORE1 functions as a scaffold, to recruit PIF4 to an ORE1-UBP12 complex that positions UBP12 for PIF4 deubiquitination. This UBP12-ORE1-PIF4 module defines a new mechanistic paradigm whereby a senescence regulator controls thermomorphogenesis by orchestrating deubiquitinase-mediated tuning of PIF4 proteostasis. Biological sciences/Plant sciences/Plant molecular biology Biological sciences/Plant sciences/Plant stress responses/Heat Thermomorphogenesis ORE1 PIF4 UBP12 protein stability Full Text Additional Declarations There is NO Competing Interest. Cite Share Download PDF Status: Under Review Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-8242956","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":566549433,"identity":"d22f96c9-f8de-4318-aa4d-0d11dedd3afd","order_by":0,"name":"Nam-Hai Chua","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA4ElEQVRIiWNgGAWjYDACCSD+AKYZHzA8KACLGRDUwjgDTDMbMCQYEKmFmYckLfyzeww/2+6xkZdsb2Z8kGBgk8/A3rxNAq8ld84YS+c8SzOczXOY2SDBIM2ygedYGV4tBhI5BtI5Bw4nyEnkH5NIMDhswCCRY0ZIi/FvC5AW+cfsPxIM/hswyL8hqMVMmgGoRVqCmQ3o/QNAW3jwa5G4kVZm2XMgzXBmTzIz0GHJBmw8acUW+LTwz0jefOPHARt5ieOHGT98qLAz4Gc/vPEGPi2YgI005aNgFIyCUTAKsAEAYENAEpYVfsYAAAAASUVORK5CYII=","orcid":"https://orcid.org/0000-0002-8991-0355","institution":"Temasek Life Sciences Laboratory","correspondingAuthor":true,"prefix":"","firstName":"Nam-Hai","middleName":"","lastName":"Chua","suffix":""},{"id":566549434,"identity":"e6085b4a-5007-47e6-bcb9-141adf2a8f30","order_by":1,"name":"Su-Hyun Park","email":"","orcid":"https://orcid.org/0000-0002-9237-7600","institution":"Temasek Life Sciences Laboratory","correspondingAuthor":false,"prefix":"","firstName":"Su-Hyun","middleName":"","lastName":"Park","suffix":""},{"id":566549435,"identity":"c1265149-b772-49fa-b726-a5e4ee7d6426","order_by":2,"name":"Teck Lim Moo","email":"","orcid":"https://orcid.org/0009-0001-9506-2380","institution":"Temasek Life Sciences Laboratory","correspondingAuthor":false,"prefix":"","firstName":"Teck","middleName":"Lim","lastName":"Moo","suffix":""}],"badges":[],"createdAt":"2025-11-30 15:15:07","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-8242956/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-8242956/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":99793901,"identity":"6c6ad003-4a7b-418f-9b10-ca594af72937","added_by":"auto","created_at":"2026-01-08 13:33:28","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"acdc-reference","size":2189450,"visible":true,"origin":"","legend":"","description":"","filename":"MSORE1NatComm.pdf","url":"https://assets-eu.researchsquare.com/files/rs-8242956/v1/1c72ba6275b4f5568dbaf14d.pdf"},{"id":99603724,"identity":"77a95c4e-581a-4ba4-b74d-ce47a6ebb29f","added_by":"auto","created_at":"2026-01-06 11:00:10","extension":"json","order_by":1,"title":"","display":"","copyAsset":false,"role":"acdc-reference","size":5070,"visible":true,"origin":"","legend":"","description":"","filename":"NCOMMS2596885.json","url":"https://assets-eu.researchsquare.com/files/rs-8242956/v1/4795d2673797bd3fc45cb003.json"},{"id":99804169,"identity":"659130d5-65b8-4fb8-9289-87cdddf53b29","added_by":"auto","created_at":"2026-01-08 14:12:08","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2182866,"visible":true,"origin":"","legend":"Article File","description":"","filename":"MSORE1NatComm.pdf","url":"https://assets-eu.researchsquare.com/files/rs-8242956/v1_covered_3a4e5740-b116-4211-bc31-0a5e4e936f13.pdf"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e Competing Interest.","formattedTitle":"ORE1 stabilizes PIF4 protein through a UBP12-dependent regulatory module in thermomorphogenesis","fulltext":[],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":true,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"nature-portfolio","isNatureJournal":true,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"","title":"Nature Portfolio","twitterHandle":"","acdcEnabled":false,"dfaEnabled":false,"editorialSystem":"ejp","reportingPortfolio":"","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Thermomorphogenesis, ORE1, PIF4, UBP12, protein stability","lastPublishedDoi":"10.21203/rs.3.rs-8242956/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-8242956/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"Understanding how plants integrate developmental programs with temperature-responsive growth remains a central challenge in thermal biology. Here, we uncover a previously unrecognized mechanism by which a canonical senescence regulator directly governs thermomorphogenesis in Arabidopsis. We show that ORESARA1 (ORE1), best known for orchestrating leaf senescence, plays an indispensable role in warm temperature-induced elongation growth. Mutant plants of ore1 display significantly reduced hypocotyl and petiole elongation and attenuated induction of the thermoresponsive genes IAA19 and YUC8. ORE1 acts upstream of PHYTOCHROME INTERACTING FACTOR 4 (PIF4), the central transcriptional hub for thermomorphogenesis, not by altering its transcript abundance but by stabilizing PIF4 protein specifically under warmth. ORE1 physically interacts with PIF4 in the nucleus and enhances its deubiquitination. We further identify the deubiquitinase UBP12 as a critical component of this pathway: UBP12 is required for PIF4 accumulation and thermomorphogenic growth, yet PIF4 does not bind UBP12 directly. Instead, our biochemical and genetic analyses support a model in which ORE1 functions as a scaffold, to recruit PIF4 to an ORE1-UBP12 complex that positions UBP12 for PIF4 deubiquitination. This UBP12-ORE1-PIF4 module defines a new mechanistic paradigm whereby a senescence regulator controls thermomorphogenesis by orchestrating deubiquitinase-mediated tuning of PIF4 proteostasis.","manuscriptTitle":"ORE1 stabilizes PIF4 protein through a UBP12-dependent regulatory module in thermomorphogenesis","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-01-06 11:00:05","doi":"10.21203/rs.3.rs-8242956/v1","editorialEvents":[],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"nature-communications","isNatureJournal":true,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"NCOMMS","sideBox":"Learn more about [Nature Communications](http://www.nature.com/ncomms/)","snPcode":"","submissionUrl":"https://mts-ncomms.nature.com/","title":"Nature Communications","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature Communications","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"1af0a7b6-e81b-4523-841a-90b93b4179ee","owner":[],"postedDate":"January 6th, 2026","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[{"id":60301460,"name":"Biological sciences/Plant sciences/Plant molecular biology"},{"id":60301461,"name":"Biological sciences/Plant sciences/Plant stress responses/Heat"}],"tags":[],"updatedAt":"2026-01-20T08:59:42+00:00","versionOfRecord":[],"versionCreatedAt":"2026-01-06 11:00:05","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-8242956","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-8242956","identity":"rs-8242956","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}