TOP1α fine-tunes TOR-PLT2 to maintain root tip homeostasis in response to sugars
Plant development is highly dependent on energy levels. TARGET OF RAPAMYCIN (TOR) activates the proximal root meristem to promote root development in response to photosynthesis-derived sugars during photomorphogenesis in Arabidopsis thaliana . However, the mechanisms of how root tip homeostasis is m...
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| Veröffentlicht in: | Nature plants 2022-07, Vol.8 (7), p.792-801 |
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| creator | Zhang, Hao Guo, Lin Li, Yongpeng Zhao, Dan Liu, Luping Chang, Wenwen Zhang, Ke Zheng, Yichao Hou, Jiajie Fu, Chenghao Zhang, Ying Zhang, Baowen Ma, Yuru Niu, Yanxiao Zhang, Kang Xing, Jihong Cui, Sujuan Wang, Fengru Tan, Ke Zheng, Shuzhi Tang, Wenqiang Dong, Jingao Liu, Xigang |
| description | Plant development is highly dependent on energy levels. TARGET OF RAPAMYCIN (TOR) activates the proximal root meristem to promote root development in response to photosynthesis-derived sugars during photomorphogenesis in
Arabidopsis thaliana
. However, the mechanisms of how root tip homeostasis is maintained to ensure proper root cap structure and gravitropism are unknown. PLETHORA (PLT) transcription factors are pivotal for the root apical meristem (RAM) identity by forming gradients, but how PLT gradients are established and maintained, and their roles in COL development are not well known. We demonstrate that endogenous sucrose induces
TOPOISOMERASE1α
(
TOP1α
) expression during the skotomorphogenesis-to-photomorphogenesis transition. TOP1α fine-tunes
TOR
expression in the root tip columella. TOR maintains columella stem cell identity correlating with reduced quiescent centre cell division in a
WUSCHEL RELATED HOMEOBOX5
-independent manner. Meanwhile, TOR promotes
PLT2
expression and phosphorylates and stabilizes PLT2 to maintain its gradient consistent with
TOR
expression pattern. PLT2 controls cell division and amyloplast formation to regulate columella development and gravitropism. This elaborate mechanism helps maintain root tip homeostasis and gravitropism in response to energy changes during root development.
Photosynthesis promotes the expression of
TOPOISOMERASE1α
, which in turn represses TARGET OF RAPAMYCIN (TOR) expression at the root tip. Glucose-TOR regulates cell division at the quiescent centre, and phosphorylates and stabilizes PLETHORA2 in columella cells to maintain root tip homeostasis. |
| doi_str_mv | 10.1038/s41477-022-01179-x |
| format | Article |
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Arabidopsis thaliana
. However, the mechanisms of how root tip homeostasis is maintained to ensure proper root cap structure and gravitropism are unknown. PLETHORA (PLT) transcription factors are pivotal for the root apical meristem (RAM) identity by forming gradients, but how PLT gradients are established and maintained, and their roles in COL development are not well known. We demonstrate that endogenous sucrose induces
TOPOISOMERASE1α
(
TOP1α
) expression during the skotomorphogenesis-to-photomorphogenesis transition. TOP1α fine-tunes
TOR
expression in the root tip columella. TOR maintains columella stem cell identity correlating with reduced quiescent centre cell division in a
WUSCHEL RELATED HOMEOBOX5
-independent manner. Meanwhile, TOR promotes
PLT2
expression and phosphorylates and stabilizes PLT2 to maintain its gradient consistent with
TOR
expression pattern. PLT2 controls cell division and amyloplast formation to regulate columella development and gravitropism. This elaborate mechanism helps maintain root tip homeostasis and gravitropism in response to energy changes during root development.
Photosynthesis promotes the expression of
TOPOISOMERASE1α
, which in turn represses TARGET OF RAPAMYCIN (TOR) expression at the root tip. Glucose-TOR regulates cell division at the quiescent centre, and phosphorylates and stabilizes PLETHORA2 in columella cells to maintain root tip homeostasis.</description><identifier>ISSN: 2055-0278</identifier><identifier>EISSN: 2055-0278</identifier><identifier>DOI: 10.1038/s41477-022-01179-x</identifier><identifier>PMID: 35817819</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/449/2653 ; 631/449/2653/1974 ; 631/449/448 ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Biomedical and Life Sciences ; Cell division ; DNA Topoisomerases, Type I - metabolism ; Energy levels ; Gene Expression Regulation, Plant ; Gravitropism ; Homeostasis ; Life Sciences ; Meristem - metabolism ; Meristems ; Phosphatidylinositol 3-Kinases - metabolism ; Photomorphogenesis ; Photosynthesis ; Plant Roots - metabolism ; Plant Sciences ; Rapamycin ; Root development ; Sirolimus - metabolism ; Skotomorphogenesis ; Stem cells ; Sucrose ; Sugar ; Sugars - metabolism ; TOR protein ; Transcription factors ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Nature plants, 2022-07, Vol.8 (7), p.792-801</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2022. corrected publication 2022. Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2022. The Author(s), under exclusive licence to Springer Nature Limited.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-d16126aa0c2ba78afcc15817596345dbd25ad6aaf991c13065bf8a50312220843</citedby><cites>FETCH-LOGICAL-c375t-d16126aa0c2ba78afcc15817596345dbd25ad6aaf991c13065bf8a50312220843</cites><orcidid>0000-0002-0031-2579 ; 0000-0003-1676-514X ; 0000-0003-4473-2900</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41477-022-01179-x$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41477-022-01179-x$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35817819$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Hao</creatorcontrib><creatorcontrib>Guo, Lin</creatorcontrib><creatorcontrib>Li, Yongpeng</creatorcontrib><creatorcontrib>Zhao, Dan</creatorcontrib><creatorcontrib>Liu, Luping</creatorcontrib><creatorcontrib>Chang, Wenwen</creatorcontrib><creatorcontrib>Zhang, Ke</creatorcontrib><creatorcontrib>Zheng, Yichao</creatorcontrib><creatorcontrib>Hou, Jiajie</creatorcontrib><creatorcontrib>Fu, Chenghao</creatorcontrib><creatorcontrib>Zhang, Ying</creatorcontrib><creatorcontrib>Zhang, Baowen</creatorcontrib><creatorcontrib>Ma, Yuru</creatorcontrib><creatorcontrib>Niu, Yanxiao</creatorcontrib><creatorcontrib>Zhang, Kang</creatorcontrib><creatorcontrib>Xing, Jihong</creatorcontrib><creatorcontrib>Cui, Sujuan</creatorcontrib><creatorcontrib>Wang, Fengru</creatorcontrib><creatorcontrib>Tan, Ke</creatorcontrib><creatorcontrib>Zheng, Shuzhi</creatorcontrib><creatorcontrib>Tang, Wenqiang</creatorcontrib><creatorcontrib>Dong, Jingao</creatorcontrib><creatorcontrib>Liu, Xigang</creatorcontrib><title>TOP1α fine-tunes TOR-PLT2 to maintain root tip homeostasis in response to sugars</title><title>Nature plants</title><addtitle>Nat. Plants</addtitle><addtitle>Nat Plants</addtitle><description>Plant development is highly dependent on energy levels. TARGET OF RAPAMYCIN (TOR) activates the proximal root meristem to promote root development in response to photosynthesis-derived sugars during photomorphogenesis in
Arabidopsis thaliana
. However, the mechanisms of how root tip homeostasis is maintained to ensure proper root cap structure and gravitropism are unknown. PLETHORA (PLT) transcription factors are pivotal for the root apical meristem (RAM) identity by forming gradients, but how PLT gradients are established and maintained, and their roles in COL development are not well known. We demonstrate that endogenous sucrose induces
TOPOISOMERASE1α
(
TOP1α
) expression during the skotomorphogenesis-to-photomorphogenesis transition. TOP1α fine-tunes
TOR
expression in the root tip columella. TOR maintains columella stem cell identity correlating with reduced quiescent centre cell division in a
WUSCHEL RELATED HOMEOBOX5
-independent manner. Meanwhile, TOR promotes
PLT2
expression and phosphorylates and stabilizes PLT2 to maintain its gradient consistent with
TOR
expression pattern. PLT2 controls cell division and amyloplast formation to regulate columella development and gravitropism. This elaborate mechanism helps maintain root tip homeostasis and gravitropism in response to energy changes during root development.
Photosynthesis promotes the expression of
TOPOISOMERASE1α
, which in turn represses TARGET OF RAPAMYCIN (TOR) expression at the root tip. Glucose-TOR regulates cell division at the quiescent centre, and phosphorylates and stabilizes PLETHORA2 in columella cells to maintain root tip homeostasis.</description><subject>631/449/2653</subject><subject>631/449/2653/1974</subject><subject>631/449/448</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biomedical and Life Sciences</subject><subject>Cell division</subject><subject>DNA Topoisomerases, Type I - metabolism</subject><subject>Energy levels</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gravitropism</subject><subject>Homeostasis</subject><subject>Life Sciences</subject><subject>Meristem - metabolism</subject><subject>Meristems</subject><subject>Phosphatidylinositol 3-Kinases - metabolism</subject><subject>Photomorphogenesis</subject><subject>Photosynthesis</subject><subject>Plant Roots - metabolism</subject><subject>Plant Sciences</subject><subject>Rapamycin</subject><subject>Root development</subject><subject>Sirolimus - metabolism</subject><subject>Skotomorphogenesis</subject><subject>Stem cells</subject><subject>Sucrose</subject><subject>Sugar</subject><subject>Sugars - metabolism</subject><subject>TOR protein</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>2055-0278</issn><issn>2055-0278</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kEtOwzAQhi0EolXpBVigSGzYBDx2nDhLVPGSKhVQWVtO4pRUTVw8iVSOxUU4Ew4tD7FgYdma-eb36CPkGOg5UC4vMIIoSULKWEgBkjTc7JEho0L4UiL3f70HZIy4pJRCIgSP6SEZcCEhkZAOycN8dg_vb0FZNSZsu8ZgMJ89hvfTOQtaG9S6alp_AmdtG7TVOni2tbHYaqww6OsG17ZB08PYLbTDI3JQ6hWa8e4ekafrq_nkNpzObu4ml9Mw54lowwJiYLHWNGeZTqQu8xz6rUQa80gUWcGELny_TFPIgdNYZKXUgnJgjFEZ8RE52-aunX3pDLaqrjA3q5VujO1QsVhKwYAz6tHTP-jSdq7x23kqhZSmDHqKbancWURnSrV2Va3dqwKqeudq61x55-rTudr4oZNddJfVpvge-TLsAb4F0LeahXE_f_8T-wFngIss</recordid><startdate>20220701</startdate><enddate>20220701</enddate><creator>Zhang, Hao</creator><creator>Guo, Lin</creator><creator>Li, Yongpeng</creator><creator>Zhao, Dan</creator><creator>Liu, Luping</creator><creator>Chang, Wenwen</creator><creator>Zhang, Ke</creator><creator>Zheng, Yichao</creator><creator>Hou, Jiajie</creator><creator>Fu, Chenghao</creator><creator>Zhang, Ying</creator><creator>Zhang, Baowen</creator><creator>Ma, Yuru</creator><creator>Niu, Yanxiao</creator><creator>Zhang, Kang</creator><creator>Xing, Jihong</creator><creator>Cui, Sujuan</creator><creator>Wang, Fengru</creator><creator>Tan, Ke</creator><creator>Zheng, Shuzhi</creator><creator>Tang, Wenqiang</creator><creator>Dong, Jingao</creator><creator>Liu, Xigang</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>7SN</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>HCIFZ</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-0031-2579</orcidid><orcidid>https://orcid.org/0000-0003-1676-514X</orcidid><orcidid>https://orcid.org/0000-0003-4473-2900</orcidid></search><sort><creationdate>20220701</creationdate><title>TOP1α fine-tunes TOR-PLT2 to maintain root tip homeostasis in response to sugars</title><author>Zhang, Hao ; Guo, Lin ; Li, Yongpeng ; Zhao, Dan ; Liu, Luping ; Chang, Wenwen ; Zhang, Ke ; Zheng, Yichao ; Hou, Jiajie ; Fu, Chenghao ; Zhang, Ying ; Zhang, Baowen ; Ma, Yuru ; Niu, Yanxiao ; Zhang, Kang ; Xing, Jihong ; Cui, Sujuan ; Wang, Fengru ; Tan, Ke ; Zheng, Shuzhi ; Tang, Wenqiang ; Dong, Jingao ; Liu, Xigang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-d16126aa0c2ba78afcc15817596345dbd25ad6aaf991c13065bf8a50312220843</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>631/449/2653</topic><topic>631/449/2653/1974</topic><topic>631/449/448</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Biomedical and Life Sciences</topic><topic>Cell division</topic><topic>DNA Topoisomerases, Type I - metabolism</topic><topic>Energy levels</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gravitropism</topic><topic>Homeostasis</topic><topic>Life Sciences</topic><topic>Meristem - metabolism</topic><topic>Meristems</topic><topic>Phosphatidylinositol 3-Kinases - metabolism</topic><topic>Photomorphogenesis</topic><topic>Photosynthesis</topic><topic>Plant Roots - metabolism</topic><topic>Plant Sciences</topic><topic>Rapamycin</topic><topic>Root development</topic><topic>Sirolimus - metabolism</topic><topic>Skotomorphogenesis</topic><topic>Stem cells</topic><topic>Sucrose</topic><topic>Sugar</topic><topic>Sugars - metabolism</topic><topic>TOR protein</topic><topic>Transcription factors</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Hao</creatorcontrib><creatorcontrib>Guo, Lin</creatorcontrib><creatorcontrib>Li, Yongpeng</creatorcontrib><creatorcontrib>Zhao, Dan</creatorcontrib><creatorcontrib>Liu, Luping</creatorcontrib><creatorcontrib>Chang, Wenwen</creatorcontrib><creatorcontrib>Zhang, Ke</creatorcontrib><creatorcontrib>Zheng, Yichao</creatorcontrib><creatorcontrib>Hou, Jiajie</creatorcontrib><creatorcontrib>Fu, Chenghao</creatorcontrib><creatorcontrib>Zhang, Ying</creatorcontrib><creatorcontrib>Zhang, Baowen</creatorcontrib><creatorcontrib>Ma, Yuru</creatorcontrib><creatorcontrib>Niu, Yanxiao</creatorcontrib><creatorcontrib>Zhang, Kang</creatorcontrib><creatorcontrib>Xing, Jihong</creatorcontrib><creatorcontrib>Cui, Sujuan</creatorcontrib><creatorcontrib>Wang, Fengru</creatorcontrib><creatorcontrib>Tan, Ke</creatorcontrib><creatorcontrib>Zheng, Shuzhi</creatorcontrib><creatorcontrib>Tang, Wenqiang</creatorcontrib><creatorcontrib>Dong, Jingao</creatorcontrib><creatorcontrib>Liu, Xigang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>SciTech Premium Collection</collection><collection>Earth, Atmospheric & Aquatic Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - Academic</collection><jtitle>Nature plants</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Hao</au><au>Guo, Lin</au><au>Li, Yongpeng</au><au>Zhao, Dan</au><au>Liu, Luping</au><au>Chang, Wenwen</au><au>Zhang, Ke</au><au>Zheng, Yichao</au><au>Hou, Jiajie</au><au>Fu, Chenghao</au><au>Zhang, Ying</au><au>Zhang, Baowen</au><au>Ma, Yuru</au><au>Niu, Yanxiao</au><au>Zhang, Kang</au><au>Xing, Jihong</au><au>Cui, Sujuan</au><au>Wang, Fengru</au><au>Tan, Ke</au><au>Zheng, Shuzhi</au><au>Tang, Wenqiang</au><au>Dong, Jingao</au><au>Liu, Xigang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>TOP1α fine-tunes TOR-PLT2 to maintain root tip homeostasis in response to sugars</atitle><jtitle>Nature plants</jtitle><stitle>Nat. Plants</stitle><addtitle>Nat Plants</addtitle><date>2022-07-01</date><risdate>2022</risdate><volume>8</volume><issue>7</issue><spage>792</spage><epage>801</epage><pages>792-801</pages><issn>2055-0278</issn><eissn>2055-0278</eissn><abstract>Plant development is highly dependent on energy levels. TARGET OF RAPAMYCIN (TOR) activates the proximal root meristem to promote root development in response to photosynthesis-derived sugars during photomorphogenesis in
Arabidopsis thaliana
. However, the mechanisms of how root tip homeostasis is maintained to ensure proper root cap structure and gravitropism are unknown. PLETHORA (PLT) transcription factors are pivotal for the root apical meristem (RAM) identity by forming gradients, but how PLT gradients are established and maintained, and their roles in COL development are not well known. We demonstrate that endogenous sucrose induces
TOPOISOMERASE1α
(
TOP1α
) expression during the skotomorphogenesis-to-photomorphogenesis transition. TOP1α fine-tunes
TOR
expression in the root tip columella. TOR maintains columella stem cell identity correlating with reduced quiescent centre cell division in a
WUSCHEL RELATED HOMEOBOX5
-independent manner. Meanwhile, TOR promotes
PLT2
expression and phosphorylates and stabilizes PLT2 to maintain its gradient consistent with
TOR
expression pattern. PLT2 controls cell division and amyloplast formation to regulate columella development and gravitropism. This elaborate mechanism helps maintain root tip homeostasis and gravitropism in response to energy changes during root development.
Photosynthesis promotes the expression of
TOPOISOMERASE1α
, which in turn represses TARGET OF RAPAMYCIN (TOR) expression at the root tip. Glucose-TOR regulates cell division at the quiescent centre, and phosphorylates and stabilizes PLETHORA2 in columella cells to maintain root tip homeostasis.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>35817819</pmid><doi>10.1038/s41477-022-01179-x</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-0031-2579</orcidid><orcidid>https://orcid.org/0000-0003-1676-514X</orcidid><orcidid>https://orcid.org/0000-0003-4473-2900</orcidid></addata></record> |
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| ispartof | Nature plants, 2022-07, Vol.8 (7), p.792-801 |
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| source | MEDLINE; SpringerLink Journals; Nature Journals Online |
| subjects | 631/449/2653 631/449/2653/1974 631/449/448 Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biomedical and Life Sciences Cell division DNA Topoisomerases, Type I - metabolism Energy levels Gene Expression Regulation, Plant Gravitropism Homeostasis Life Sciences Meristem - metabolism Meristems Phosphatidylinositol 3-Kinases - metabolism Photomorphogenesis Photosynthesis Plant Roots - metabolism Plant Sciences Rapamycin Root development Sirolimus - metabolism Skotomorphogenesis Stem cells Sucrose Sugar Sugars - metabolism TOR protein Transcription factors Transcription Factors - genetics Transcription Factors - metabolism |
| title | TOP1α fine-tunes TOR-PLT2 to maintain root tip homeostasis in response to sugars |
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