Plant PIEZO homologs modulate vacuole morphology during tip growth
Piezo sensors in animal cells are localized in the cell membrane and transduce mechanical signals. The cell membrane of plant cells, unlike that of animal cells, is usually plastered up against a stiff cell wall and does not have much mobility. Much of the cell’s volume is accounted for by a large c...
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Veröffentlicht in: | Science (American Association for the Advancement of Science) 2021-07, Vol.373 (6554), p.586-590 |
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creator | Radin, Ivan Richardson, Ryan A. Coomey, Joshua H. Weiner, Ethan R. Bascom, Carlisle S. Li, Ting Bezanilla, Magdalena Haswell, Elizabeth S. |
description | Piezo sensors in animal cells are localized in the cell membrane and transduce mechanical signals. The cell membrane of plant cells, unlike that of animal cells, is usually plastered up against a stiff cell wall and does not have much mobility. Much of the cell’s volume is accounted for by a large central vacuole, the membrane of which, the tonoplast, is not so mechanically constrained. Radin
et al
. studied how and where plant cells use Piezo sensors. Plant homologs of the animal mechanosensitive channels are found not in the plasma membrane but rather in the tonoplast. In both moss and the small flowering plant
Arabidopsis
, mutations in plant Piezo sensors altered vacuolar morphology and growth patterns in tip-growing cells. —PJH
Mechanosensitive channels localize to the vacuole membrane in
Arabidopsis
and moss and regulate vacuolar membrane growth.
In animals, PIEZOs are plasma membrane–localized cation channels involved in diverse mechanosensory processes. We investigated PIEZO function in tip-growing cells in the moss
Physcomitrium patens
and the flowering plant
Arabidopsis thaliana
.
Pp
PIEZO1 and
Pp
PIEZO2 redundantly contribute to the normal growth, size, and cytoplasmic calcium oscillations of caulonemal cells. Both
Pp
PIEZO1 and
Pp
PIEZO2 localized to vacuolar membranes. Loss-of-function, gain-of-function, and overexpression mutants revealed that moss PIEZO homologs promote increased complexity of vacuolar membranes through tubulation, internalization, and/or fission.
Arabidopsis
PIEZO1 also localized to the tonoplast and is required for vacuole tubulation in the tips of pollen tubes. We propose that in plant cells the tonoplast has more freedom of movement than the plasma membrane, making it a more effective location for mechanosensory proteins. |
doi_str_mv | 10.1126/science.abe6310 |
format | Article |
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et al
. studied how and where plant cells use Piezo sensors. Plant homologs of the animal mechanosensitive channels are found not in the plasma membrane but rather in the tonoplast. In both moss and the small flowering plant
Arabidopsis
, mutations in plant Piezo sensors altered vacuolar morphology and growth patterns in tip-growing cells. —PJH
Mechanosensitive channels localize to the vacuole membrane in
Arabidopsis
and moss and regulate vacuolar membrane growth.
In animals, PIEZOs are plasma membrane–localized cation channels involved in diverse mechanosensory processes. We investigated PIEZO function in tip-growing cells in the moss
Physcomitrium patens
and the flowering plant
Arabidopsis thaliana
.
Pp
PIEZO1 and
Pp
PIEZO2 redundantly contribute to the normal growth, size, and cytoplasmic calcium oscillations of caulonemal cells. Both
Pp
PIEZO1 and
Pp
PIEZO2 localized to vacuolar membranes. Loss-of-function, gain-of-function, and overexpression mutants revealed that moss PIEZO homologs promote increased complexity of vacuolar membranes through tubulation, internalization, and/or fission.
Arabidopsis
PIEZO1 also localized to the tonoplast and is required for vacuole tubulation in the tips of pollen tubes. We propose that in plant cells the tonoplast has more freedom of movement than the plasma membrane, making it a more effective location for mechanosensory proteins.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.abe6310</identifier><language>eng</language><publisher>Washington: The American Association for the Advancement of Science</publisher><subject>Arabidopsis ; Calcium signalling ; Cell membranes ; Cell walls ; Cytology ; Flowering ; Growth patterns ; Homology ; Internalization ; Ion channels ; Mechanical stimuli ; Mechanosensitive channels ; Membranes ; Morphology ; Mosses ; Mutation ; Plant cells ; Pollen ; Pollen tubes ; Sensors</subject><ispartof>Science (American Association for the Advancement of Science), 2021-07, Vol.373 (6554), p.586-590</ispartof><rights>Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c409t-f96b5594b9bca7e75d608c2ccaca18103f2d97af82c5be43ea23bbb83264ddee3</citedby><cites>FETCH-LOGICAL-c409t-f96b5594b9bca7e75d608c2ccaca18103f2d97af82c5be43ea23bbb83264ddee3</cites><orcidid>0000-0001-5866-6671 ; 0000-0001-6124-9916 ; 0000-0001-9030-8874 ; 0000-0002-4246-065X ; 0000-0001-5711-2861 ; 0000-0003-0188-8657 ; 0000-0002-9897-8351</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,2871,2872,27901,27902</link.rule.ids></links><search><creatorcontrib>Radin, Ivan</creatorcontrib><creatorcontrib>Richardson, Ryan A.</creatorcontrib><creatorcontrib>Coomey, Joshua H.</creatorcontrib><creatorcontrib>Weiner, Ethan R.</creatorcontrib><creatorcontrib>Bascom, Carlisle S.</creatorcontrib><creatorcontrib>Li, Ting</creatorcontrib><creatorcontrib>Bezanilla, Magdalena</creatorcontrib><creatorcontrib>Haswell, Elizabeth S.</creatorcontrib><title>Plant PIEZO homologs modulate vacuole morphology during tip growth</title><title>Science (American Association for the Advancement of Science)</title><description>Piezo sensors in animal cells are localized in the cell membrane and transduce mechanical signals. The cell membrane of plant cells, unlike that of animal cells, is usually plastered up against a stiff cell wall and does not have much mobility. Much of the cell’s volume is accounted for by a large central vacuole, the membrane of which, the tonoplast, is not so mechanically constrained. Radin
et al
. studied how and where plant cells use Piezo sensors. Plant homologs of the animal mechanosensitive channels are found not in the plasma membrane but rather in the tonoplast. In both moss and the small flowering plant
Arabidopsis
, mutations in plant Piezo sensors altered vacuolar morphology and growth patterns in tip-growing cells. —PJH
Mechanosensitive channels localize to the vacuole membrane in
Arabidopsis
and moss and regulate vacuolar membrane growth.
In animals, PIEZOs are plasma membrane–localized cation channels involved in diverse mechanosensory processes. We investigated PIEZO function in tip-growing cells in the moss
Physcomitrium patens
and the flowering plant
Arabidopsis thaliana
.
Pp
PIEZO1 and
Pp
PIEZO2 redundantly contribute to the normal growth, size, and cytoplasmic calcium oscillations of caulonemal cells. Both
Pp
PIEZO1 and
Pp
PIEZO2 localized to vacuolar membranes. Loss-of-function, gain-of-function, and overexpression mutants revealed that moss PIEZO homologs promote increased complexity of vacuolar membranes through tubulation, internalization, and/or fission.
Arabidopsis
PIEZO1 also localized to the tonoplast and is required for vacuole tubulation in the tips of pollen tubes. We propose that in plant cells the tonoplast has more freedom of movement than the plasma membrane, making it a more effective location for mechanosensory proteins.</description><subject>Arabidopsis</subject><subject>Calcium signalling</subject><subject>Cell membranes</subject><subject>Cell walls</subject><subject>Cytology</subject><subject>Flowering</subject><subject>Growth patterns</subject><subject>Homology</subject><subject>Internalization</subject><subject>Ion channels</subject><subject>Mechanical stimuli</subject><subject>Mechanosensitive channels</subject><subject>Membranes</subject><subject>Morphology</subject><subject>Mosses</subject><subject>Mutation</subject><subject>Plant cells</subject><subject>Pollen</subject><subject>Pollen tubes</subject><subject>Sensors</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNpdkD1PwzAQhi0EEqUws1piYUnrj9iJR6haqFSpHWBhiWzn0qZK4mAnoP57ErUT00n3Pnp19yD0SMmMUibnwZbQWJhpA5JTcoUmlCgRKUb4NZoQwmWUkkTcorsQjoQMmeIT9LqrdNPh3Xr5tcUHV7vK7QOuXd5XugP8o23vKhgWvj2M2QnnvS-bPe7KFu-9--0O9-im0FWAh8ucos_V8mPxHm22b-vFyyayMVFdVChphFCxUcbqBBKRS5JaZq22mqaU8ILlKtFFyqwwEHPQjBtjUs5knOcAfIqez72td989hC6ry2ChGh4A14eMCZEwRlOVDujTP_Toet8M142UjKVkfKTmZ8p6F4KHImt9WWt_yijJRqfZxWl2ccr_AM8cbN8</recordid><startdate>20210730</startdate><enddate>20210730</enddate><creator>Radin, Ivan</creator><creator>Richardson, Ryan A.</creator><creator>Coomey, Joshua H.</creator><creator>Weiner, Ethan R.</creator><creator>Bascom, Carlisle S.</creator><creator>Li, Ting</creator><creator>Bezanilla, Magdalena</creator><creator>Haswell, Elizabeth S.</creator><general>The American Association for the Advancement of Science</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5866-6671</orcidid><orcidid>https://orcid.org/0000-0001-6124-9916</orcidid><orcidid>https://orcid.org/0000-0001-9030-8874</orcidid><orcidid>https://orcid.org/0000-0002-4246-065X</orcidid><orcidid>https://orcid.org/0000-0001-5711-2861</orcidid><orcidid>https://orcid.org/0000-0003-0188-8657</orcidid><orcidid>https://orcid.org/0000-0002-9897-8351</orcidid></search><sort><creationdate>20210730</creationdate><title>Plant PIEZO homologs modulate vacuole morphology during tip growth</title><author>Radin, Ivan ; Richardson, Ryan A. ; Coomey, Joshua H. ; Weiner, Ethan R. ; Bascom, Carlisle S. ; Li, Ting ; Bezanilla, Magdalena ; Haswell, Elizabeth S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c409t-f96b5594b9bca7e75d608c2ccaca18103f2d97af82c5be43ea23bbb83264ddee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Arabidopsis</topic><topic>Calcium signalling</topic><topic>Cell membranes</topic><topic>Cell walls</topic><topic>Cytology</topic><topic>Flowering</topic><topic>Growth patterns</topic><topic>Homology</topic><topic>Internalization</topic><topic>Ion channels</topic><topic>Mechanical stimuli</topic><topic>Mechanosensitive channels</topic><topic>Membranes</topic><topic>Morphology</topic><topic>Mosses</topic><topic>Mutation</topic><topic>Plant cells</topic><topic>Pollen</topic><topic>Pollen tubes</topic><topic>Sensors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Radin, Ivan</creatorcontrib><creatorcontrib>Richardson, Ryan A.</creatorcontrib><creatorcontrib>Coomey, Joshua H.</creatorcontrib><creatorcontrib>Weiner, Ethan R.</creatorcontrib><creatorcontrib>Bascom, Carlisle S.</creatorcontrib><creatorcontrib>Li, Ting</creatorcontrib><creatorcontrib>Bezanilla, Magdalena</creatorcontrib><creatorcontrib>Haswell, Elizabeth S.</creatorcontrib><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</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>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Radin, Ivan</au><au>Richardson, Ryan A.</au><au>Coomey, Joshua H.</au><au>Weiner, Ethan R.</au><au>Bascom, Carlisle S.</au><au>Li, Ting</au><au>Bezanilla, Magdalena</au><au>Haswell, Elizabeth S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Plant PIEZO homologs modulate vacuole morphology during tip growth</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><date>2021-07-30</date><risdate>2021</risdate><volume>373</volume><issue>6554</issue><spage>586</spage><epage>590</epage><pages>586-590</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><abstract>Piezo sensors in animal cells are localized in the cell membrane and transduce mechanical signals. The cell membrane of plant cells, unlike that of animal cells, is usually plastered up against a stiff cell wall and does not have much mobility. Much of the cell’s volume is accounted for by a large central vacuole, the membrane of which, the tonoplast, is not so mechanically constrained. Radin
et al
. studied how and where plant cells use Piezo sensors. Plant homologs of the animal mechanosensitive channels are found not in the plasma membrane but rather in the tonoplast. In both moss and the small flowering plant
Arabidopsis
, mutations in plant Piezo sensors altered vacuolar morphology and growth patterns in tip-growing cells. —PJH
Mechanosensitive channels localize to the vacuole membrane in
Arabidopsis
and moss and regulate vacuolar membrane growth.
In animals, PIEZOs are plasma membrane–localized cation channels involved in diverse mechanosensory processes. We investigated PIEZO function in tip-growing cells in the moss
Physcomitrium patens
and the flowering plant
Arabidopsis thaliana
.
Pp
PIEZO1 and
Pp
PIEZO2 redundantly contribute to the normal growth, size, and cytoplasmic calcium oscillations of caulonemal cells. Both
Pp
PIEZO1 and
Pp
PIEZO2 localized to vacuolar membranes. Loss-of-function, gain-of-function, and overexpression mutants revealed that moss PIEZO homologs promote increased complexity of vacuolar membranes through tubulation, internalization, and/or fission.
Arabidopsis
PIEZO1 also localized to the tonoplast and is required for vacuole tubulation in the tips of pollen tubes. We propose that in plant cells the tonoplast has more freedom of movement than the plasma membrane, making it a more effective location for mechanosensory proteins.</abstract><cop>Washington</cop><pub>The American Association for the Advancement of Science</pub><doi>10.1126/science.abe6310</doi><tpages>5</tpages><orcidid>https://orcid.org/0000-0001-5866-6671</orcidid><orcidid>https://orcid.org/0000-0001-6124-9916</orcidid><orcidid>https://orcid.org/0000-0001-9030-8874</orcidid><orcidid>https://orcid.org/0000-0002-4246-065X</orcidid><orcidid>https://orcid.org/0000-0001-5711-2861</orcidid><orcidid>https://orcid.org/0000-0003-0188-8657</orcidid><orcidid>https://orcid.org/0000-0002-9897-8351</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Calcium signalling Cell membranes Cell walls Cytology Flowering Growth patterns Homology Internalization Ion channels Mechanical stimuli Mechanosensitive channels Membranes Morphology Mosses Mutation Plant cells Pollen Pollen tubes Sensors |
title | Plant PIEZO homologs modulate vacuole morphology during tip growth |
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