Secreting salt glands constrain cuticle fracture to enhance desalination efficiency

Plants responding to excessive soil salinity by discharging brine onto their leaf surface risk dehydration through the osmotic continuity between the living tissue and the surface brine, which further enriches with evaporation. Cuticle cracks have long been identified as essential for salt to reach...

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Autores: Mai, Melissa H, Rockwell, Fulton E, Losada, Juan M, Nicholson, Nya, Suo, Zhigang, Holbrook, N Michele
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:dnet:digitalcsic_::ea2feaaf2be39e41cfcf28c806208d46
Acceso en línea:http://hdl.handle.net/10261/428580
https://api.elsevier.com/content/abstract/scopus_id/105020993068
Access Level:acceso abierto
Palabra clave:desalination
fracture mechanics
halophytes
plant physiology
salt glands
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spelling Secreting salt glands constrain cuticle fracture to enhance desalination efficiencyMai, Melissa HRockwell, Fulton ELosada, Juan MNicholson, NyaSuo, ZhigangHolbrook, N Micheledesalinationfracture mechanicshalophytesplant physiologysalt glandsPlants responding to excessive soil salinity by discharging brine onto their leaf surface risk dehydration through the osmotic continuity between the living tissue and the surface brine, which further enriches with evaporation. Cuticle cracks have long been identified as essential for salt to reach the leaf surface but enable a potentially desiccating continuity between the brine and the gland interior. Using the secreting salt gland of Nolana mollis as a model system, we integrate mathematical modeling, imaging, and physiological measurements to examine the mechanical and biochemical processes required for efficient salt removal. We find that the subcuticular space between the concentrated surface brine and the more dilute secreting cell eases the energetic limits of active salt secretion by reducing the concentration gradient of salt across the cell membrane. We show that crack size plays a critical role in balancing the osmotic and pressure gradients required for salt removal without runaway foliar desiccation.This work was supported by the NSF through the Harvard University Materials Research Science and Engineering Center (DMR-2011754). We acknowledge Adam Graham from the Harvard University Center for Nano scale Systems for his support on the cryo-SEM and light microscopy.M.H.M. recognizes support from the Fannie and John Hertz Foundation Fellowship and the NSF Graduate Research Fellowship (Grant no. DGE1745303)and thanks Sophie Everbach, Liesbeth van den Brink, Tomás Fuenzalida, andJacques Dumais for helpful discussions, and Ayman Fayad, Cory Hahn, andPeter Wiggin for growth facility support. J.M.L. was funded by a grant from the Agencia Estatal de Investigación (PID2021-129074OB-100) and a Fulbright-Consejo Superior de Investigaciones Científicas fellowship (FULBR23036)Peer reviewedNational Academy of Sciences (U.S.)Harvard UniversityAgencia Estatal de Investigación (España)Fulbright CommissionConsejo Superior de Investigaciones Científicas (España)0000-0002-9426-70180000-0002-2527-60330000-0002-7966-50180009-0005-0809-08180000-0002-4068-48440000-0003-3325-5395Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202620262025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Postprintinfo:eu-repo/semantics/acceptedVersionhttp://hdl.handle.net/10261/428580https://api.elsevier.com/content/abstract/scopus_id/105020993068reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-129074OB-I00Proceedings of the National Academy of Sciences of the United States of Americahttps://doi.org/10.1073/pnas.2505598122Síinfo:eu-repo/semantics/openAccessoai:dnet:digitalcsic_::ea2feaaf2be39e41cfcf28c806208d462026-05-22T06:33:51Z
dc.title.none.fl_str_mv Secreting salt glands constrain cuticle fracture to enhance desalination efficiency
title Secreting salt glands constrain cuticle fracture to enhance desalination efficiency
spellingShingle Secreting salt glands constrain cuticle fracture to enhance desalination efficiency
Mai, Melissa H
desalination
fracture mechanics
halophytes
plant physiology
salt glands
title_short Secreting salt glands constrain cuticle fracture to enhance desalination efficiency
title_full Secreting salt glands constrain cuticle fracture to enhance desalination efficiency
title_fullStr Secreting salt glands constrain cuticle fracture to enhance desalination efficiency
title_full_unstemmed Secreting salt glands constrain cuticle fracture to enhance desalination efficiency
title_sort Secreting salt glands constrain cuticle fracture to enhance desalination efficiency
dc.creator.none.fl_str_mv Mai, Melissa H
Rockwell, Fulton E
Losada, Juan M
Nicholson, Nya
Suo, Zhigang
Holbrook, N Michele
author Mai, Melissa H
author_facet Mai, Melissa H
Rockwell, Fulton E
Losada, Juan M
Nicholson, Nya
Suo, Zhigang
Holbrook, N Michele
author_role author
author2 Rockwell, Fulton E
Losada, Juan M
Nicholson, Nya
Suo, Zhigang
Holbrook, N Michele
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Harvard University
Agencia Estatal de Investigación (España)
Fulbright Commission
Consejo Superior de Investigaciones Científicas (España)
0000-0002-9426-7018
0000-0002-2527-6033
0000-0002-7966-5018
0009-0005-0809-0818
0000-0002-4068-4844
0000-0003-3325-5395
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv desalination
fracture mechanics
halophytes
plant physiology
salt glands
topic desalination
fracture mechanics
halophytes
plant physiology
salt glands
description Plants responding to excessive soil salinity by discharging brine onto their leaf surface risk dehydration through the osmotic continuity between the living tissue and the surface brine, which further enriches with evaporation. Cuticle cracks have long been identified as essential for salt to reach the leaf surface but enable a potentially desiccating continuity between the brine and the gland interior. Using the secreting salt gland of Nolana mollis as a model system, we integrate mathematical modeling, imaging, and physiological measurements to examine the mechanical and biochemical processes required for efficient salt removal. We find that the subcuticular space between the concentrated surface brine and the more dilute secreting cell eases the energetic limits of active salt secretion by reducing the concentration gradient of salt across the cell membrane. We show that crack size plays a critical role in balancing the osmotic and pressure gradients required for salt removal without runaway foliar desiccation.
publishDate 2025
dc.date.none.fl_str_mv 2025
2026
2026
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Postprint
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/428580
https://api.elsevier.com/content/abstract/scopus_id/105020993068
url http://hdl.handle.net/10261/428580
https://api.elsevier.com/content/abstract/scopus_id/105020993068
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-129074OB-I00
Proceedings of the National Academy of Sciences of the United States of America
https://doi.org/10.1073/pnas.2505598122

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv National Academy of Sciences (U.S.)
publisher.none.fl_str_mv National Academy of Sciences (U.S.)
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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