Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle

In plants, a complex mixture of solutes and macromolecules is transported by the phloem. Here, we examined how solutes and macromolecules are separated when they exit the phloem during the unloading process. We used a combination of approaches (non-invasive imaging, 3D-electron microscopy, and mathe...

Full description

Bibliographic Details
Main Authors: Timothy J Ross-Elliott, Kaare H Jensen, Katrine S Haaning, Brittney M Wager, Jan Knoblauch, Alexander H Howell, Daniel L Mullendore, Alexander G Monteith, Danae Paultre, Dawei Yan, Sofia Otero, Matthieu Bourdon, Ross Sager, Jung-Youn Lee, Ykä Helariutta, Michael Knoblauch, Karl J Oparka
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/24125
_version_ 1811180378783744000
author Timothy J Ross-Elliott
Kaare H Jensen
Katrine S Haaning
Brittney M Wager
Jan Knoblauch
Alexander H Howell
Daniel L Mullendore
Alexander G Monteith
Danae Paultre
Dawei Yan
Sofia Otero
Matthieu Bourdon
Ross Sager
Jung-Youn Lee
Ykä Helariutta
Michael Knoblauch
Karl J Oparka
author_facet Timothy J Ross-Elliott
Kaare H Jensen
Katrine S Haaning
Brittney M Wager
Jan Knoblauch
Alexander H Howell
Daniel L Mullendore
Alexander G Monteith
Danae Paultre
Dawei Yan
Sofia Otero
Matthieu Bourdon
Ross Sager
Jung-Youn Lee
Ykä Helariutta
Michael Knoblauch
Karl J Oparka
author_sort Timothy J Ross-Elliott
collection DOAJ
description In plants, a complex mixture of solutes and macromolecules is transported by the phloem. Here, we examined how solutes and macromolecules are separated when they exit the phloem during the unloading process. We used a combination of approaches (non-invasive imaging, 3D-electron microscopy, and mathematical modelling) to show that phloem unloading of solutes in Arabidopsis roots occurs through plasmodesmata by a combination of mass flow and diffusion (convective phloem unloading). During unloading, solutes and proteins are diverted into the phloem-pole pericycle, a tissue connected to the protophloem by a unique class of ‘funnel plasmodesmata’. While solutes are unloaded without restriction, large proteins are released through funnel plasmodesmata in discrete pulses, a phenomenon we refer to as ‘batch unloading’. Unlike solutes, these proteins remain restricted to the phloem-pole pericycle. Our data demonstrate a major role for the phloem-pole pericycle in regulating phloem unloading in roots.
first_indexed 2024-04-11T09:01:01Z
format Article
id doaj.art-dd4aab87e524416492cee6e67c939fa8
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-11T09:01:01Z
publishDate 2017-02-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-dd4aab87e524416492cee6e67c939fa82022-12-22T04:32:46ZengeLife Sciences Publications LtdeLife2050-084X2017-02-01610.7554/eLife.24125Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycleTimothy J Ross-Elliott0https://orcid.org/0000-0002-0991-9588Kaare H Jensen1https://orcid.org/0000-0003-0787-5283Katrine S Haaning2Brittney M Wager3https://orcid.org/0000-0001-9679-659XJan Knoblauch4https://orcid.org/0000-0002-8952-3961Alexander H Howell5https://orcid.org/0000-0001-6735-0660Daniel L Mullendore6Alexander G Monteith7https://orcid.org/0000-0003-1731-0446Danae Paultre8Dawei Yan9https://orcid.org/0000-0001-8256-0279Sofia Otero10https://orcid.org/0000-0001-9409-8544Matthieu Bourdon11Ross Sager12Jung-Youn Lee13Ykä Helariutta14Michael Knoblauch15https://orcid.org/0000-0003-0391-9891Karl J Oparka16https://orcid.org/0000-0002-8035-5076School of Biological Sciences, Washington State University, Pullman, United StatesDepartment of Physics, Technical University of Denmark, Lyngby, DenmarkDepartment of Physics, Technical University of Denmark, Lyngby, DenmarkSchool of Biological Sciences, Washington State University, Pullman, United StatesSchool of Biological Sciences, Washington State University, Pullman, United StatesSchool of Biological Sciences, Washington State University, Pullman, United StatesSchool of Biological Sciences, Washington State University, Pullman, United StatesDepartment of Biological and Medical Sciences, Oxford Brookes University, Headington, Oxford, United KingdomInstitute of Molecular Plant Science, University of Edinburgh, Edinburgh, United KingdomSainsbury Laboratory, University of Cambridge, Cambridge, United KingdomSainsbury Laboratory, University of Cambridge, Cambridge, United KingdomSainsbury Laboratory, University of Cambridge, Cambridge, United KingdomDepartment of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, United StatesDepartment of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, United StatesSainsbury Laboratory, University of Cambridge, Cambridge, United KingdomSchool of Biological Sciences, Washington State University, Pullman, United StatesInstitute of Molecular Plant Science, University of Edinburgh, Edinburgh, United KingdomIn plants, a complex mixture of solutes and macromolecules is transported by the phloem. Here, we examined how solutes and macromolecules are separated when they exit the phloem during the unloading process. We used a combination of approaches (non-invasive imaging, 3D-electron microscopy, and mathematical modelling) to show that phloem unloading of solutes in Arabidopsis roots occurs through plasmodesmata by a combination of mass flow and diffusion (convective phloem unloading). During unloading, solutes and proteins are diverted into the phloem-pole pericycle, a tissue connected to the protophloem by a unique class of ‘funnel plasmodesmata’. While solutes are unloaded without restriction, large proteins are released through funnel plasmodesmata in discrete pulses, a phenomenon we refer to as ‘batch unloading’. Unlike solutes, these proteins remain restricted to the phloem-pole pericycle. Our data demonstrate a major role for the phloem-pole pericycle in regulating phloem unloading in roots.https://elifesciences.org/articles/24125phloemfunnel plasmodesmatalong distance signalingphloem unloadingprotophloemphloem pole pericycle
spellingShingle Timothy J Ross-Elliott
Kaare H Jensen
Katrine S Haaning
Brittney M Wager
Jan Knoblauch
Alexander H Howell
Daniel L Mullendore
Alexander G Monteith
Danae Paultre
Dawei Yan
Sofia Otero
Matthieu Bourdon
Ross Sager
Jung-Youn Lee
Ykä Helariutta
Michael Knoblauch
Karl J Oparka
Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle
eLife
phloem
funnel plasmodesmata
long distance signaling
phloem unloading
protophloem
phloem pole pericycle
title Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle
title_full Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle
title_fullStr Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle
title_full_unstemmed Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle
title_short Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle
title_sort phloem unloading in arabidopsis roots is convective and regulated by the phloem pole pericycle
topic phloem
funnel plasmodesmata
long distance signaling
phloem unloading
protophloem
phloem pole pericycle
url https://elifesciences.org/articles/24125
work_keys_str_mv AT timothyjrosselliott phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT kaarehjensen phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT katrineshaaning phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT brittneymwager phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT janknoblauch phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT alexanderhhowell phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT daniellmullendore phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT alexandergmonteith phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT danaepaultre phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT daweiyan phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT sofiaotero phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT matthieubourdon phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT rosssager phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT jungyounlee phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT ykahelariutta phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT michaelknoblauch phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle
AT karljoparka phloemunloadinginarabidopsisrootsisconvectiveandregulatedbythephloempolepericycle