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

Timothy J. Ross-Elliott, Kaare Hartvig 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

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Abstract

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.
Original languageEnglish
Article numbere24125
JournaleLife
Volume6
Number of pages31
ISSN2050-084X
DOIs
Publication statusPublished - 2017

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This article is distributed under the terms of the Creative Commons Attribution License

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Ross-Elliott, T. J., Jensen, K. H., Haaning, K. S., Wager, B. M., Knoblauch, J., Howell, A. H., ... Oparka, K. J. (2017). Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. eLife, 6, [e24125]. https://doi.org/10.7554/eLife.24125
Ross-Elliott, Timothy J. ; Jensen, Kaare Hartvig ; Haaning, Katrine S. ; Wager, Brittney M. ; Knoblauch, Jan ; Howell, Alexander H. ; Mullendore, Daniel L. ; Monteith, Alexander G ; Paultre, Danae ; Yan, Dawei ; Otero, Sofia ; Bourdon, Matthieu ; Sager, Ross ; Lee, Jung-Youn ; Helariutta, Ykä ; Knoblauch, Michael ; Oparka, Karl J. / Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. In: eLife. 2017 ; Vol. 6.
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abstract = "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.",
author = "Ross-Elliott, {Timothy J.} and Jensen, {Kaare Hartvig} and Haaning, {Katrine S.} and Wager, {Brittney M.} and Jan Knoblauch and Howell, {Alexander H.} and Mullendore, {Daniel L.} and Monteith, {Alexander G} and Danae Paultre and Dawei Yan and Sofia Otero and Matthieu Bourdon and Ross Sager and Jung-Youn Lee and Yk{\"a} Helariutta and Michael Knoblauch and Oparka, {Karl J.}",
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language = "English",
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Ross-Elliott, TJ, Jensen, KH, Haaning, KS, Wager, BM, Knoblauch, J, Howell, AH, Mullendore, DL, Monteith, AG, Paultre, D, Yan, D, Otero, S, Bourdon, M, Sager, R, Lee, J-Y, Helariutta, Y, Knoblauch, M & Oparka, KJ 2017, 'Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle', eLife, vol. 6, e24125. https://doi.org/10.7554/eLife.24125

Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. / Ross-Elliott, Timothy J.; Jensen, Kaare Hartvig; Haaning, Katrine S.; Wager, Brittney M.; Knoblauch, Jan; Howell, Alexander H.; Mullendore, Daniel L.; Monteith, Alexander G; Paultre, Danae; Yan, Dawei; Otero, Sofia; Bourdon, Matthieu; Sager, Ross; Lee, Jung-Youn; Helariutta, Ykä; Knoblauch, Michael; Oparka, Karl J.

In: eLife, Vol. 6, e24125, 2017.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle

AU - Ross-Elliott, Timothy J.

AU - Jensen, Kaare Hartvig

AU - Haaning, Katrine S.

AU - Wager, Brittney M.

AU - Knoblauch, Jan

AU - Howell, Alexander H.

AU - Mullendore, Daniel L.

AU - Monteith, Alexander G

AU - Paultre, Danae

AU - Yan, Dawei

AU - Otero, Sofia

AU - Bourdon, Matthieu

AU - Sager, Ross

AU - Lee, Jung-Youn

AU - Helariutta, Ykä

AU - Knoblauch, Michael

AU - Oparka, Karl J.

N1 - This article is distributed under the terms of the Creative Commons Attribution License

PY - 2017

Y1 - 2017

N2 - 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.

AB - 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.

U2 - 10.7554/eLife.24125

DO - 10.7554/eLife.24125

M3 - Journal article

C2 - 28230527

VL - 6

JO - eLife

JF - eLife

SN - 2050-084X

M1 - e24125

ER -