Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading

Dawei Yan, Shri Ram Yadav, Andrea Paterlini, William J. Nicolas, Jules D. Petit, Lysiane Brocard, Ilya Belevich, Magali S. Grison, Anne Vaten, Leila Karami, Sedeer el-Showk, Jung Youn Lee, Gosia M. Murawska, Jenny Mortimer, Michael Knoblauch, Eija Jokitalo, Jonathan E. Markham, Emmanuelle M. Bayer, Ykä Helariutta

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

During phloem unloading, multiple cell-to-cell transport events move organic substances to the root meristem. Although the primary unloading event from the sieve elements to the phloem pole pericycle has been characterized to some extent, little is known about post-sieve element unloading. Here, we report a novel gene, PHLOEM UNLOADING MODULATOR (PLM), in the absence of which plasmodesmata-mediated symplastic transport through the phloem pole pericycle–endodermis interface is specifically enhanced. Increased unloading is attributable to a defect in the formation of the endoplasmic reticulum–plasma membrane tethers during plasmodesmal morphogenesis, resulting in the majority of pores lacking a visible cytoplasmic sleeve. PLM encodes a putative enzyme required for the biosynthesis of sphingolipids with very-long-chain fatty acid. Taken together, our results indicate that post-sieve element unloading involves sphingolipid metabolism, which affects plasmodesmal ultrastructure. They also raise the question of how and why plasmodesmata with no cytoplasmic sleeve facilitate molecular trafficking.

Original languageEnglish (US)
Pages (from-to)604-615
Number of pages12
JournalNature Plants
Volume5
Issue number6
DOIs
StatePublished - Jun 1 2019

Fingerprint

sphingolipids
phloem
ultrastructure
sieve elements
biosynthesis
plasmodesmata
very long chain fatty acids
root meristems
morphogenesis
organic matter
cells
metabolism
enzymes
genes

ASJC Scopus subject areas

  • Plant Science

Cite this

Yan, D., Yadav, S. R., Paterlini, A., Nicolas, W. J., Petit, J. D., Brocard, L., ... Helariutta, Y. (2019). Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading. Nature Plants, 5(6), 604-615. https://doi.org/10.1038/s41477-019-0429-5

Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading. / Yan, Dawei; Yadav, Shri Ram; Paterlini, Andrea; Nicolas, William J.; Petit, Jules D.; Brocard, Lysiane; Belevich, Ilya; Grison, Magali S.; Vaten, Anne; Karami, Leila; el-Showk, Sedeer; Lee, Jung Youn; Murawska, Gosia M.; Mortimer, Jenny; Knoblauch, Michael; Jokitalo, Eija; Markham, Jonathan E.; Bayer, Emmanuelle M.; Helariutta, Ykä.

In: Nature Plants, Vol. 5, No. 6, 01.06.2019, p. 604-615.

Research output: Contribution to journalArticle

Yan, D, Yadav, SR, Paterlini, A, Nicolas, WJ, Petit, JD, Brocard, L, Belevich, I, Grison, MS, Vaten, A, Karami, L, el-Showk, S, Lee, JY, Murawska, GM, Mortimer, J, Knoblauch, M, Jokitalo, E, Markham, JE, Bayer, EM & Helariutta, Y 2019, 'Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading', Nature Plants, vol. 5, no. 6, pp. 604-615. https://doi.org/10.1038/s41477-019-0429-5
Yan D, Yadav SR, Paterlini A, Nicolas WJ, Petit JD, Brocard L et al. Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading. Nature Plants. 2019 Jun 1;5(6):604-615. https://doi.org/10.1038/s41477-019-0429-5
Yan, Dawei ; Yadav, Shri Ram ; Paterlini, Andrea ; Nicolas, William J. ; Petit, Jules D. ; Brocard, Lysiane ; Belevich, Ilya ; Grison, Magali S. ; Vaten, Anne ; Karami, Leila ; el-Showk, Sedeer ; Lee, Jung Youn ; Murawska, Gosia M. ; Mortimer, Jenny ; Knoblauch, Michael ; Jokitalo, Eija ; Markham, Jonathan E. ; Bayer, Emmanuelle M. ; Helariutta, Ykä. / Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading. In: Nature Plants. 2019 ; Vol. 5, No. 6. pp. 604-615.
@article{ddd4f04c0b6744db8dddffc340a67f72,
title = "Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading",
abstract = "During phloem unloading, multiple cell-to-cell transport events move organic substances to the root meristem. Although the primary unloading event from the sieve elements to the phloem pole pericycle has been characterized to some extent, little is known about post-sieve element unloading. Here, we report a novel gene, PHLOEM UNLOADING MODULATOR (PLM), in the absence of which plasmodesmata-mediated symplastic transport through the phloem pole pericycle–endodermis interface is specifically enhanced. Increased unloading is attributable to a defect in the formation of the endoplasmic reticulum–plasma membrane tethers during plasmodesmal morphogenesis, resulting in the majority of pores lacking a visible cytoplasmic sleeve. PLM encodes a putative enzyme required for the biosynthesis of sphingolipids with very-long-chain fatty acid. Taken together, our results indicate that post-sieve element unloading involves sphingolipid metabolism, which affects plasmodesmal ultrastructure. They also raise the question of how and why plasmodesmata with no cytoplasmic sleeve facilitate molecular trafficking.",
author = "Dawei Yan and Yadav, {Shri Ram} and Andrea Paterlini and Nicolas, {William J.} and Petit, {Jules D.} and Lysiane Brocard and Ilya Belevich and Grison, {Magali S.} and Anne Vaten and Leila Karami and Sedeer el-Showk and Lee, {Jung Youn} and Murawska, {Gosia M.} and Jenny Mortimer and Michael Knoblauch and Eija Jokitalo and Markham, {Jonathan E.} and Bayer, {Emmanuelle M.} and Yk{\"a} Helariutta",
year = "2019",
month = "6",
day = "1",
doi = "10.1038/s41477-019-0429-5",
language = "English (US)",
volume = "5",
pages = "604--615",
journal = "Nature Plants",
issn = "2055-026X",
publisher = "Palgrave Macmillan Ltd.",
number = "6",

}

TY - JOUR

T1 - Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading

AU - Yan, Dawei

AU - Yadav, Shri Ram

AU - Paterlini, Andrea

AU - Nicolas, William J.

AU - Petit, Jules D.

AU - Brocard, Lysiane

AU - Belevich, Ilya

AU - Grison, Magali S.

AU - Vaten, Anne

AU - Karami, Leila

AU - el-Showk, Sedeer

AU - Lee, Jung Youn

AU - Murawska, Gosia M.

AU - Mortimer, Jenny

AU - Knoblauch, Michael

AU - Jokitalo, Eija

AU - Markham, Jonathan E.

AU - Bayer, Emmanuelle M.

AU - Helariutta, Ykä

PY - 2019/6/1

Y1 - 2019/6/1

N2 - During phloem unloading, multiple cell-to-cell transport events move organic substances to the root meristem. Although the primary unloading event from the sieve elements to the phloem pole pericycle has been characterized to some extent, little is known about post-sieve element unloading. Here, we report a novel gene, PHLOEM UNLOADING MODULATOR (PLM), in the absence of which plasmodesmata-mediated symplastic transport through the phloem pole pericycle–endodermis interface is specifically enhanced. Increased unloading is attributable to a defect in the formation of the endoplasmic reticulum–plasma membrane tethers during plasmodesmal morphogenesis, resulting in the majority of pores lacking a visible cytoplasmic sleeve. PLM encodes a putative enzyme required for the biosynthesis of sphingolipids with very-long-chain fatty acid. Taken together, our results indicate that post-sieve element unloading involves sphingolipid metabolism, which affects plasmodesmal ultrastructure. They also raise the question of how and why plasmodesmata with no cytoplasmic sleeve facilitate molecular trafficking.

AB - During phloem unloading, multiple cell-to-cell transport events move organic substances to the root meristem. Although the primary unloading event from the sieve elements to the phloem pole pericycle has been characterized to some extent, little is known about post-sieve element unloading. Here, we report a novel gene, PHLOEM UNLOADING MODULATOR (PLM), in the absence of which plasmodesmata-mediated symplastic transport through the phloem pole pericycle–endodermis interface is specifically enhanced. Increased unloading is attributable to a defect in the formation of the endoplasmic reticulum–plasma membrane tethers during plasmodesmal morphogenesis, resulting in the majority of pores lacking a visible cytoplasmic sleeve. PLM encodes a putative enzyme required for the biosynthesis of sphingolipids with very-long-chain fatty acid. Taken together, our results indicate that post-sieve element unloading involves sphingolipid metabolism, which affects plasmodesmal ultrastructure. They also raise the question of how and why plasmodesmata with no cytoplasmic sleeve facilitate molecular trafficking.

UR - http://www.scopus.com/inward/record.url?scp=85067084405&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85067084405&partnerID=8YFLogxK

U2 - 10.1038/s41477-019-0429-5

DO - 10.1038/s41477-019-0429-5

M3 - Article

C2 - 31182845

AN - SCOPUS:85067084405

VL - 5

SP - 604

EP - 615

JO - Nature Plants

JF - Nature Plants

SN - 2055-026X

IS - 6

ER -