Sphingolipids in the Root Play an Important Role in Regulating the Leaf Ionome in Arabidopsis thaliana

Dai-Yin Chao, Kenneth Gable, Ming Chen, Ivan Baxter, Charles R. Dietrich, Edgar B. Cahoon, Mary Lou Guerinot, Brett Lahner, Shiyou Lue, Jonathan E. Markham, Joe Morrissey, Gongshe Han, Sita D. Gupta, Jeffrey M. Harmon, Jan G. Jaworski, Teresa M. Dunn, David E. Salt

Research output: Contribution to journalArticle

59 Citations (Scopus)

Abstract

Sphingolipid synthesis is initiated by condensation of Ser with palmitoyl-CoA producing 3-ketodihydrosphinganine (3-KDS), which is reduced by a 3-KDS reductase to dihydrosphinganine. Ser palmitoyltransferase is essential for plant viability. Arabidopsis thaliana contains two genes (At3g06060/TSC10A and At5g19200/TSC10B) encoding proteins with significant similarity to the yeast 3-KDS reductase, Tsc10p. Heterologous expression in yeast of either Arabidopsis gene restored 3-KDS reductase activity to the yeast tsc10 Delta mutant, confirming both as bona fide 3-KDS reductase genes. Consistent with sphingolipids having essential functions in plants, double mutant progeny lacking both genes were not recovered from crosses of single tsc10A and tsc10B mutants. Although the 3-KDS reductase genes are functionally redundant and ubiquitously expressed in Arabidopsis, 3-KDS reductase activity was reduced to 10% of wild-type levels in the loss-of-function tsc10a mutant, leading to an altered sphingolipid profile. This perturbation of sphingolipid biosynthesis in the Arabidopsis tsc10a mutant leads an altered leaf ionome, including increases in Na, K, and Rb and decreases in Mg, Ca, Fe, and Mo. Reciprocal grafting revealed that these changes in the leaf ionome are driven by the root and are associated with increases in root suberin and alterations in Fe homeostasis.

Original languageEnglish
Pages (from-to)1061-1081
Number of pages21
JournalThe Plant Cell
Volume23
Issue number3
DOIs
Publication statusPublished - Mar 2011

Keywords

  • Programmed cell-death
  • Detergent-resistant membranes
  • Serine palmitoyltransferase
  • Saccharomyces-cerevisiae
  • Signal-transduction
  • Metal transporter
  • Plasma-membrane
  • Lipid rafts
  • Gene
  • Plants

Cite this

Sphingolipids in the Root Play an Important Role in Regulating the Leaf Ionome in Arabidopsis thaliana. / Chao, Dai-Yin; Gable, Kenneth; Chen, Ming; Baxter, Ivan; Dietrich, Charles R.; Cahoon, Edgar B.; Guerinot, Mary Lou; Lahner, Brett; Lue, Shiyou; Markham, Jonathan E.; Morrissey, Joe; Han, Gongshe; Gupta, Sita D.; Harmon, Jeffrey M.; Jaworski, Jan G.; Dunn, Teresa M.; Salt, David E.

In: The Plant Cell, Vol. 23, No. 3, 03.2011, p. 1061-1081.

Research output: Contribution to journalArticle

Chao, D-Y, Gable, K, Chen, M, Baxter, I, Dietrich, CR, Cahoon, EB, Guerinot, ML, Lahner, B, Lue, S, Markham, JE, Morrissey, J, Han, G, Gupta, SD, Harmon, JM, Jaworski, JG, Dunn, TM & Salt, DE 2011, 'Sphingolipids in the Root Play an Important Role in Regulating the Leaf Ionome in Arabidopsis thaliana', The Plant Cell, vol. 23, no. 3, pp. 1061-1081. https://doi.org/10.1105/tpc.110.079095
Chao, Dai-Yin ; Gable, Kenneth ; Chen, Ming ; Baxter, Ivan ; Dietrich, Charles R. ; Cahoon, Edgar B. ; Guerinot, Mary Lou ; Lahner, Brett ; Lue, Shiyou ; Markham, Jonathan E. ; Morrissey, Joe ; Han, Gongshe ; Gupta, Sita D. ; Harmon, Jeffrey M. ; Jaworski, Jan G. ; Dunn, Teresa M. ; Salt, David E. / Sphingolipids in the Root Play an Important Role in Regulating the Leaf Ionome in Arabidopsis thaliana. In: The Plant Cell. 2011 ; Vol. 23, No. 3. pp. 1061-1081.
@article{818b2234e67e4a4f93e6766d59bf2b7b,
title = "Sphingolipids in the Root Play an Important Role in Regulating the Leaf Ionome in Arabidopsis thaliana",
abstract = "Sphingolipid synthesis is initiated by condensation of Ser with palmitoyl-CoA producing 3-ketodihydrosphinganine (3-KDS), which is reduced by a 3-KDS reductase to dihydrosphinganine. Ser palmitoyltransferase is essential for plant viability. Arabidopsis thaliana contains two genes (At3g06060/TSC10A and At5g19200/TSC10B) encoding proteins with significant similarity to the yeast 3-KDS reductase, Tsc10p. Heterologous expression in yeast of either Arabidopsis gene restored 3-KDS reductase activity to the yeast tsc10 Delta mutant, confirming both as bona fide 3-KDS reductase genes. Consistent with sphingolipids having essential functions in plants, double mutant progeny lacking both genes were not recovered from crosses of single tsc10A and tsc10B mutants. Although the 3-KDS reductase genes are functionally redundant and ubiquitously expressed in Arabidopsis, 3-KDS reductase activity was reduced to 10{\%} of wild-type levels in the loss-of-function tsc10a mutant, leading to an altered sphingolipid profile. This perturbation of sphingolipid biosynthesis in the Arabidopsis tsc10a mutant leads an altered leaf ionome, including increases in Na, K, and Rb and decreases in Mg, Ca, Fe, and Mo. Reciprocal grafting revealed that these changes in the leaf ionome are driven by the root and are associated with increases in root suberin and alterations in Fe homeostasis.",
keywords = "Programmed cell-death, Detergent-resistant membranes, Serine palmitoyltransferase, Saccharomyces-cerevisiae, Signal-transduction, Metal transporter, Plasma-membrane, Lipid rafts, Gene, Plants",
author = "Dai-Yin Chao and Kenneth Gable and Ming Chen and Ivan Baxter and Dietrich, {Charles R.} and Cahoon, {Edgar B.} and Guerinot, {Mary Lou} and Brett Lahner and Shiyou Lue and Markham, {Jonathan E.} and Joe Morrissey and Gongshe Han and Gupta, {Sita D.} and Harmon, {Jeffrey M.} and Jaworski, {Jan G.} and Dunn, {Teresa M.} and Salt, {David E.}",
year = "2011",
month = "3",
doi = "10.1105/tpc.110.079095",
language = "English",
volume = "23",
pages = "1061--1081",
journal = "The Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "3",

}

TY - JOUR

T1 - Sphingolipids in the Root Play an Important Role in Regulating the Leaf Ionome in Arabidopsis thaliana

AU - Chao, Dai-Yin

AU - Gable, Kenneth

AU - Chen, Ming

AU - Baxter, Ivan

AU - Dietrich, Charles R.

AU - Cahoon, Edgar B.

AU - Guerinot, Mary Lou

AU - Lahner, Brett

AU - Lue, Shiyou

AU - Markham, Jonathan E.

AU - Morrissey, Joe

AU - Han, Gongshe

AU - Gupta, Sita D.

AU - Harmon, Jeffrey M.

AU - Jaworski, Jan G.

AU - Dunn, Teresa M.

AU - Salt, David E.

PY - 2011/3

Y1 - 2011/3

N2 - Sphingolipid synthesis is initiated by condensation of Ser with palmitoyl-CoA producing 3-ketodihydrosphinganine (3-KDS), which is reduced by a 3-KDS reductase to dihydrosphinganine. Ser palmitoyltransferase is essential for plant viability. Arabidopsis thaliana contains two genes (At3g06060/TSC10A and At5g19200/TSC10B) encoding proteins with significant similarity to the yeast 3-KDS reductase, Tsc10p. Heterologous expression in yeast of either Arabidopsis gene restored 3-KDS reductase activity to the yeast tsc10 Delta mutant, confirming both as bona fide 3-KDS reductase genes. Consistent with sphingolipids having essential functions in plants, double mutant progeny lacking both genes were not recovered from crosses of single tsc10A and tsc10B mutants. Although the 3-KDS reductase genes are functionally redundant and ubiquitously expressed in Arabidopsis, 3-KDS reductase activity was reduced to 10% of wild-type levels in the loss-of-function tsc10a mutant, leading to an altered sphingolipid profile. This perturbation of sphingolipid biosynthesis in the Arabidopsis tsc10a mutant leads an altered leaf ionome, including increases in Na, K, and Rb and decreases in Mg, Ca, Fe, and Mo. Reciprocal grafting revealed that these changes in the leaf ionome are driven by the root and are associated with increases in root suberin and alterations in Fe homeostasis.

AB - Sphingolipid synthesis is initiated by condensation of Ser with palmitoyl-CoA producing 3-ketodihydrosphinganine (3-KDS), which is reduced by a 3-KDS reductase to dihydrosphinganine. Ser palmitoyltransferase is essential for plant viability. Arabidopsis thaliana contains two genes (At3g06060/TSC10A and At5g19200/TSC10B) encoding proteins with significant similarity to the yeast 3-KDS reductase, Tsc10p. Heterologous expression in yeast of either Arabidopsis gene restored 3-KDS reductase activity to the yeast tsc10 Delta mutant, confirming both as bona fide 3-KDS reductase genes. Consistent with sphingolipids having essential functions in plants, double mutant progeny lacking both genes were not recovered from crosses of single tsc10A and tsc10B mutants. Although the 3-KDS reductase genes are functionally redundant and ubiquitously expressed in Arabidopsis, 3-KDS reductase activity was reduced to 10% of wild-type levels in the loss-of-function tsc10a mutant, leading to an altered sphingolipid profile. This perturbation of sphingolipid biosynthesis in the Arabidopsis tsc10a mutant leads an altered leaf ionome, including increases in Na, K, and Rb and decreases in Mg, Ca, Fe, and Mo. Reciprocal grafting revealed that these changes in the leaf ionome are driven by the root and are associated with increases in root suberin and alterations in Fe homeostasis.

KW - Programmed cell-death

KW - Detergent-resistant membranes

KW - Serine palmitoyltransferase

KW - Saccharomyces-cerevisiae

KW - Signal-transduction

KW - Metal transporter

KW - Plasma-membrane

KW - Lipid rafts

KW - Gene

KW - Plants

U2 - 10.1105/tpc.110.079095

DO - 10.1105/tpc.110.079095

M3 - Article

VL - 23

SP - 1061

EP - 1081

JO - The Plant Cell

JF - The Plant Cell

SN - 1040-4651

IS - 3

ER -