Spingolipids in the root play an important role in regulating the leaf ionome in Arabidopsis thaliana

Authors: CHAO, DAIYIN - Purdue University; GABLE, KENNETH - Danforth Plant Science Center; Baxter, Ivan; CHEN, MING - Danforth Plant Science Center; DIETRICH, CHARLES - Danforth Plant Science Center; CAHOON, EDGAR - University Of Nebraska; GUERINOT, MARY LOU - Dartmouth College; LAHNER, BRETT - Purdue University; LU, SHIYOU - Purdue University; MARKHAM, JONATHAN - Danforth Plant Science Center; MORRISSEY, JOE - Dartmouth College; HAN, GONGSHE - Uniformed Services University; GUPTA, SITA - Uniformed Services University; HARMON, JEFF - Uniformed Services University; JAWORSKI, JAN - Danforth Plant Science Center; DUNN, TERESA - Uniformed Services University; SALT, DAVID - Purdue University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/27/2011
Publication Date: 3/1/2011
Citation: Chao, D., Gable, K., Baxter, I.R., Chen, M., Dietrich, C.R., Cahoon, E.B., Guerinot, M., Lahner, B., Lu, S., Markham, J., Morrissey, J., Han, G., Gupta, S., Harmon, J., Jaworski, J.G., Dunn, T., Salt, D.E. 2011. Spingolipids in the root play an important role in regulating the leaf ionome in Arabidopsis thaliana. The Plant Cell. 23(3):1061-1081.

Interpretive Summary: Sphingolipids, a class of membrane lipids with essential functions in all Eukaryotes, are thought to make up a large percentage of some plant membranes and have specific roles in cell processes through the formation of small microdomains (distinct "patches" in the membrane). Here we discuss the role of two genes that code for a single enzyme in the sphigolipid biosynthesis pathway, one is highly expressed, the other accounts for only 10% of the enzyme produced in the plant. When both genes are disrupted, the plants do not survive germination. However, when the more highly expressed gene is disrupted, the plants appear normal but elemental profiling reveals that they have significantly altered elemental accumulation in their leaves, such as higher sodium and lower magnesium. Several of the elemental changes appear to be the result of alteration in the the amount of suberin, a polymer which forms a barrier to water and ion movement in the root. We also observed alterations in the plants iron homestasis mechanisms, the cause of which is still unknown. Understanding these processes will enable the production of crops that are more efficient in their water and nutrient uptake efficiency, a goal that if attained will greatly improve food security and lower the costs of crop production.

Technical Abstract: Sphingolipid synthesis is initiated by condensation of serine with palmitoyl-CoA to produce 3-ketodihydrosphinganine (3-KDS), which is subsequently reduced by a 3-KDS reductase to dihydrosphinganine (DHS). Serine palmitoyltransferase was recently shown to be essential for plant viability, but the 3-KDS reductase step of sphingolipid synthesis has not been investigated in plants. Arabidopsis thaliana contains two genes (At3g06060/TSC10A and At5g19200/TSC10B) that encode proteins with significant homology to the yeast 3-KDS reductase, Tsc10p. Heterologous expression, in yeast, of either A. thaliana gene restored 3-KDS reductase activity to the yeast tsc10' mutant, thereby identifying both as bona fide 3-KDS reductase genes. Consistent with previous evidence that sphingolipids have essential functions in plants, double mutant progeny lacking both genes were not recovered. Although the 3-KDS reductase genes are functionally redundant and ubiquitously expressed in A. thaliana, 3-KDS reductase activity was reduced to approximately 10% of wild-type levels in the loss-of-function tsc10a mutant, leading to an altered sphingolipid profile compared to wild-type plants. Interestingly, this perturbation of sphingolipid biosynthesis in the A. thaliana tsc10a mutant leads to significant alterations in the leaf ionome, including increases in Na, K and Rb (a K analogue), 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 both increases in root suberin, and elevation of expression in the root of genes involved in Fe homoeostasis, including the Fe-transporter IRT1.