Nuclear Localised MORE SULPHUR ACCUMULATION1 Epigenetically Regulates Sulphur Homeostasis in Arabidopsis thaliana

Xin-Yuan Huang; Dai-Yin Chao; Anna Koprivova; John Danku; Markus Wirtz; Steffen Müller; Francisco J Sandoval; Hermann Bauwe; Sanja Roje; Brian Dilkes; Rüdiger Hell; Stanislav Kopriva; David E Salt

doi:10.1371/journal.pgen.1006298

Nuclear Localised MORE SULPHUR ACCUMULATION1 Epigenetically Regulates Sulphur Homeostasis in Arabidopsis thaliana

Xin-Yuan Huang, Dai-Yin Chao, Anna Koprivova, John Danku, Markus Wirtz, Steffen Müller, Francisco J Sandoval, Hermann Bauwe, Sanja Roje, Brian Dilkes, Rüdiger Hell, Stanislav Kopriva, David E Salt

Aberdeen Centre For Environmental Sustainability

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Abstract

Sulphur (S) is an essential element for all living organisms. The uptake, assimilation and metabolism of S in plants are well studied. However, the regulation of S homeostasis remains largely unknown. Here, we report on the identification and characterisation of the more sulphur accumulation1 (msa1-1) mutant. The MSA1 protein is localized to the nucleus and is required for both S-adenosylmethionine (SAM) production and DNA methylation. Loss of function of the nuclear localised MSA1 leads to a reduction in SAM in roots and a strong S-deficiency response even at ample S supply, causing an over-accumulation of sulphate, sulphite, cysteine and glutathione. Supplementation with SAM suppresses this high S phenotype. Furthermore, mutation of MSA1 affects genome-wide DNA methylation, including the methylation of S-deficiency responsive genes. Elevated S accumulation in msa1-1 requires the increased expression of the sulphate transporter genes SULTR1;1 and SULTR1;2 which are also differentially methylated in msa1-1. Our results suggest a novel function for MSA1 in the nucleus in regulating SAM biosynthesis and maintaining S homeostasis epigenetically via DNA methylation.

Original language	English
Article number	e1006298
Journal	PLoS Genetics
Volume	12
Issue number	9
DOIs	https://doi.org/10.1371/journal.pgen.1006298
Publication status	Published - 13 Sept 2016

Bibliographical note

Acknowledgments
We thank Dr Hideki Takahashi in Michigan State University for providing sultr1;1 sultr1;2 double mutant, and Professor Pradipsinh Rathod in University of Washington for E. coli GS245(DE3)pLysS strain. We thank Phillip SanMiguel and the Purdue Agricultural Genomics Center for the short read sequencing and analysis. We thank Elena Yakubova and Brett Lahner for ICP-MS analysis, Dr Andrea Raab for use of the HPLC facility, and the Microscopy and Histology Core Facility at the University of Aberdeen for using the confocal laser-scanning microscopy.

Funding:
This work was supported by grants from the U.S. National Science Foundation Arabidopsis 2010 Program (IOB 0419695), U.S. National Science Foundation Plant Genome Research Program (Grant IOS 0701119) and the European Commission (grant PCIG9-GA-2011-291798) to DES.

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10.1371/journal.pgen.1006298Licence: CC BY

Nuclear Localised MORE SULPHUR ACCUMULATION1 Epigenetically Regulates Sulphur Homeostasis in Arabidopsis thaliana
Copyright: © 2016 Huang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. https://creativecommons.org/licenses/by/4.0/
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title = "Nuclear Localised MORE SULPHUR ACCUMULATION1 Epigenetically Regulates Sulphur Homeostasis in Arabidopsis thaliana",

abstract = "Sulphur (S) is an essential element for all living organisms. The uptake, assimilation and metabolism of S in plants are well studied. However, the regulation of S homeostasis remains largely unknown. Here, we report on the identification and characterisation of the more sulphur accumulation1 (msa1-1) mutant. The MSA1 protein is localized to the nucleus and is required for both S-adenosylmethionine (SAM) production and DNA methylation. Loss of function of the nuclear localised MSA1 leads to a reduction in SAM in roots and a strong S-deficiency response even at ample S supply, causing an over-accumulation of sulphate, sulphite, cysteine and glutathione. Supplementation with SAM suppresses this high S phenotype. Furthermore, mutation of MSA1 affects genome-wide DNA methylation, including the methylation of S-deficiency responsive genes. Elevated S accumulation in msa1-1 requires the increased expression of the sulphate transporter genes SULTR1;1 and SULTR1;2 which are also differentially methylated in msa1-1. Our results suggest a novel function for MSA1 in the nucleus in regulating SAM biosynthesis and maintaining S homeostasis epigenetically via DNA methylation.",

author = "Xin-Yuan Huang and Dai-Yin Chao and Anna Koprivova and John Danku and Markus Wirtz and Steffen M{\"u}ller and Sandoval, {Francisco J} and Hermann Bauwe and Sanja Roje and Brian Dilkes and R{\"u}diger Hell and Stanislav Kopriva and Salt, {David E}",

note = "Acknowledgments We thank Dr Hideki Takahashi in Michigan State University for providing sultr1;1 sultr1;2 double mutant, and Professor Pradipsinh Rathod in University of Washington for E. coli GS245(DE3)pLysS strain. We thank Phillip SanMiguel and the Purdue Agricultural Genomics Center for the short read sequencing and analysis. We thank Elena Yakubova and Brett Lahner for ICP-MS analysis, Dr Andrea Raab for use of the HPLC facility, and the Microscopy and Histology Core Facility at the University of Aberdeen for using the confocal laser-scanning microscopy. Funding: This work was supported by grants from the U.S. National Science Foundation Arabidopsis 2010 Program (IOB 0419695), U.S. National Science Foundation Plant Genome Research Program (Grant IOS 0701119) and the European Commission (grant PCIG9-GA-2011-291798) to DES.",

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AU - Huang, Xin-Yuan

AU - Chao, Dai-Yin

AU - Koprivova, Anna

AU - Danku, John

AU - Wirtz, Markus

AU - Müller, Steffen

AU - Sandoval, Francisco J

AU - Bauwe, Hermann

AU - Roje, Sanja

AU - Dilkes, Brian

AU - Hell, Rüdiger

AU - Kopriva, Stanislav

AU - Salt, David E

N1 - Acknowledgments We thank Dr Hideki Takahashi in Michigan State University for providing sultr1;1 sultr1;2 double mutant, and Professor Pradipsinh Rathod in University of Washington for E. coli GS245(DE3)pLysS strain. We thank Phillip SanMiguel and the Purdue Agricultural Genomics Center for the short read sequencing and analysis. We thank Elena Yakubova and Brett Lahner for ICP-MS analysis, Dr Andrea Raab for use of the HPLC facility, and the Microscopy and Histology Core Facility at the University of Aberdeen for using the confocal laser-scanning microscopy. Funding: This work was supported by grants from the U.S. National Science Foundation Arabidopsis 2010 Program (IOB 0419695), U.S. National Science Foundation Plant Genome Research Program (Grant IOS 0701119) and the European Commission (grant PCIG9-GA-2011-291798) to DES.

PY - 2016/9/13

Y1 - 2016/9/13

N2 - Sulphur (S) is an essential element for all living organisms. The uptake, assimilation and metabolism of S in plants are well studied. However, the regulation of S homeostasis remains largely unknown. Here, we report on the identification and characterisation of the more sulphur accumulation1 (msa1-1) mutant. The MSA1 protein is localized to the nucleus and is required for both S-adenosylmethionine (SAM) production and DNA methylation. Loss of function of the nuclear localised MSA1 leads to a reduction in SAM in roots and a strong S-deficiency response even at ample S supply, causing an over-accumulation of sulphate, sulphite, cysteine and glutathione. Supplementation with SAM suppresses this high S phenotype. Furthermore, mutation of MSA1 affects genome-wide DNA methylation, including the methylation of S-deficiency responsive genes. Elevated S accumulation in msa1-1 requires the increased expression of the sulphate transporter genes SULTR1;1 and SULTR1;2 which are also differentially methylated in msa1-1. Our results suggest a novel function for MSA1 in the nucleus in regulating SAM biosynthesis and maintaining S homeostasis epigenetically via DNA methylation.

AB - Sulphur (S) is an essential element for all living organisms. The uptake, assimilation and metabolism of S in plants are well studied. However, the regulation of S homeostasis remains largely unknown. Here, we report on the identification and characterisation of the more sulphur accumulation1 (msa1-1) mutant. The MSA1 protein is localized to the nucleus and is required for both S-adenosylmethionine (SAM) production and DNA methylation. Loss of function of the nuclear localised MSA1 leads to a reduction in SAM in roots and a strong S-deficiency response even at ample S supply, causing an over-accumulation of sulphate, sulphite, cysteine and glutathione. Supplementation with SAM suppresses this high S phenotype. Furthermore, mutation of MSA1 affects genome-wide DNA methylation, including the methylation of S-deficiency responsive genes. Elevated S accumulation in msa1-1 requires the increased expression of the sulphate transporter genes SULTR1;1 and SULTR1;2 which are also differentially methylated in msa1-1. Our results suggest a novel function for MSA1 in the nucleus in regulating SAM biosynthesis and maintaining S homeostasis epigenetically via DNA methylation.

U2 - 10.1371/journal.pgen.1006298

DO - 10.1371/journal.pgen.1006298

M3 - Article

C2 - 27622452

SN - 1553-7390

VL - 12

JO - PLoS Genetics

JF - PLoS Genetics

IS - 9

M1 - e1006298

ER -

Nuclear Localised MORE SULPHUR ACCUMULATION1 Epigenetically Regulates Sulphur Homeostasis in Arabidopsis thaliana

Abstract

Bibliographical note

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