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Front. Plant Sci. | doi: 10.3389/fpls.2018.01709

The photorespiratory BOU gene mutation alters sulfur assimilation and its crosstalk with carbon and nitrogen metabolism in Arabidopsis thaliana

 Sladjana Samuilov1*,  Dominik Brilhaus2,  Nadine Rademacher2, Samanta Flachbart2, Leila Arab1, Saleh Alfarraj3, Franziska Kuhnert2,  Stanislav Kopriva4,  Andreas P. Weber2, Tabea Mettler-Altmann2 and  Heinz Rennenberg1
  • 1Chair of Tree Physiology, Institute of Forest Sciences, Faculty of Environment and Natural Resources, University of Freiburg, Germany
  • 2Institute of Plant Biochemistry and Cluster of Excellence in Plant Sciences (CEPLAS), Heinrich Heine Universität Düsseldorf, Germany
  • 3King Saud University, Saudi Arabia
  • 4Botanical Institute and Cluster of Excellence in Plant Sciences (CEPLAS), Universität zu Köln, Germany

This study was aimed at elucidating the significance of photorespiratory serine (Ser) production for cysteine (Cys) biosynthesis. For this purpose, sulfur (S) metabolism and its crosstalk with nitrogen (N) and carbon (C) metabolism were analyzed in wildtype Arabidopsis and its photorespiratory bou-2 mutant with impaired glycine decarboxylase (GDC) activity. Foliar glycine and Ser contents were enhanced in the mutant at day and night. The high Ser levels in the mutant cannot be explained by transcript abundances of genes of the photorespiratory pathway or two alternative pathways of Ser biosynthesis. Despite enhanced foliar Ser, reduced GDC activity mediated decline in sulfur flux into major sulfur pools in the mutant, as a result of deregulation of genes of sulfur reduction and assimilation. Still, foliar Cys and glutathione contents in the mutant were enhanced. The use of Cys for methionine and glucosinolates synthesis was reduced in the mutant. Reduced GDC activity in the mutant downregulated Calvin Cycle and nitrogen assimilation genes, upregulated key enzymes of glycolysis and the tricarboxylic acid (TCA) pathway and modified accumulation of sugars and TCA intermediates. Thus, photorespiratory Ser production can be replaced by other metabolic Ser sources, but this replacement deregulates the cross-talk between S, N and C metabolism.

Keywords: Cysteine synthesis, Glutathione, Glycine, Glycolysis, nitrogen assimilation, photorespiration, Ser biosynthesis, TCA cycle

Received: 07 Aug 2018; Accepted: 02 Nov 2018.

Edited by:

Hans-Henning Kunz, Washington State University, United States

Reviewed by:

Astrid Wingler, University College Cork, Ireland
Christine H. Foyer, University of Leeds, United Kingdom  

Copyright: © 2018 Samuilov, Brilhaus, Rademacher, Flachbart, Arab, Alfarraj, Kuhnert, Kopriva, Weber, Mettler-Altmann and Rennenberg. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: PhD. Sladjana Samuilov, University of Freiburg, Chair of Tree Physiology, Institute of Forest Sciences, Faculty of Environment and Natural Resources, Freiburg, 79085, Baden-Wurttemberg, Germany, sladjana.samuilov@ctp.uni-freiburg.de