Research article
Sulfate resupply accentuates protein synthesis in coordination with
nitrogen metabolism in sulfur deprived Brassica napus
Qian Zhang
a
, Bok-Rye Lee
a, b
, Sang-Hyun Park
a
, Rashed Zaman
a
,
Jean-Christophe Avice
c, d
, Alain Ourry
c, d
, Tae-Hwan Kim
a, *
a
Department of Animal Science, Institute of Agricultural Science and Technology, College of Agriculture & Life Science, Chonnam National University, Buk-
Gwangju P.O Box 205, Gwangju 500-600, Republic of Korea
b
Biotechnology Research Institute, Chonnam National University, Gwangju 500-757, Republic of Korea
c
Universit e de Caen Basse-Normandie, Esplanade de la Paix, F-14032 Caen Cedex, France
d
UCBN, UMR INRA-UCBN 950 Ecophysiologie V eg etale, Agronomie et Nutritions N, C, S, Esplanade de la Paix, 14032 Caen Cedex, France
article info
Article history:
Received 14 October 2014
Accepted 10 December 2014
Available online 11 December 2014
Keywords:
Brassica napus
Interaction N and S
15
N and
34
S chase
S deprivation
Sulfate assimilation
abstract
To investigate the regulatory interactions between S assimilation and N metabolism in Brassica napus, de
novo synthesis of amino acids and proteins was quantified by
15
N and
34
S tracing, and the responses of
transporter genes, assimilatory enzymes and metabolites pool involving in nitrate and sulfate meta-
bolism were assessed under continuous sulfur supply, sulfur deprivation and sulfate resupply after 3 days
of sulfur (S) deprivation. S-deprived plants were characterized by a strong induction of sulfate trans-
porter genes, ATP sulfurylase (ATPS) and adenosine 5
0
-phosphosulfate reductase (APR), and by a
repressed activity of nitrate reductase (NR) and glutamine synthetase (GS). Sulfate resupply to the S-
deprived plants strongly increased cysteine, amino acids and proteins concentration. The increase in
sulfate and cysteine concentration caused by sulfate resupply was not matched with the expression of
sulfate transporters and the activity of ATPS and APR which were rapidly decreased by sulfate resupply. A
strong induction of O-acetylserine(thiol)lyase (OASTL), NR and GS upon sulfate resupply was accompa-
nied with the increase in cysteine, amino acids and proteins pool. Sulfate resupply resulted in a strong
increase in de novo synthesis of amino acids and proteins, as evidenced by the increases in N and S
incorporation into amino acids (1.8- and 2.4-fold increase) and proteins (2.2-and 6.3-fold increase) when
compared to S-deprived plants. The results thus indicate that sulfate resupply followed by S-deprivation
accelerates nitrate assimilation for protein synthesis.
© 2014 Elsevier Masson SAS. All rights reserved.
1. Introduction
Oilseed rape (Brassica napus L.) has a higher critical N and S
demand (Berry et al., 2010) and requires relatively high amount of
other nutrients (Rathke et al., 2006) when compared to cereals. In
recent decades, the reduction of industrial S emissions to the at-
mosphere and the subsequent reduction of deposition on the soil
have increased the incidence of S-limitation in oilseed rape in many
agricultural areas (McGrath and Zhao, 1995). The limitation of
sulfur supply generally induces multiple responses facilitating
sulfate uptake efficiency at the whole plant level. For instance, in
sulfate deprived plants, there is strongly enhanced expression of
various members of the sulfate transporters (Hawkesford, 2003;
Buchner et al., 2004; Kataoka et al., 2004; Koralewska et al.,
2009). The uptake, distribution and reduction of sulfate in plants
are driven presumably by the sulfur demand for growth (Anderson
and Fitzgerald, 2003) and highly coordinated with exogenous sulfur
supply (Hawkesford, 2003; Buchner et al., 2004). However, there
was apparently no strict and direct shoot to root signaling for the
regulation of sulfate uptake and transport to the shoot in relation to
the variation in sulfur supply (Hawkesford and De Kok, 2006). The
relationship between sulfate content and expression of the sulfate
transporters is ambiguous (Koralewska et al., 2009). For example,
the increase in the overall capacity of sulfate uptake by root is
limited (Hawkesford, 2003; Buchner et al., 2004; Lee et al., 2013,
2014), although the expression of sulfate transporters is strongly
enhanced under S-limitation (Buchner et al., 2004; Kataoka et al.,
2004; Honsel et al., 2012).
* Corresponding author.
E-mail address: grassl@chonnam.ac.kr (T.-H. Kim).
Contents lists available at ScienceDirect
Plant Physiology and Biochemistry
journal homepage: www.elsevier.com/locate/plaphy
http://dx.doi.org/10.1016/j.plaphy.2014.12.006
0981-9428/© 2014 Elsevier Masson SAS. All rights reserved.
Plant Physiology and Biochemistry 87 (2015) 1e8