Journal of Experimental Botany, Vol. 70, No. 16 pp.
4069–4073, 2019
doi:10.1093/jxb/erz319
eXtra Botany
Special Issue Editorial
Sulfur nutrition: impacts on plant development, metabolism,
and stress responses
Sulfur is an essential element for all organisms and has a
wide variety of functions. Plant sulfur nutrition is particu-
larly important as plants are our primary source of the es-
sential amino acid methionine. Sulfur deficiency affects the
growth, development, disease resistance, and perform-
ance of plants and has a great impact on the nutritional
quality of crops. In this special issue, a collection of papers
based mainly on contributions from the 11th International
Plant Sulfur Workshop gives an overview of different facets
of sulfur functions in plants and highlights the importance
of sulfur nutrition for different parts of the plant life cycle.
From a biochemical point of view, sulfur is a remarkably
interesting mineral element because it transitions into a wide
range of oxidation states, allowing sulfur-containing com-
pounds to be involved in diverse chemical reactions. In add-
ition, sulfur utilization is dependent on assimilation pathways
that incorporate sulfur into organic molecules in either re-
duced form of organic thiols or as organic sulfated compounds
(Box 1) (Takahashi et al., 2011). The amino acid cysteine is a
product of the reductive sulfate assimilation pathway. Cysteine
is a source of reduced sulfur for many other essential metab-
olites, including methionine. Furthermore, the reactivity of
the thiol group (-SH) makes cysteine residues in proteins im-
portant for their structural maintenance as they form disulfide
bridges. They are also important for enzyme reaction mech-
anisms and for regulation directed through either changes
in redox states or covalent modifications. Thiol residues of
glutathione (GSH), phytochelatins, and some other func-
tional polypeptides such as thioredoxins and metallothioneins
are essential for detoxification of heavy metals, xenobiotics,
pathogen/pest-borne molecules, and reactive oxygen species.
3´-Phosphoadenosine 5´-phosphosulfate (PAPS) produced in
the sulfate assimilation pathway provides activated sulfate for
sulfation of metabolites that play characteristic roles in the
mitigation of both abiotic and biotic stress (Box 1). In addition
to the essential amino acid methionine, a number of plant
sulfur metabolites are important ingredients in human diets,
such as glucosinolates and their derivatives in Brassicaceae
species, and are responsible for distinctive tastes or flavors as
well as also being recognized as compounds that are beneficial
to health (Traka and Mithen, 2009).
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Thus, there is clear value in fundamental research aimed at
understanding how plants utilize sulfate (the primary mineral-
ized inorganic form in which sulfur occurs in soils) in order
to produce an array of sulfur-containing metabolites, and in
understanding how this utilization is controlled. Increasing
our knowledge will lead to potential agronomical, ecological,
and nutritional benefits. Accordingly, plant sulfur research has
been positioned at the forefront of plant science, adopting new
experimental approaches to investigate underlying molecular
mechanisms, and in addition exploring potential applications
in several important areas associated with global sustainability
and human well-being. Some specific questions addressed in
plant sulfur research have dealt with crop quality beyond prod-
uctivity issues, such as studies with wheat and potato that have
examined the effect of sulfur deficiency on the accumulation
of free asparagine, which correlates with acrylamide forma-
tion in foods that occurs through the Maillard reaction during
cooking (Halford et  al., 2012), and studies that have evalu-
ated the genetic potential for increasing contents of health-
promoting sulfur metabolites in broccoli (Traka et  al., 2013).
This special issue illustrates recent progress that has been made
in diverse fields of plant sulfur research and provides perspec-
tives on major future directions and routes toward applications
based on concepts developed in the post-genomic era.
Sulfur research in the post-genomic era
Sulfur research entered the post-genomic era after decades
of primarily using biochemical approaches, then molecular
genetics and systems biology. Rapid progress has been made
during the past two decades, particularly with the emergence
of systems biology, where we have seen early pioneering studies
focused on responses to sulfate deficiency that have pushed
the boundaries and shown the power of ‘omics’ approaches
in identifying new genes, gene regulatory networks, and gene
functions (Hirai et al., 2003, 2005, 2007; Maruyama-Nakashita
et al., 2003; Nikiforova et al., 2003, 2004, 2005). Precise infor-
mation on genome structures and sequences, which became
available in the post-genomic era alongside the development of
high-throughput sequencing technologies, has greatly acceler-
ated the procedures used to identify causal genes for variation
in many plant traits and candidate genes of interest for trait
development. The increasing availability of reference genome
4070 | Kopriva et al.

Box 1.  Plant sulfur metabolism for essential biological processes

Plants take up sulfate (SO42-) from soil and synthesize S-amino acids cysteine (Cys) and methionine (Met).
In the reductive sulfate assimilation pathway, SO42- is first activated to adenosine 5’-phosphosulfate
(APS) using ATP, which is followed by reduction to sulfite (SO32-) and then to sulfide (S2-). Cys is
formed by condensation of S2- and an amino acid Ser derived carbon skeleton O-acetylserine (OAS).
SO32- is required for the sulfolipid biosynthesis. S2- is involved in protein modification and redox
control. Met and S-adenosylmethionine (SAM) are synthesized downstream of the Cys biosynthetic
pathway. SAM serves as a methyl donor for various methylation reactions and a substrate for ethylene

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biosynthesis. Glutathione (GSH; γ-glutamyl-cysteinylglycine) synthesized from Cys plays pivotal roles
in redox control and detoxification of cytotoxic molecules, such as reactive oxygen species (ROS) and
heavy metals.
In plants, following SO42- activation to APS, the sulfate assimilation pathway bifurcates into two
pathways – one for the SO42- reduction as mentioned above, and the other for the 3’-phosphoadenosine
5’-phosphosulfate (PAPS) biosynthesis. PAPS serves as the sulfate donor for sulfation of peptides,
hormones, and specialized metabolites. Sulfation thus modulates functions of peptides and
metabolites involved in biologically important processes in the plant life cycle, such as abiotic/biotic
stress mitigation and growth regulation. 3’-Phosphoadenosine 5’-phosphate (PAP), the byproduct of
sulfation, acts as a retrograde signal for stress responses. Specialized metabolites derived from Cys
and sulfation contribute to tastes and flavors of foods, and are also known as nutraceuticals.
The diagram illustrates an overview of the S metabolic pathways highlighting their connections
to essential biological processes. Only the representative pathways are shown. The S compounds
displayed in clockwise order: adenosine 5’-phosphosulfate (1), sulfoquinovosyl dipalmitoylglycerol
(2), cysteine (3), methionine (4), glutathione (5), S-adenosylmethionine (6), allicin (7), glucosinolate (8),
phytosulfokine (9).

sequences and transcriptome datasets across the plant kingdom
has allowed us to search for homologs and to explore the evolu-
tionary history of genes and complex traits. This technological
development and the rapid increase in genomic information
that occurred alongside it broke the existing boundaries of our
research areas and extended the depth of our knowledge, al-
lowing us to tackle more complex research questions and to
investigate and engineer specific traits directly in non-model
plant species, including crops.
Among the new approaches that were enabled by the in-
crease in data, genome-wide association studies (GWAS) have
had a particularly strong impact on the field of sulfur research
(Chan et al., 2011; Chao et al., 2014). GWAS demonstrate their
power not only in identifying genes responsible for variation in,
for example, sulfate content or glucosinolate composition, but
also in providing ideas and further questions about ecological
drivers of adaptations in sulfur metabolism. Several GWAS
have taken advantage of the development of the ionomics ap-
proach, a high-throughput method for determining the elem-
ental composition of plants (Chao et al., 2014). The impact of
ionomics on sulfur research has been demonstrated by the dis-
covery of a unique epigenetic regulatory mechanism (Huang
 Sulfur nutrition: impacts on plant development, metabolism, and stress responses  |  4071
et  al., 2016), and the approach also helps us understand the
interconnection of multiple nutrients, as described by Courbet
et al. (2019) in this special issue.
Much sulfur research in non-model plant species has been
aimed at addressing questions relevant to the agricultural impact
of sulfur and the traits connected with the nutritional quality of
crops.There are multiple examples presented in this special issue,
such as metabolism of non-proteinogenic sulfur-containing
amino acids in legumes (Joshi et  al. 2019), analysis of the ef-
fects of sulfur deficiency and water stress on protein compos-
ition in peas (Henriet et al., 2019), and a detailed examination
of the synthesis of organosulfur compounds in onion and garlic
(Yoshimoto and Saito, 2019). Interest in non-model species is
not limited to crops, and Jobe et al. (2019) present a review with
a focus on sulfur metabolism in C4 plants. However, despite this
diversification in the range of species that are being studied in
the post-genomic era, traditional topics and approaches in model
plant species still remain highly relevant in sulfur research.
Sulfate transport, metabolism, and
regulation: gene discovery and annotation
Elucidating the functions and regulation of transporters and
enzymes involved in sulfur metabolism has been the main re-
search topic for decades. A  collection of reviews in this spe-
cial issue illustrates recent progress and perspectives. Takahashi
(2019) presents the concept of regulatory coordination of
the signals that modulate the expression and activity of trans-
porters for sulfate uptake and internal distribution, while Jez
(2019) reviews the unique fine-tuned switching mechanisms
that control the activity of sulfur assimilatory enzymes that
have been found in studies based on protein structure ana-
lysis. Selles et al. (2019) address a less well-known component
of sulfur metabolism by discussing the diverse functionalities
of sulfurtransferases in sulfur metabolism and, more broadly,
in processes involved in mineral utilization. As noted above,
genome sequencing has contributed greatly to our know-
ledge and has increased the number of genes and proteins to
be functionally characterized.Transcriptomics, proteomics, and
metabolomics have then produced large and complex datasets.
Watanabe and Hoefgen (2019) provide an overview of such
data collections and indicate potential approaches to identify
novel gene or protein functions based on ‘omics’ data ana-
lyses. The majority of information on regulatory mechanisms
published in relation to sulfur research is derived from studies
that have explored the phenotypic consequences of genetic
alterations. Recent studies, however, indicate that epigenetic
regulatory mechanisms also have substantial impacts on the
pathways that control sulfate transport and utilization, as re-
viewed by Huang et al. (2019).
Growing attention is being paid to specialized sulfur-
containing metabolites that impart distinctive flavors and poten-
tial health benefits to food (Traka and Mithen, 2009; Nakabayashi
and Saito, 2017). However, many of these metabolites are often
specific to non-model plant species and while their uniqueness
in chemistry is of inherent interest, the lack of adequate gen-
omic sequence data has hitherto limited the power of gene dis-
covery. As noted above, progress in genome sequencing and the
increasing availability of transcriptome datasets now are now
helping us to study the molecular basis of these unique meta-
bolic traits in non-model species. Yoshimoto and Saito (2019)
highlight the biosynthesis of S-alk(en)ylcysteine sulfoxide in
the genus Allium and present predictive approaches that can be
implemented to identify reaction mechanisms and the relevant
pathway enzymes. Joshi et al. (2019) review pathways for bio-
synthesis of cysteine-derived non-proteinogenic sulfur amino
acids and their γ-glutamyl dipeptides and homoglutathione de-
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rivatives that are found in legume species.
The biosynthetic pathways for specialized sulfur-containing
metabolites begin with S-amino acids or via a connection with
the primary sulfate assimilation pathway at several steps down-
stream of derivatization. Because of these metabolic connec-
tions, the pathways for primary and specialized metabolism show
regulatory coordination that depends on sulfur availability and
the specific demands for the bioactive compounds. Amir et  al.
(2019) discuss the potential for enhancing the levels of the es-
sential amino acid methionine in seeds, either by increasing the
sink capacity of seed storage proteins or by manipulating the flux
of methionine synthesis and catabolism. Chan et al. (2019) re-
view sulfation of metabolites (e.g. glucosinolates), hormones, and
peptides as part of the specialized metabolism, and discuss their
regulatory coordination and possible cooperative roles in stress
mitigation, as they all require PAPS as the sulfate donor.
Sulfur assimilation in general plant
metabolism and growth regulation
Remarkable progress has been made in determining the path-
ways that control plant nutrient uptake, metabolism, and homeo-
stasis. However, the mechanisms that coordinate the acquisition
of individual nutrients and their integration in cellular metabolic
networks are less well understood. In this special issue, three re-
views summarize progress in understanding the integration of
sulfur nutrition with other nutrient uptake and metabolic path-
ways. Courbet et al. (2019) address the coordination of multiple
macro- and micronutrients from the perspective of a balanced
ionome. Mendoza-Cózatl et  al. (2019) discuss the interplay of
sulfur more specifically with a single nutrient, iron. A more gen-
eral integration of sulfur nutrition with primary plant product-
ivity is given by Jobe et al. (2019). From all three papers it may
be concluded that sulfur metabolism is necessarily modulated
for the improvement of various plant traits that are seemingly
not directly associated with sulfur. In line with this concept, the
activity of target-of-rapamycin (TOR) kinase has been shown
to control plant growth under sulfur-limited conditions (Dong
et al., 2017).The requirement for cysteine for the biosynthesis of
abscisic acid and subsequent stomatal closure implicates sulfur
nutrition and metabolism as being important for in plant water
relations (Batool et al., 2018).
Sulfur in redox signaling and stress
mitigation: impacts on plant growth and
development
Thiol groups of GSH and protein cysteine (Cys) residues are
essential for redox homeostasis of cells. Enzyme activity and
4072 | Kopriva et al.
protein function can be modulated by modification of Cys res-
idues. Several review articles in this special issue describe how
changes in redox status control sulfur assimilation together
with targets in other cellular processes to affect plant responses
under stress conditions. Telman and Dietz (2019) review redox
regulation of key enzymes in sulfur assimilation and discuss a
link between the sulfur and oxilipin signaling pathways. The
redox switches of these key enzymes are also discussed from
the structural perspective by Jez (2019). Gotor et  al. (2019)
highlight chemical features of sulfide and cyanide produced
in the sulfur assimilation and downstream metabolic pathways
that promote post-translational protein persulfidation and
S-cyanylation. Umbreen et al. (2019) discuss another example
of redox-based post-translational modification with a focus on
nitric oxide acting on S-nitrosation of protein Cys residues.
Chan et al. (2019) examine the roles of 3′-phosphoadenosine
5′-phosphate (PAP), a by-product of sulfation, in acting as a
retrograde signaling molecule to control abiotic stress responses.
The redox control of nucleotide phosphatase that is responsible
for PAP catabolism further indicates multifaceted connections
with sulfate assimilation (Chan et  al., 2016). Kaufmann and
Sauter (2019) provide an overview of peptide sulfation, with a
discussion of the key roles of sulfated small signaling peptides
in the regulation of plant immunity and developmental pro-
cesses, such as the formation of the Casparian strip in roots
(Doblas et al., 2017; Nakayama et al., 2017).
Two research articles in this special issue report new find-
ings in relation to the mitigation of abiotic and biotic stress.
Henriet et  al. (2019) describe the combinatorial effects of
water and sulfur limitation on reproductive growth, seed
production, and the seed transcriptome and proteome in
Pisum sativum, while Hunziker et al. (2019) report the dis-
covery of numerous plasmodesmata that form connections
between the glucosinolate storage cells (S-cells) and neigh-
boring cells that synthesize glucosinolate in the vasculature
of Arabidopsis.
Future directions
Our knowledge of sulfur metabolism has increased expo-
nentially in the past two decades. Similar to nitrogen and
phosphorus, sulfur is an element that is present in the macro-
molecules that are essential for plant growth and development,
such as amino acids, proteins, and membrane lipids. In face of
global sustainability issues, improvements in nutrient-use ef-
ficiency and yield performance are considered important tar-
gets of crop breeding in the 21st century. Sulfur is clearly one
of the essential macronutrients that needs to be studied. Sulfur
has unique features, for example it is indispensable for the ac-
tivities of redox modulators, and for some defense chemicals
and attractants that play important roles in stress mitigation,
and thus it affects crop productivity. Together with the im-
pact of sulfur metabolites on nutritional quality, this makes
sulfur research important for achieving global food security.
However, in order to be able to contribute to solving the
great challenges that we face in crop production, precise and
detailed information on biological and molecular mechanisms
needs to be collected and thoroughly analysed. Plant biology
and biochemistry are the core subject areas for the study of
these key biological questions – more specifically, we need to
understand the molecular functions of the genes, proteins, and
metabolites that are involved in sulfur sensing, signaling, me-
tabolism, and regulation.
Combinations of biochemistry, molecular genetics, gen-
omics, and systems biology will continue to drive fundamental
research, allowing us to develop ideas and strategies to explore
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new features of gene–protein–metabolite regulatory networks.
Integrative approaches using ‘omics’ tools and information re-
sources will further help us to build hypotheses and models to
be tested against empirical knowledge. Recent developments
in genome-editing technologies have great potential to ration-
alize ideas for trait improvement in crop breeding. However,
we may encounter major obstacles due to the complexities of
genome architecture, life-cycle, fertility, and feasibility for gen-
etic transformation of crop species.
Besides these technological issues, significant gaps in our
knowledge still remain in a number of areas. Given the im-
portance of the geochemical cycle of sulfur in nature, the roles
of sulfur nutrition and metabolites in the environmental adap-
tation of plants need to be studied with more attention given
to ecophysiological aspects. The effects of availabilities of other
mineral nutrients on sulfur utilization also need to be studied
in more detail by focusing on their interactions. The func-
tions of sulfur metabolites in assisting mutualistic interactions
between living organisms (i.e. microbes, animals, and plants)
are not fully understood. With the exception of a number of
known examples characterized so far for essential biological or
nutritional functions, the diversity of sulfur metabolites appears
to be an unexplored area worthy of further study in order to
build up a comprehensive ‘S-chemicals’ catalogue. Analyses of
proteomes, post-translational modifications, and protein struc-
tures are areas to be exploited to gain more information. Sulfur
has unique characteristics in various aspects, some of which
provide potential areas for practical applications, as summar-
ized in this special issue. We endeavor to explore the biology
of sulfur to gain further mechanistic understanding of plant
systems and networks in nature. This special issue is thus not a
final report of sulfur research but rather a summary of current
progress with future outlooks that illustrates the dynamic na-
ture of this topic.
Acknowledgements
Most of the contributions in this special issue derive from presentations
given at the 11th International Plant Sulfur Workshop held on 16–20th
September 2018 in Conegliano, Italy. We are grateful to the plant sulfur
research community, which has been actively supporting the workshop
series since the first meeting in 1989 in Groningen, in the Netherlands.
We also thank the Journal of Experimental Botany for supporting our
research community and for providing us with an opportunity to present
updates in this second special issue 15 years after the publication of the
first (Hawkesford, 2004).
Keywords: Plant nutrition, primary metabolism, redox regulation,
specialized metabolism, stress response, sulfur.
 Sulfur nutrition: impacts on plant development, metabolism, and stress responses  |  4073
Stanislav Kopriva1,*, , Mario Malagoli2,* and Hideki Takahashi3,*,
1 
Botanical Institute and Cluster of Excellence on Plant Sciences
(CEPLAS), University of Cologne, 50674 Cologne, Germany
2  Huang XY, Li M, Luo R, Zhao F-J, Salt DE. 2019. Epigenetic regulation of
Department of Agronomy, Food, Natural resources, Animals and
Environment, University of Padua, 35020 Legnaro, Italy
3 
Department of Biochemistry and Molecular Biology, Michigan
State University, East Lansing, MI 48824, USA
* Correspondence: skopriva@uni-koeln.de,
mario.malagoli@unipd.it, htakaha@msu.edu
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