1. Introduction

The role of sulfur in the resistance of crops against fungal diseases became obvious at the end of the 1980s when atmospheric sulfur depositions were so much reduced by clean air acts that sulfur deficiency became a widespread nutrient disorder in Western European agriculture and the infection of crops with certain diseases became increasingly obvious, mostly in Scotland and Germany [1]. The emission of sulfur oxides into the atmosphere was also dramatically reduced in Central Europe at the end of the last century, mainly due to modernization of thermal power stations and to the reduction in fossil fuel combustion. At the beginning of this century, the level of emission of different sulfur oxides (ingredients of acid rain) was reduced by more than 70% as compared to emissions in 1980 [2]. The reduction in anthropogenic sulfur deposition resulted in progressive sulfur deficiency in plant mineral nutrition. Therefore, sulfate salts were applied to fields to cover the sulfur demand of plants. Interestingly, such agricultural field experiments showed that soil-applied sulfur in the form of inorganic sulfate salts can markedly increase the disease resistance of crops against certain fungal pathogens. A significant repressive effect of soil-applied sulfur on the infection of oilseed rape with Pyrenopeziza brassicae, grapes with Uncinula necator, and potato tubers with Rhizoctonia solani was found ^[3][4][5][3–5]. These results led to the development of the concept of sulfur-induced resistance (SIR) ^[6][7][1,4,6,7]. This new disease resistance form has also been observed in pathophysiological and biochemical experiments using plants grown under controlled greenhouse conditions, when this phenomenon was described as sulfur-enhanced defense (SED) ^[8][5,8]. The concepts of SIR and SED describe the same phenomenon from different experimental approaches, from an agricultural and a plant biological point of view, respectively. In spite of numerous studies, the mechanisms underlying SIR/SED are, however, far from understood.

Acclimation and adaptation processes are crucial for plants to survive in changing environments and the goal for the plant is to optimize the use of available sulfur to match the demand for growth and development, and resistance to biotic and abiotic stress [9]. Sulfur requirements can vary among plant families. Members of the Brassicaceae are found to be the most sulfur-dependent group of plants, followed by Fabaceae and Poaceae [10]. The primary sulfur source of the plants are inorganic sulfate anions available from the soil [11]. The sulfate anion is taken up from the soil by specialized sulfate transporter proteins, which are localized in the epidermal cells of the roots [12]. Excess sulfate is transported to the leaves and is stored in vacuoles that constitute a large S reservoir for plant metabolism [13]. The transportation of sulfate within or between plant cells is also mediated by sulfate transporters [14]. Sulfate in plant cells is activated to form adenosine 5′-phosphosulfate, a process catalyzed by ATP sulfurylase [15]. The activated sulfate is reduced in a multistep pathway in which eight electrons are added to form sulfide through sulfite as an intermediate form [16]. Sulfide, together with O-acetylseryne (OAS), forms cysteine (Cys), a reaction catalyzed by two enzymes, serine acetyltransferase (SAT) and O-acetylserine(thiol)lyase (OASTL) [17]. In these processes the sulfur atom is ultimately incorporated into Cys, the first organic molecule carrying reduced sulfur and a central hub of SDC biosynthesis in plants ^{[18][19][20][21]}[18–21] (Figure 1).

Figure 1. Schematic representation of biosynthetic pathways of the most important sulfur-associated compounds in plants. Sulfur-associated compounds mentioned in this review are highlighted.

2. Conclusions

Conclusions

Sufficient levels of sulfur in soils confer the optimal plant uptake of inorganic sulfate salts,

a prerequisite for sulfur-containing defense compound (SDC) concentrations required for plant disease

resistance responses. Indeed, sufficient sulfur fertilization is generally reflected in higher contents

of SDCs, as well as a lower rate of infection compared to sulfur-deprived plants. In spite of the very

diverse chemical structures of SDCs, there are some similarities in their modes of action against

pathogens. SDCs are instrumental both in pathogen perception and initiating resistance-associated

signal transduction pathways. Importantly, these processes are interconnected with various defense

responses regulated by plant hormones (in particular, salicylic acid, jasmonic acid and ethylene),

NO and reactive oxygen species (ROS). Sulfur-derived metabolites are major participants of plant redox

metabolism and post-translational modifications as well as of detoxification processes. In fact,

the unique chemical properties of sulfur (S), occurring in a wide range of oxidation states in

various compounds, may contribute to the versatile roles of SDCs in plant resistance responses to

pathogens. On the other hand, diverse S-containing compounds also have specific roles. An important

characteristic of Cys is that it is the central hub of plant sulfur metabolism, in particular, Cys is

a precursor molecule of numerous SDCs. Met and the Met cycle is connected to DNA, RNA and

histone methylation reactions as well as to the biosynthesis of the plant hormone ethylene and

polyamines. GSH participates in antioxidative and detoxification reactions and conducts the signaling

of diff erent plant hormones during pathogen infection. Importantly, a self-regulating circuit of H2O2,

NO, glutathione and salicylic acid (SA) controls SA-mediated defense responses to bacterial and

fungal infections ^[22][23][24][96,98–100]. Future research should clarify whether the same/similar self-regulating

signaling is also responsible for the efficiency of SA-mediated plant defense responses during viral

infections. Cysteine-rich peptides like defensins and thionins show direct antimicrobial eff ects and

have additional roles in plant growth and development. Phytoanticipins are preformed SDCs which

are already present before the plant is attacked, or which are produced rapidly and spontaneously

from a preformed substrate by simple chemical or enzymatic modifications via a pre-existing enzyme.

A unique characteristic of RSS is S-sulfhydration or persulfidation of redox-sensitive cysteine residues

in various defense-associated proteins.

S The future engineering of these sulfur-assoccesiated redox-switches by,

e.g., gene editing sfhoul plant d enable a temporally and spatially targeted induction of defense responses of

crops to a gainstiven pathogen.

References

1. attaSck (i.e., resistance) is often associatehnug, E.; Haneklaus, S. Diagnosis of sulphur nutrition. In Sulphur in Agroecosystems. Nutrients in Ecosystems;

Schnug, E., Ed.; with enhancedSpringer: Dordrecht, The Netherlands, 1998; Volume 2, pp. 1–38. ISBN 978-94-011-5100-9.

2. ROSyant, P.; Dolezelova, E.; productiFabrik, I.; Baloun, J.; Adam, V.; Babula, P.; Kizek, R. Electrochemical determination

of (low molecular mass thiols coxidative burst). In thintent in potatoes (Solanum tuberosum) cultivated in the presence of various

sulphur foregard, the recent ms and infected by late blight (Phytophora infestans). Sensors 2008, 8, 3165–3182. [CrossRef]

[PubMed]

3. Bloem, E.; Riemenscovery of the first extracelhneider, A.; Volker, J.; Papenbrock, J.; Schmidt, A.; Salac, I.; Haneklaus, S.; Schnug, E.

Sulphular H₂O₂r supply and infection with Pyrenopeziza brassicae rinfluenceceptor (HPCA1) L-cysteine desulphydrase activity in

Brassica naplantus ^[25]L. J. Exprovid. Bot. 2004, 55, 2305–2312. [CrossRef] [PubMed]

4. Bloem, E.; Haneklaus a missing link to the, S.; Salac, I.; Wickenhäuser, P.; Schnug, E. Facts and fiction about sulfur metabolism in

relation to plant-pa operation of thogen interactions. Plant Biol. 2007, 9, 596–607. [CrossRef] [PubMed]

5. Kruse, C.; Jo-called ROS wst, R.; Lipschis, M.; Kopp, B.; Hartmann, M.; Hell, R. Sulfur-enhanced defence: E ects of sulfur

metavbolism, nitroges. These ROn supply, and pathogen lifestyle. Plant Biol. 2007, 9, 608–619. [CrossRef]

6. Dubuis, P.H.; Marazzi, C.; Städler, producing waves are initiaE.; Mauch, F. Sulphur deficiency causes a reduction in antimicrobial

potedntial upon stress-exposure and confer a and leads to increased disease susceptibility of oilseed rape. J. Phytopathol. 2005, 153, 27–36.

[CrapidossRef]

7. Bloem, E.; H₂O₂-manediklated cell-to-cell defense sigus, S.; Schnug, E. Milestones in plant sulfur research on sulfur-induced-resistance (SIR) in

Europe. Front. Plaling. ROSnt Sci. 2015, 5, 779. [CrossRef]

8. bKrursts ultimately rese, C.; Haas, F.H.; Jost, R.; Reiser, B.; Reichelt, M.;Wirtz, M.; Gershenzon, J.; Schnug, E.; Hell, R. Improved

sulfur nutrit in different types of reversible oxidation (disulfide foion provides the basis for enhanced production of sulfur-containing defense compounds in

Armation, sulfenylation, glutathionylation) ofbidopsis thaliana upon inoculation with Alternaria brassicicola. J. Plant Physiol. 2012, 169, 740–743. [CrossRef]

9. cysCapaldi, F.R.; Grateine (Cys) residuão, P.L.; Reis, A.R.; Lima, L.W.; Azevedo, R.A. Sulfur metabolism and stress defense

res pon variousses in plant proteins. Theses. Trop. Plant Biol. 2015, 8, 60–73. [CrossRef]

10. plAarabi, F.; Naant redox modifications (redoxome) have profouke, T.; Fernie, A.R.; Hoefgen, R. Coordinating sulfur pools under sulfate deprivation.

Trends efPlant Sci. 2020, 25, 1227–1239. [CrossRef]

11. Hawkesford, M.; Horst, W.; Kichects on y, T.; Lambers, H.; Schjoerring, J.; Møller, I.S.; White, P. Functions of

macronultiple protein functions like ctrients. In Marschner’s Mineral Nutrition of Higher Plants, 3rd ed.; Marschner, P., Ed.; Elsevier Inc.:

Amsterdam, The Netalytherlands, 2011; pp. 135–189, ISBN 9780123849052.

12. Takahashic, H.; activity, subcellular locaKopriva, S.; Giordano, M.; Saito, K.; Hell, R. Sulfur assimilation in photosynthetic organisms:

Molecular functization and, last but not lons and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 2011,

62, 157–184. [CrossRef]

13. Iqbal, N.; Mast, the signal traood, A.; Khan, M.I.R.; Asgher, M.; Fatma, M.; Khan, N.A. Cross-talk between sulfur assimilations

anduc etion ofhylene signaling in plant defense res. Plant Signal. Behav. 2013, 8, e22478. [CrossRef] [PubMed]

14. Gigolashvili, T.; Koponses during pathogriva, S. Transporters in plant sulfur metabolism. Front. Plant Sci. 2014, 5, 442. [CrossRef]

[PubMend]

15. Prinfections. However, the impact of pathoretti, L.; Gontero, B.; Hell, R.; Giordano, M. Diversity and regulation of ATP sulfurylase in photosynthetic

orgen-triggeredanisms. Front. Plant Sci. 2014, 5, 597. [CrossRef] [PubMed]

16. ROLeustek, T.; S bursts and, in particular, SDCsaito, K. Sulfate transport and assimilation in plants. Plant Physiol. 1999, 120, 637–643. [CrossRef]

17. oWatan the diverse oxidative cysteine modificatioabe, M.; Hubberten, H.M.; Saito, K.; Hoefgen, R. General regulatory patterns of plant promineral nutrient

depletins is still only partially characterized. The futuon as revealed by serat quadruple mutants disturbed in cysteine synthesis. Mol. Plant 2010, 3, 438–466.

[CrossRef]

18. Lengineering of these ustek, T.; Martin, M.N.; Bick, J.A.; Davies, J.P. Pathways and regulation of sulfur-associa metabolism revealed

through moled redox-switches by, e.g., genecular and genetic studies. Annu. Rev. Plant Biol. 2000, 51, 141–165. [CrossRef]

19. Saito, K. Rediting should enable a temporally and spagulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant

Biaolly targeted. 2000, 3, 188–195. [CrossRef]

20. Nakainduction of defense responses , Y.; Maruyama-Nakashita, A. Biosynthesis of sulfur-containing small biomolecules in plants. Int. J.

Mofl. cropsSci. 2020, 21, 3470. [CrossRef]   

21. Álvarez, C.; Bermúdez, M.Á.; Romero, L.C.; Goto a givr, C.; García, I. Cysteine homeostasis plays an essential role

in plathogen.

nt immunity. New Phytol. 2012, 193, 165–177.    [CrossRef]