Sulfur in Plant Defense: Comparison
Please note this is a comparison between Version 2 by Bruce Ren and Version 1 by Lorant Kiraly.

Sulfur (S) is an essential plant macronutrient and the pivotal role of sulfur compounds in plant disease resistance has become obvious in recent decades. These compounds include sulfur containing amino acids such as cysteine and methionine, the tripeptide glutathione, thionins and defensins, glucosinolates and phytoalexins and, last but not least, reactive sulfur species and hydrogen sulfide. SDCs play versatile roles both in pathogen perception and initiating signal transduction pathways that are interconnected with various defense processes regulated by plant hormones (salicylic acid, jasmonic acid and ethylene) and reactive oxygen species (ROS). Importantly, ROS-mediated reversible oxidation of cysteine residues on plant proteins have profound effects on protein functions like signal transduction of plant defense responses during pathogen infections. Indeed, the multifaceted plant defense responses initiated by SDCs should provide novel tools for plant breeding to endow crops with efficient defense responses to invading pathogens.

  • cysteine
  • defensin
  • glucosinolate
  • glutathione
  • hydrogen peroxide
  • hydrogen sulfide
  • reactive sulfur species
  • salicylic acid
  • sulfur-containing defense compounds
  • thionin

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 [3–5][3][4][5]. These results led to the development of the concept of sulfur-induced resistance (SIR) [1,4,6,7][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) [5,8][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 [18–21][18][19][20][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.

Conclusions

2. 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 di fferent 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 [96,98–100][22][23][24]. 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 e ffects 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. The f

Suturcce engineering of these sulfur-associated redox-switches by,

ssful plant defense.g., gene editing should enable a temporally and spatially targeted induction of defense responses of

against pathogen attack (i.e., resistance) is often assocrops iato a given pathogen.

References

1. Sced with enhnug, E.; Haneklaus, S. Diagnosis of sulphur nutrition. In Sulphur in Agroecosystems. Nutrients in Ecosystems;

Schnug, E.,ced ROS production (oxidative burst). In this Ed.; Springer: Dordrecht, The Netherlands, 1998; Volume 2, pp. 1–38. ISBN 978-94-011-5100-9.

2. Regard, the recent discoveryant, P.; Dolezelova, E.; Fabrik, I.; Baloun, J.; Adam, V.; Babula, P.; Kizek, R. Electrochemical determination

of of the first extracelow molecular massular H2O2 recepthiols content in potatoeor (HPCA1) in plants (Solanum[25] tubeprosum) cultivated in the presence of variouvides a mis

sulphur forms aind infected by late blight (Phytophora infestans). Sensors 2008, 8, 3165–3182. [CrossRef]

[PubMed]

3.g link to the in planta operation of Blsoem, E.; Riemenschneider, A.; Volker, J.; Papenbrock, J.; Schmidt, A.; Salac, I.; Haneklaus, S.; Schnug, E.

Sul-called ROS waves. These ROS phur supply and infection with Pyrenopeziza brassicae influence L-cysteine desulphydrase activity ioducing waves are initiated upon

Brassica napus L. J. Exp. Bot. 2004, 55, 2305–2312. [CrossRef] [PubMed]

4. Bltress-expoem, E.; Haneklaus, S.; Salac, I.; Wickenhäuser, P.; Schnug, E. Facts and fiction about sulfur metabolism in

ure and confer a relation to plantpid, H2O2-pathogmen interactions. Plant Biol. 2007, 9, 596–607. [CrossRef] [PubMed]

5.diated Kruse, C.; Jost, R.; Lipschis, M.; Kopp, B.; Hartmann, M.; Hell, R. Sulfur-enhancedell-to-cell defence: E ects of sulfur

metabolse sism, nitrogen supply, and pathogen lifestyle. Plant Biol. 2007, 9, 608–619. [CrossRef]

6.naling. ROS bursts Dubuis, P.H.; Marazzi, C.; Städler, E.; Mauch, F. Sulphur deficiency causes a reduction in antimicrobial

potltimately result in differential and leads to increased disease susceptibility of oilseed rape. J. Phytopathol. 2005, 153, 27–36.

[Crotypes of reversible oxidation (disulfide formation, ssReulf]

7. Bloem, E.; Haneklaus, S.; Schnug, E. Milestones in plant sulfur research on sulfur-induced-resistance (SIR) in

Eylation, glutathionylation) of cysteine (Cys) residurope. Front. Plant Sci. 2015, 5, 779. [CrossRef]

8. Krs on variouse, C.; Haas, F.H.; Jost, R.; Reiser, B.; Reichelt, M.;Wirtz, M.; Gershenzon, J.; Schnug, E.; Hell, R. Improveplant proteins. These plant redox mod

sulifur nutrition provides the basis for enhanced production of sulfur-containing defense compounds in

Acations (redoxome) have profound effects on multiple prabidopsis thaliana upon inoculation with Alternaria brassicicola. J. Plant Physiol. 2012, 169, 740–743. [CrossRef]

9. Captein functions like cataldyti, F.R.; Gratão, P.L.; Reis, A.R.; Lima, L.W.; Azevedo, R.A. Sulfur metabolism and stress defense

responses in pc activity, subcellular lants. Trop. Plant Biol. 2015, 8, 60–73. [CrossRef]

10. Aarabcali, F.; Nzaake, T.; Fernie, A.R.; Hoefgen, R. Coordinating sulfur pools under sulfate deprivation.

Trendstion and, last but Plant Sci. 2020, 25, 1227–1239. [CrossRef]

11. Hot leawkesford, M.; Horst, W.; Kichey, T.; Lambers, H.; Schjoerring, J.; Møller, I.S.; White, P. Functions of

mact, the signal tronutrients. In Marschner’s Mineral Nutritnsduction of Higher Plants, 3rd ed.; Marschner, P., Ed.; Elsevier Inc.:

Amsteplant defense rdam, The Netherlands, 2011; pp. 135–189, ISBN 9780123849052.

12. Takahashi, H.; Kspopriva, S.; Giordano, M.; Saito, K.; Hell, R. Sulfur assimilation in photosynthetic organisms:

Molses during pathogecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 2011,

62, 157–184. [CrossR infections. Howevef]

13. Iqbal, N.; Masood, A.; Khan, M.I.R.; Asgher, M.; Fatma, M.; Khan, N.A. Cross-talk between sulfur assimilation

he impact of pand ethylene signaling in plants. Plant Signal. Behav. 2013, 8, e22478. [CrossRef] [PubMed]

14.ogen-triggered Gigolashvili, T.; Kopriva, ROS. Transporters in plant sulfur metabolism. Front. Plant Sci. 2014, 5, 442. [CrossRef]

[PubMed]

15. bursts and, in particular, SDCs Prioretti, L.; Gontero, B.; Hell, R.; Giordano, M. Diversity and regulation of ATP sulfurylase in photosynthetic

n the diverse oxidative cysteine modificatiorganisms. Front. Plant Sci. 2014, 5, 597. [CrossRef] [PubMed]

16. Leuss of plant protek, T.; Saito, K. Sulfate transport and assimilation in plants. Plant Physiol. 1999, 120, 637–643. [CrossRef]

17. Wns is still only patanabe, M.; Hubberten, H.M.; Saito, K.; Hoefgen, R. General regulatory patterns of plant mineral nutrient

ially characterizedepletion. as revealed by serat quadruple mutants disturbed in cysteine synthesis. Mol. Plant 2010, 3, 438–466.

[CrThe future engineering ossRef]

18. Leustek, T.; Martin, M.N.; Bick, J.A.; Davies, J.P. Pathways and regulation of hese sulfur metabolism reveal-associated

th rough molecular and genetic studies. Annu. Rev. Plant Biol. 2000, 51, 141–165. [CrossRef]

19. Sadox-switches by, e.g., gene edito, K. Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Planng should enable a temporally and spat

Bioall. 2000, 3, 188–195. [CrossRef]

20.y targeted Nakai, Y.; Maruyama-Nakashita, A. Biosynthesis of sulfur-containing small biomolecules in plants. Int. J.

Mnduction of defense responses ol.f Sci. 2020, 21, 3470. [CrossRef]   

21.crops Álvarez, C.; Bermúdez, M.Á.; Romero, L.C.; Gotor, C.; García, I. Cysteine homeostasis plays an essential rol a given pathoge

in plant immunity. New Phytol. 2012, 193, 165–177.

    [CrossRef]                                                                                                                                                                      

 

References

  1. Schnug, E.; Haneklaus, S. Diagnosis of sulphur nutrition. In Sulphur in Agroecosystems. Nutrients in Ecosystems; Schnug, E., Ed.; Springer: Dordrecht, The Netherlands, 1998; Volume 2, pp. 1–38, ISBN 978-94-011-5100-9.
  2. Ryant, P.; Dolezelova, E.; Fabrik, I.; Baloun, J.; Adam, V.; Babula, P.; Kizek, R. Electrochemical determination of low molecular mass thiols content in potatoes (Solanum tuberosum) cultivated in the presence of various sulphur forms and infected by late blight (Phytophora infestans). Sensors 2008, 8, 3165–3182, doi:10.3390/s8053165.
  3. Bloem, E.; Riemenschneider, A.; Volker, J.; Papenbrock, J.; Schmidt, A.; Salac, I.; Haneklaus, S.; Schnug, E. Sulphur supply and infection with Pyrenopeziza brassicae influence L-cysteine desulphydrase activity in Brassica napus L. J. Exp. Bot. 2004, 55, 2305–2312, doi:10.1093/jxb/erh236.
  4. Bloem, E.; Haneklaus, S.; Salac, I.; Wickenhäuser, P.; Schnug, E. Facts and fiction about sulfur metabolism in relation to plant-pathogen interactions. Plant Biol. 2007, 9, 596–607, doi:10.1055/s-2007-965420.
  5. Kruse, C.; Jost, R.; Lipschis, M.; Kopp, B.; Hartmann, M.; Hell, R. Sulfur-enhanced defence: Effects of sulfur metabolism, nitrogen supply, and pathogen lifestyle. Plant Biol. 2007, 9, 608–619, doi:10.1055/s-2007-965432.
  6. Dubuis, P.H.; Marazzi, C.; Städler, E.; Mauch, F. Sulphur deficiency causes a reduction in antimicrobial potential and leads to increased disease susceptibility of oilseed rape. J. Phytopathol. 2005, 153, 27–36, doi:10.1111/j.1439-0434.2004.00923.x.
  7. Bloem, E.; Haneklaus, S.; Schnug, E. Milestones in plant sulfur research on sulfur-induced-resistance (SIR) in Europe. Front. Plant Sci. 2015, 5, 779, doi:10.3389/fpls.2014.00779.
  8. Kruse, C.; Haas, F.H.; Jost, R.; Reiser, B.; Reichelt, M.; Wirtz, M.; Gershenzon, J.; Schnug, E.; Hell, R. Improved sulfur nutrition provides the basis for enhanced production of sulfur-containing defense compounds in Arabidopsis thaliana upon inoculation with Alternaria brassicicola. J. Plant Physiol. 2012, 169, 740–743, doi:10.1016/j.jplph.2011.12.017.
  9. Capaldi, F.R.; Gratão, P.L.; Reis, A.R.; Lima, L.W.; Azevedo, R.A. Sulfur metabolism and stress defense responses in plants. Trop. Plant Biol. 2015, 8, 60–73, doi:10.1007/s12042-015-9152-1.
  10. Aarabi, F.; Naake, T.; Fernie, A.R.; Hoefgen, R. Coordinating sulfur pools under sulfate deprivation. Trends Plant Sci. 2020, 25, 1227–1239, doi:10.1016/j.tplants.2020.07.007.
  11. Hawkesford, M.; Horst, W.; Kichey, T.; Lambers, H.; Schjoerring, J.; Møller, I.S.; White, P. Functions of macronutrients. In Marschner’s Mineral Nutrition of Higher Plants, 3rd ed.; Marschner, P., Ed.; Elsevier Inc.: Amsterdam, The Netherlands, 2011; pp. 135–189, ISBN 9780123849052.
  12. Takahashi, H.; Kopriva, S.; Giordano, M.; Saito, K.; Hell, R. Sulfur assimilation in photosynthetic organisms: Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 2011, 62, 157–184, doi:10.1146/annurev-arplant-042110-103921.
  13. Iqbal, N.; Masood, A.; Khan, M.I.R.; Asgher, M.; Fatma, M.; Khan, N.A. Cross-talk between sulfur assimilation and ethylene signaling in plants. Plant Signal. Behav. 2013, 8, e22478, doi:10.4161/psb.22478.
  14. Gigolashvili, T.; Kopriva, S. Transporters in plant sulfur metabolism. Front. Plant Sci. 2014, 5, 442, doi:10.3389/fpls.2014.00442.
  15. Prioretti, L.; Gontero, B.; Hell, R.; Giordano, M. Diversity and regulation of ATP sulfurylase in photosynthetic organisms. Front. Plant Sci. 2014, 5, 597, doi:10.3389/fpls.2014.00597.
  16. Leustek, T.; Saito, K. Sulfate transport and assimilation in plants. Plant Physiol. 1999, 120, 637–643, doi:10.1104/pp.120.3.637.
  17. Watanabe, M.; Hubberten, H.M.; Saito, K.; Hoefgen, R. General regulatory patterns of plant mineral nutrient depletion as revealed by serat quadruple mutants disturbed in cysteine synthesis. Mol. Plant 2010, 3, 438–466, doi:10.1093/mp/ssq009.
  18. Leustek, T.; Martin, M.N.; Bick, J.A.; Davies, J.P. Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Biol. 2000, 51, 141–165, doi:10.1146/annurev.arplant.51.1.141.
  19. Saito, K. Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant Biol. 2000, 3, 188–195, doi:10.1016/S1369-5266(00)00063-7.
  20. Nakai, Y.; Maruyama-Nakashita, A. Biosynthesis of sulfur-containing small biomolecules in plants. Int. J. Mol. Sci. 2020, 21, 3470, doi:10.3390/ijms21103470.
  21. Álvarez, C.; Bermúdez, M.Á.; Romero, L.C.; Gotor, C.; García, I. Cysteine homeostasis plays an essential role in plant immunity. New Phytol. 2012, 193, 165–177, doi:10.1111/j.1469-8137.2011.03889.x.
  22. Kovacs, I.; Durner, J.; Lindermayr, C. Crosstalk between nitric oxide and glutathione is required for nonexpressor of pathogenesis-related GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol. 2015, 208, 860–872, doi:10.1111/nph.13502.
  23. Feechan, A.; Kwon, E.; Yun, B.W.; Wang, Y.; Pallas, J.A.; Loake, G.J. A central role for S-nitrosothiols in plant disease resistance. Proc. Natl. Acad. Sci. USA 2005, 102, 8054–8059, doi:10.1073/pnas.0501456102.
  24. Zhang, T.; Ma, M.; Chen, T.; Zhang, L.; Fan, L.; Zhang, W.; Wei, B.; Li, S.; Xuan, W.; Noctor, G.; et al. Glutathione-dependent denitrosation of GSNOR1 promotes oxidative signalling downstream of H2O2. Plant Cell Environ. 2020, 43, 1175–1191, doi:10.1111/pce.13727.
  25. Wu, F.; Chi, Y.; Jiang, Z.; Xu, Y.; Xie, L.; Huang, F.; Wan, D.; Ni, J.; Yuan, F.; Wu, X.; et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 2020, 578, 577–581, doi:10.1038/s41586-020-2032-3.
More
Video Production Service