Hydrogen sulfide in plants: From dissipation of excess sulfur to signaling molecule

Nitric Oxide - Biology and Chemistry

Volumn 41, Issue , 2014, Pages 72-78

  Calderwood, Alexander ^a   Kopriva, Stanislav ^a,b  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Cysteine; Hydrogen sulfide; Plants; Signaling; Sulfate assimilation

Indexed keywords

ACETYL COENZYME A; CYSTEINE; CYSTEINE SYNTHASE; HYDROGEN SULFIDE; ORGANIC COMPOUND; SULFITE REDUCTASE; SULFUR;

AIR POLLUTION; COMPLEX FORMATION; DROUGHT STRESS; GLUTATHIONE METABOLISM; HUMAN; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PHYSIOLOGY; PLANT DEFENSE; PLANT GROWTH; PLANT METABOLISM; PLANT NUTRITION; PLANT STRESS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNTHESIS; METABOLISM; PLANT;

ALGAE; ANIMALIA; FUNGI; PROKARYOTA;

CYSTEINE; HYDROGEN SULFIDE; PLANTS; SIGNAL TRANSDUCTION;

EID: 84907598746     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2014.02.005     Document Type: Review

References (97)

1. J. Bradbury, Medicine nobel prize awarded to US pharmacologists, Lancet 352 (1998) 1287.
2. L.J. Ignarro, G.M. Buga, K.S. Wood, R.E. Byrns, G. Chaudhuri, Endotheliumderived relaxing factor produced and released from artery and vein is nitric oxide, Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 9265-9269.
3. R.M. Palmer, A.G. Ferrige, S. Moncada, Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor, Nature 327 (1987) 524-526.
4. M. Delledonne, Y. Xia, R.A. Dixon, C. Lamb, Nitric oxide functions as a signal in plant disease resistance, Nature 394 (1998) 585-588.
5. J. Durner, D. Wendehenne, D.F. Klessig, Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose, Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 10328-10333.
6. B. Almeida, S. Buttner, S. Ohlmeier, A. Silva, A. Mesquita, B. Sampaio-Marques, N.S. Osorio, A. Kollau, B. Mayer, C. Leao, J. Laranjinha, F. Rodrigues, F. Madeo, P. Ludovico, NO-mediated apoptosis in yeast, J. Cell Sci. 120 (2007) 3279-3288.
7. L. Xue, G. Farrugia, S.M. Miller, C.D. Ferris, S.H. Snyder, J.H. Szurszewski, Carbon monoxide and nitric oxide as coneurotransmitters in the enteric nervous system: evidence from genomic deletion of biosynthetic enzymes, Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 1851-1855.
8. Y. Kimura, H. Kimura, Hydrogen sulfide protects neurons from oxidative stress, FASEB J. 18 (2004) 1165-1167.
9. N. Hogg, Nitric oxide expands scope to cover hydrogen sulfide and carbon monoxide, Nitric Oxide 35 (2013) 1.
10. M. Lisjak, T. Teklic, I.D. Wilson, M. Whiteman, J.T. Hancock, Hydrogen sulfide: environmental factor or signalling molecule?, Plant Cell Environ 36 (2013) 1607-1616.
11. C. Garcia-Mata, L. Lamattina, Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange, Plant Sci. 201-202 (2013) 66-73.
12. H. Takahashi, S. Kopriva, M. Giordano, K. Saito, R. Hell, Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes, Annu. Rev. Plant Biol. 62 (62) (2011) 157-184.
13. H. Takahashi, Regulation of sulfate transport and assimilation in plants, Int. Rev. Cell Mol. Biol. 281 (2010) 129-159.
14. M. Wirtz, R. Hell, Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties, J. Plant Physiol. 163 (2006) 273-286.
15. S. Krueger, A. Niehl, M.C. Lopez Martin, D. Steinhauser, A. Donath, T. Hildebrandt, L.C. Romero, R. Hoefgen, C. Gotor, H. Hesse, Analysis of cytosolic and plastidic serine acetyltransferase mutants and subcellular metabolite distributions suggests interplay of the cellular compartments for cysteine biosynthesis in Arabidopsis, Plant Cell Environ. 32 (2009) 349-367.
16. S. Kopriva, S.G. Mugford, C. Matthewman, A. Koprivova, Plant sulfate assimilation genes: redundancy versus specialization, Plant Cell Rep. 28 (2009) 1769-1780.
17. C. Heeg, C. Kruse, R. Jost, M. Gutensohn, T. Ruppert, M. Wirtz, R. Hell, Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis, Plant Cell 20 (2008) 168-185.
18. M. Watanabe, K. Mochida, T. Kato, S. Tabata, N. Yoshimoto, M. Noji, K. Saito, Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis, Plant Cell 20 (2008) 2484-2496.
19. M. Wirtz, R. Hell, The role of cellular compartmentation for sulfur amino acid biosynthesis, Amino Acids 33 (2007). Xxxvii-Xxxvii.
20. H.W. Heldt, K. Werdan, M. Milovanc, G. Geller, Alkalization of chloroplast stroma caused by light-dependent proton flux into thylakoid space, Biochim. Biophys. Acta 314 (1973) 224-241.
21. S. Kopriva, A. Koprivova, Plant adenosine 50-phosphosulphate reductase: The past, the present, and the future, J. Exp. Bot. 55 (2004) 1775-1783.
22. A. Schmidt, Sulfate reduction in a cell-free system of Chlorella. The ferredoxin dependent reduction of a protein-bound intermediate by a thiosulfonate reductase, Arch. Mikrobiol. 93 (1973) 29-52.
23. M.S. Khan, F.H. Haas, A.A. Samami, A.M. Gholami, A. Bauer, K. Fellenberg, M. Reichelt, R. Hansch, R.R. Mendel, A.J. Meyer, M. Wirtz, R. Hell, Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana, Plant Cell 22 (2010) 1216-1231.
24. U. Scheerer, R. Haensch, R.R. Mendel, S. Kopriva, H. Rennenberg, C. Herschbach, Sulphur flux through the sulphate assimilation pathway is differently controlled by adenosine 50-phosphosulphate reductase under stress and in transgenic poplar plants overexpressing gamma-ECS, SO, or APR, J. Exp. Bot. 61 (2010) 609-622.
25. M. Wirtz, M. Droux, R. Hell, O-acetylserine (thiol) lyase: An enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana, J. Exp. Bot. 55 (2004) 1785-1798.
26. A. Riemenschneider, K. Riedel, R. Hoefgen, J. Papenbrock, H. Hesse, Impact of reduced O-acetylserine(thiol)lyase isoform contents on potato plant metabolism, Plant Physiol. 137 (2005) 892-900.
27. H.M. Harrington, I.K. Smith, Cysteine metabolism in cultured tobacco cells, Plant Physiol. 65 (1980) 151-155.
28. C. Alvarez, L. Calo, L.C. Romero, I. Garcia, C. Gotor, An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis, Plant Physiol. 152 (2010) 656-669.
29. T.N. Akopyan, A.E. Braunstein, E.V. Goryachenkova, Beta-cyanoalanine synthase: purification and characterization, Proc. Natl. Acad. Sci. U.S.A. 72 (1975) 1617-1621.
30. Y. Hatzfeld, A. Maruyama, A. Schmidt, M. Noji, K. Ishizawa, K. Saito, Betacyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis, Plant Physiol. 123 (2000) 1163-1171.
31. A.G. Warrilow, M.J. Hawkesford, Cysteine synthase (O-acetylserine (thiol) lyase) substrate specificities classify the mitochondrial isoform as a cyanoalanine synthase, J. Exp. Bot. 51 (2000) 985-993.
32. A. Riemenschneider, R. Wegele, A. Schmidt, J. Papenbrock, Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana, FEBS J. 272 (2005) 1291-1304.
33. C.R. Thompson, G. Kats, Effects of continuous hydrogen sulphide fumigation on crop and forest plants, Environ. Sci. Technol. 12 (1978) 550-553.
34. L.P. Lamers, L.L. Govers, I.C. Janssen, J.J. Geurts, M.E. Van der Welle, M.M. Van Katwijk, T. Van der Heide, J.G. Roelofs, A.J. Smolders, Sulfide as a soil phytotoxin-a review, Front Plant Sci. 4 (2013) 268.
35. D. Yarmolinsky, G. Brychkova, R. Fluhr, M. Sagi, Sulfite reductase protects plants against sulfite toxicity, Plant Physiol. 161 (2013) 725-743.
36. C.E. Stuiver, L.J. De Kok, Atmospheric H(2)S as sulfur source for Brassica oleracea: kinetics of H(2)S uptake and activity of O-acetylserine (thiol)lyase as affected by sulfur nutrition, Environ. Exp. Bot. 46 (2001) 29-36.
37. A. Riemenschneider, V. Nikiforova, R. Hoefgen, L.J. De Kok, J. Papenbrock, Impact of elevated H(2)S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism, Plant Physiol. Biochem. 43 (2005) 473-483.
38. C. Brunold, W. Landolt, P. Lavanchy, SO2 and assimilatory sulfate reduction in beech leaves, Physiol. Plant. 59 (1983) 313-318.
39. G. Brychkova, Z. Xia, G. Yang, Z. Yesbergenova, Z. Zhang, O. Davydov, R. Fluhr, M. Sagi, Sulfite oxidase protects plants against sulfur dioxide toxicity, Plant J. 50 (2007) 696-709.
40. T. Eilers, G. Schwarz, H. Brinkmann, C. Witt, T. Richter, J. Nieder, B. Koch, R. Hille, R. Hansch, R.R. Mendel, Identification and biochemical characterization of Arabidopsis thaliana sulfite oxidase. A new player in plant sulfur metabolism, J. Biol. Chem. 276 (2001) 46989-46994.
41. M. Durenkamp, L.J. De Kok, Impact of pedospheric and atmospheric sulphur nutrition on sulphur metabolism of Allium cepa L., a species with a potential sink capacity for secondary sulphur compounds, J. Exp. Bot. 55 (2004) 1821- 1830.
42. A. Koralewska, C.E.E. Stuiver, F.S. Posthumus, S. Kopriva, M.J. Hawkesford, L.J. De Kok, Regulation of sulfate uptake, expression of the sulfate transporters Sultr1;1 and Sultr1;2, and APS reductase in Chinese cabbage (Brassica pekinensis) as affected by atmospheric H(2)S nutrition and sulfate deprivation, Funct. Plant Biol. 35 (2008) 318-327.
43. M. Durenkamp, L.J. De Kok, S. Kopriva, Adenosine 50-phosphosulphate reductase is regulated differently in Allium cepa L. and Brassica oleracea L. upon exposure to H2S, J. Exp. Bot. 58 (2007) 1571-1579.
44. H. Rennenberg, The fate of excess sulfur in higher plants, Annu. Rev. Plant Physiol. 35 (1984) 121-153.
45. E. Schnug, E.J. Evans, Monitoring of the sulfur supply of agricultural crops in northern Europe, Phyton 32 (1992) 119-122.
46. M.Y. Hirai, T. Fujiwara, M. Awazuhara, T. Kimura, M. Noji, K. Saito, Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition, Plant J. 33 (2003) 651-663.
47. M.Y. Hirai, M. Klein, Y. Fujikawa, M. Yano, D.B. Goodenowe, Y. Yamazaki, S. Kanaya, Y. Nakamura, M. Kitayama, H. Suzuki, N. Sakurai, D. Shibata, J. Tokuhisa, M. Reichelt, J. Gershenzon, J. Papenbrock, K. Saito, Elucidation of gene-to-gene and metabolite-to-gene networks in arabidopsis by integration of metabolomics and transcriptomics, J. Biol. Chem. 280 (2005) 25590-25595.
48. V. Nikiforova, J. Freitag, S. Kempa, M. Adamik, H. Hesse, R. Hoefgen, Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity, Plant J. 33 (2003) 633- 650.
49. A. Maruyama-Nakashita, E. Inoue, A. Watanabe-Takahashi, T. Yamaya, H. Takahashi, Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways, Plant Physiol. 132 (2003) 597-605.
50. L.G. Wilson, R.A. Bressan, P. Filner, Light-dependent emission of hydrogen sulfide from plants, Plant Physiol. 61 (1978) 184-189.
51. H. Rennenberg, Role of o-acetylserine in hydrogen sulfide emission from pumpkin leaves in response to sulfate, Plant Physiol. 73 (1983) 560-565.
52. J. Sekiya, A. Schmidt, L.G. Wilson, P. Filner, Emission of hydrogen sulfide by leaf tissue in response to L-Cysteine, Plant Physiol. 70 (1982) 430-436.
53. E. Bloem, S. Haneklaus, I. Salac, P. Wickenhauser, E. Schnug, Facts and fiction about sulfur metabolism in relation to plant-pathogen interactions, Plant Biol (Stuttg) 9 (2007) 596-607.
54. J. Papenbrock, A. Riemenschneider, A. Kamp, H.N. Schulz-Vogt, A. Schmidt, Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants-from the field to the test tube and back, Plant Biol. (Stuttg) 9 (2007) 582-588.
55. T. Rausch, A. Wachter, Sulfur metabolism: A versatile platform for launching defence operations, Trends Plant Sci. 10 (2005) 503-509.
56. G. Noctor, C.H. Foyer, ASCORBATE AND GLUTATHIONE: keeping active oxygen under control, Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 (1998) 249-279.
57. B.A. Halkier, J. Gershenzon, Biology and biochemistry of glucosinolates, Annu. Rev. Plant Biol. 57 (2006) 303-333.
58. M.G. Jones, J. Hughes, A. Tregova, J. Milne, A.B. Tomsett, H.A. Collin, Biosynthesis of the flavour precursors of onion and garlic, J. Exp. Bot. 55 (2004) 1903-1918.
59. R. Rodriguez-Kabana, J.W. Jordan, J.P. Hollis, Nematodes: biological control in rice fields: role of hydrogen sulfide, Science 148 (1965) 524-526.
60. E. Bloem, S. Haneklaus, J. Kesselmeier, E. Schnug, Sulfur fertilization and fungal infections affect the exchange of H(2)S and COS from agricultural crops, J. Agric. Food Chem. 60 (2012) 7588-7596.
61. E. Bloem, A. Riemenschneider, J. Volker, J. Papenbrock, A. Schmidt, I. Salac, S. Haneklaus, E. Schnug, Sulphur supply and infection with Pyrenopeziza brassicae influence L-cysteine desulphydrase activity in Brassica napus L, J. Exp. Bot. 55 (2004) 2305-2312.
62. M. Wirtz, K.F.M. Beard, C.P. Lee, A. Boltz, M. Schwarzlander, C. Fuchs, A.J. Meyer, C. Heeg, L.J. Sweetlove, R.G. Ratcliffe, R. Hell, Mitochondrial cysteine synthase complex regulates O-acetylserine biosynthesis in plants, J. Biol. Chem. 287 (2012) 27941-27947.
63. M. Wirtz, H. Birke, C. Heeg, C. Muller, F. Hosp, C. Throm, S. Konig, A. Feldman- Salit, K. Rippe, G. Petersen, R.C. Wade, V. Rybin, K. Scheffzek, R. Hell, Structure and function of the hetero-oligomeric cysteine synthase complex in plants, J. Biol. Chem. 285 (2010) 32810-32817.
64. M. Droux, M.L. Ruffet, R. Douce, D. Job, Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants - Structural and kinetic properties of the free and bound enzymes, Eur. J. Biochem. 255 (1998) 235-245.
65. M. Droux, Plant serine acetyltransferase: new insights for regulation of sulphur metabolism in plant cells, Plant Physiol. Biochem. 41 (2003) 619-627.
66. J.A. Francois, S. Kumaran, J.M. Jez, Structural basis for interaction of Oacetylserine sulfhydrylase and serine acetyltransferase in the Arabidopsis cysteine synthase complex, Plant Cell 18 (2006) 3647-3655.
67. O. Berkowitz, M. Wirtz, A. Wolf, J. Kuhlmann, R. Hell, Use of biomolecular interaction analysis to elucidate the regulatory mechanism of the cysteine synthase complex from Arabidopsis thaliana, J. Biol. Chem. 277 (2002) 30629- 30634.
68. H. Birke, F.H. Haas, L.J. De Kok, J. Balk, M. Wirtz, R. Hell, Cysteine biosynthesis, in concert with a novel mechanism, contributes to sulfide detoxification in mitochondria of Arabidopsis thaliana, Biochem. J. 445 (2012) 275-283.
69. H. Zhang, L.Y. Hu, K.D. Hu, Y.D. He, S.H. Wang, J.P. Luo, Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress, J. Integr. Plant Biol. 50 (2008) 1518-1529.
70. H. Zhang, Z.Q. Tan, L.Y. Hu, S.H. Wang, J.P. Luo, R.L. Jones, Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings, J. Integr. Plant Biol. 52 (2010) 556-567.
71. J. Sun, R. Wang, X. Zhang, Y. Yu, R. Zhao, Z. Li, S. Chen, Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells, Plant Physiol. Biochem. 65 (2013) 67-74.
72. B.L. Wang, L. Shi, Y.X. Li, W.H. Zhang, Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings, Planta 231 (2010) 1301- 1309.
73. Z. Jin, J. Shen, Z. Qiao, G. Yang, R. Wang, Y. Pei, Hydrogen sulfide improves drought resistance in Arabidopsis thaliana, Biochem. Biophys. Res. Commun. 414 (2011) 481-486.
74. W. Cheng, L. Zhang, C. Jiao, M. Su, T. Yang, L. Zhou, R. Peng, R. Wang, C. Wang, Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum, Plant Physiol. Biochem. 70 (2013) 278-286.
75. A. Koprivova, S. Kopriva, D. Jager, B. Will, L. Jouanin, H. Rennenberg, Evaluation of transgenic poplars over-expressing enzymes of glutathione synthesis for phytoremediation of cadmium, Plant Biol. 4 (2002) 664-670.
76. A. Christou, G.A. Manganaris, I. Papadopoulos, V. Fotopoulos, Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways, J. Exp. Bot. 64 (2013) 1953-1966.
77. L. Ball, G.P. Accotto, U. Bechtold, G. Creissen, D. Funck, A. Jimenez, B. Kular, N. Leyland, J. Mejia-Carranza, H. Reynolds, S. Karpinski, P.M. Mullineaux, Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis, Plant Cell 16 (2004) 2448-2462.
78. F.D. Dooley, S.P. Nair, P.D. Ward, Increased growth and germination success in plants following hydrogen sulfide administration, PLoS ONE 8 (2013) e62048.
79. C. Garcia-Mata, L. Lamattina, Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress, Plant Physiol. 126 (2001) 1196-1204.
80. S.J. Neill, R. Desikan, A. Clarke, J.T. Hancock, Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells, Plant Physiol. 128 (2002) 13-16.
81. C. Garcia-Mata, L. Lamattina, Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling, New Phytol. 188 (2010) 977-984.
82. M. Lisjak, N. Srivastava, T. Teklic, L. Civale, K. Lewandowski, I. Wilson, M.E. Wood, M. Whiteman, J.T. Hancock, A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation, Plant Physiol. Biochem. 48 (2010) 931-935.
83. J. Shen, T. Xing, H. Yuan, Z. Liu, Z. Jin, L. Zhang, Y. Pei, Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by MicroRNA expressions, PLoS ONE 8 (2013) e77047.
84. Z. Jin, S. Xue, Y. Luo, B. Tian, H. Fang, H. Li, Y. Pei, Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis, Plant Physiol. Biochem. 62 (2013) 41-46.
85. Z. Hou, L. Wang, J. Liu, L. Hou, X. Liu, Hydrogen sulfide regulates ethyleneinduced stomatal closure in Arabidopsis thaliana, J. Integr. Plant Biol. 55 (2013) 277-289.
86. J.D. Rabinowitz, E. White, Autophagy and metabolism, Science 330 (2010) 1344-1348.
87. D.J. Klionsky, Autophagy: from phenomenology to molecular understanding in less than a decade, Nat. Rev. Mol. Cell Biol. 8 (2007) 931-937.
88. Y. Liu, D.C. Bassham, Autophagy: pathways for self-eating in plant cells, Annu. Rev. Plant Biol. 63 (2012) 215-237.
89. F. Li, R.D. Vierstra, Autophagy: A multifaceted intracellular system for bulk and selective recycling, Trends Plant Sci. 17 (2012) 526-537.
90. A.R. Thompson, R.D. Vierstra, Autophagic recycling: lessons from yeast help define the process in plants, Curr. Opin. Plant Biol. 8 (2005) 165-173.
91. Y.C. Wu, X.J. Wang, L. Yu, F.K. Chan, A.S. Cheng, J. Yu, J.J. Sung, W.K. Wu, C.H. Cho, Hydrogen sulfide lowers proliferation and induces protective autophagy in colon epithelial cells, PLoS ONE 7 (2012) e37572.
92. F. Talaei, V.M. van Praag, R.H. Henning, Hydrogen sulfide restores a normal morphological phenotype in Werner syndrome fibroblasts, attenuates oxidative damage and modulates mTOR pathway, Pharmacol. Res. 74 (2013) 34-44.
93. D. Wang, Y. Ma, Z. Li, K. Kang, X. Sun, S. Pan, J. Wang, H. Pan, L. Liu, D. Liang, H. Jiang, The role of AKT1 and autophagy in the protective effect of hydrogen sulphide against hepatic ischemia/reperfusion injury in mice, Autophagy 8 (2012) 954-962.
94. C. Alvarez, I. Garcia, I. Moreno, M.E. Perez-Perez, J.L. Crespo, L.C. Romero, C. Gotor, Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis, Plant Cell 24 (2012) 4621-4634.
95. K. Zientara-Rytter, J. Lukomska, G. Moniuszko, R. Gwozdecki, P. Surowiecki, M. Lewandowska, F. Liszewska, A. Wawrzynska, A. Sirko, Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors, Autophagy 7 (2011) 1145-1158.
96. J.L. Bada, New insights into prebiotic chemistry from Stanley Miller's spark discharge experiments, Chem. Soc. Rev. 42 (2013) 2186-2196.
97. S. Kopriva, S.G. Mugford, P. Baraniecka, B.R. Lee, C.A. Matthewman, A. Koprivova, Control of sulfur partitioning between primary and secondary metabolism in Arabidopsis, Front Plant Sci. 3 (2012) 163.