Signaling in the plant cytosol: Cysteine or sulfide?

Amino Acids

Volumn 47, Issue 10, 2015, Pages 2155-2164

  Gotor, Cecilia ^a   Laureano Marín, Ana M ^a   Moreno, Inmaculada ^a   Aroca, Ángeles ^a   García, Irene ^a   Romero, Luis C ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Abiotic stress; Arabidopsis; Autophagy; Biotic stress; Sulfur metabolism

Indexed keywords

ATG8 PROTEIN; CYSTEINE; CYSTEINE SYNTHASE; DES1 PROTEIN; REACTIVE OXYGEN METABOLITE; REACTIVE SULFUR SPECIES; SERINE ACETYLTRANSFERASE; SULFIDE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN;

ABIOTIC STRESS; AMINO ACID SYNTHESIS; ARABIDOPSIS THALIANA; BIOTIC STRESS; CHAPERONE-MEDIATED AUTOPHAGY; ENZYME ACTIVITY; GENETIC COMPLEMENTATION; MACROAUTOPHAGY; MICROAUTOPHAGY; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PLANT IMMUNITY; PLANT RESPONSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; PROTEIN PROTEIN INTERACTION; REVIEW; ARABIDOPSIS; CYTOSOL; HOMEOSTASIS; METABOLISM; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYSTEINE; CYTOSOL; HOMEOSTASIS; SIGNAL TRANSDUCTION; SULFIDES;

EID: 84942503494     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-014-1786-z     Document Type: Review

References (94)

1. Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152(2):656-669. doi: 10.1104/pp.109.147975
2. Alvarez C, Bermudez MA, Romero LC, Gotor C, Garcia I (2012a) Cysteine homeostasis plays an essential role in plant immunity. New Phytol 193(1):165-177. doi: 10.1111/j.1469-8137.2011.03889.x
3. Alvarez C, Garcia I, Moreno I, Perez-Perez ME, Crespo JL, Romero LC, Gotor C (2012b) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24(11):4621-4634. doi: 10.1105/tpc.112.105403
4. Alvarez C, Garcia I, Romero LC, Gotor C (2012c) Mitochondrial sulfide detoxification requires a functional isoform O-acetylserine(thiol)lyase C in Arabidopsis thaliana. Mol Plant 5(6):1217-1226. doi: 10.1093/mp/sss043
5. Bassham DC (2007) Plant autophagy - more than a starvation response. Curr Opin Plant Biol 10(6):587-593. doi: 10.1016/j.pbi.2007.06.006
6. Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2006) Autophagy in development and stress responses of plants. Autophagy 2(1):2-11 2092 [pii]
7. Bermudez MA, Paez-Ochoa MA, Gotor C, Romero LC (2010) Arabidopsis S-sulfocysteine synthase activity is essential for chloroplast function and long-day light-dependent redox control. Plant Cell 22(2):403-416. doi: 10.1105/tpc.109.071985
8. Bermudez MA, Galmes J, Moreno I, Mullineaux PM, Gotor C, Romero LC (2012) Photosynthetic adaptation to length of day is dependent on s-sulfocysteine synthase activity in the thylakoid lumen. Plant Physiol 160(1):274-288. doi: 10.1104/pp.112.201491
9. Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1-18. doi: 10.1146/annurev.cellbio.16.1.1
10. Bonner ER, Cahoon RE, Knapke SM, Jez JM (2005) Molecular basis of cysteine biosynthesis in plants: structural and functional analysis of O-acetylserine sulfhydrylase from Arabidopsis thaliana. J Biol Chem 280(46):38803-38813
11. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187-220
12. Buchner P, Stuiver CE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H(2)S and pedospheric sulfate nutrition. Plant Physiol 136(2):3396-3408
13. Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62(13):4481-4493. doi: 10.1093/jxb/err145
14. Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278-286. doi: 10.1016/j.plaphy.2013.05.042
15. Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) 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(7):1953-1966. doi: 10.1093/jxb/ert055
16. Chung T, Suttangkakul A, Vierstra RD (2009) The ATG autophagic conjugation system in maize: aTG transcripts and abundance of the ATG8-lipid adduct are regulated by development and nutrient availability. Plant Physiol 149(1):220-234. doi: 10.1104/pp.108.126714
17. Contento AL, Kim SJ, Bassham DC (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol 135(4):2330-2347. doi: 10.1104/pp.104.044362
18. Dawood M, Cao F, Jahangir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209-210:121-128. doi: 10.1016/j.jhazmat.2011.12.076
19. Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3(3):REVIEWS3004
20. Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79(3):331-348
21. Droux M, Ruffet ML, Douce R, Job D (1998) 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(1):235-245
22. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155(1):2-18. doi: 10.1104/pp.110.167569
23. Francois JA, Kumaran S, Jez JM (2006) Structural basis for interaction of O-acetylserine sulfhydrylase and serine acetyltransferase in the Arabidopsis cysteine synthase complex. Plant Cell 18(12):3647-3655
24. Garcia I, Castellano JM, Vioque B, Solano R, Gotor C, Romero LC (2010) Mitochondrial {beta}-cyanoalanine synthase is essential for root hair formation in Arabidopsis thaliana. Plant Cell 22(10):3268-3279. doi: 10.1105/tpc.110.076828
25. Garcia I, Rosas T, Bejarano ER, Gotor C, Romero LC (2013) Transient transcriptional regulation of the CYS-C1 gene and cyanide accumulation upon pathogen infection in the plant immune response. Plant Physiol 162(4):2015-2027. doi: 10.1104/pp.113.219436
26. Garcia I, Gotor C, Romero LC (2014) Beyond toxicity: a regulatory role for mitochondrial cyanide. Plant Signal Behav 9:e27612
27. Garcia-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188(4):977-984. doi: 10.1111/j.1469-8137.2010.03465.x
28. Garcia-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201-202:66-73. doi: 10.1016/j.plantsci.2012.11.007
29. Gotor C, Romero LC (2013) S-sulfocysteine synthase function in sensing chloroplast redox status. Plant Signal Behav 8:e23313
30. Gotor C, Alvarez C, Bermudez MA, Moreno I, Garcia I, Romero LC (2010) Low abundance does not mean less importance in cysteine metabolism. Plant Signal Behav 5:1028-1030
31. Gotor C, Garcia I, Crespo JL, Romero LC (2013) Sulfide as a signaling molecule in autophagy. Autophagy 9(4):609-611. doi: 10.4161/auto.23460
32. Gutierrez-Marcos JF, Roberts MA, Campbell EI, Wray JL (1996) Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and "APS reductase" activity. Proc Natl Acad Sci USA 93(23):13377-13382
33. Haag AF, Kerscher B, Dall'Angelo S, Sani M, Longhi R, Baloban M, Wilson HM, Mergaert P, Zanda M, Ferguson GP (2012) Role of cysteine residues and disulfide bonds in the activity of a legume root nodule-specific, cysteine-rich peptide. J Biol Chem 287(14):10791-10798. doi: 10.1074/jbc.M111.311316
34. Haas FH, Heeg C, Queiroz R, Bauer A, Wirtz M, Hell R (2008) Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol 148(2):1055-1067
35. Hatzfeld Y, Lee S, Lee M, Leustek T, Saito K (2000a) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248(1-2):51-58
36. Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000b) Beta-cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123(3):1163-1171
37. Heeg C, Kruse C, Jost R, Gutensohn M, Ruppert T, Wirtz M, Hell R (2008) Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20(1):168-185
38. Howarth JR, Dominguez-Solis JR, Gutierrez-Alcala G, Wray JL, Romero LC, Gotor C (2003) The serine acetyltransferase gene family in Arabidopsis thaliana and the regulation of its expression by cadmium. Plant Mol Biol 51(4):589-598
39. Hu LY, Hu SL, Wu J, Li YH, Zheng JL, Wei ZJ, Liu J, Wang HL, Liu YS, Zhang H (2012) Hydrogen sulfide prolongs postharvest shelf life of strawberry and plays an antioxidative role in fruits. J Agric Food Chem 60(35):8684-8693. doi: 10.1021/jf300728h
40. Jacob C, Giles GI, Giles NM, Sies H (2003) Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Edn Engl 42(39):4742-4758
41. Jez JM, Dey S (2013) The cysteine regulatory complex from plants and microbes: what was old is new again. Curr Opin Struct Biol 23(2):302-310. doi: 10.1016/j.sbi.2013.02.011
42. Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414(3):481-486. doi: 10.1016/j.bbrc.2011.09.090
43. Kawashima CG, Berkowitz O, Hell R, Noji M, Saito K (2005) Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol 137(1):220-230
44. Khan MS, Haas FH, Samami AA, Gholami AM, Bauer A, Fellenberg K, Reichelt M, Hansch R, Mendel RR, Meyer AJ, Wirtz M, Hell R (2010) Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana. Plant Cell 22(4):1216-1231. doi: 10.1105/tpc.110.074088
45. Kopriva S, Koprivova A (2004) Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55(404):1775-1783. doi: 10.1093/jxb/erh185
46. Krueger S, Niehl A, Lopez Martin MC, Steinhauser D, Donath A, Hildebrandt T, Romero LC, Hoefgen R, Gotor C, Hesse H (2009) 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(4):349-367. doi: 10.1111/j.1365-3040.2008.01928.x
47. Laxman S, Sutter BM, Tu BP (2014) Methionine is a signal of amino acid sufficiency that inhibits autophagy through the methylation of PP2A. Autophagy 10(2):386-387. doi: 10.4161/auto.27485
48. Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17(9):526-537. doi: 10.1016/j.tplants.2012.05.006
49. Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25(3):617-631. doi: 10.1007/s10534-012-9551-9
50. Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36(8):1564-1572. doi: 10.1111/pce.12092
51. Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48(12):931-935. doi: 10.1016/j.plaphy.2010.09.016
52. Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36(9):1607-1616. doi: 10.1111/pce.12073
53. Lopez-Martin MC, Becana M, Romero LC, Gotor C (2008a) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol 147(2):562-572
54. Lopez-Martin MC, Romero LC, Gotor C (2008b) Cytosolic cysteine in redox signaling. Plant Signal Behav 3(10):880-881
55. Mendoza-Cozatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14(5):554-562. doi: 10.1016/j.pbi.2011.07.004
56. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35(2):454-484. doi: 10.1111/j.1365-3040.2011.02400.x
57. Park S, Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the fenton reaction. J Bacteriol 185(6):1942-1950
58. Perez-Perez ME, Florencio FJ, Crespo JL (2010) Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiol 152(4):1874-1888. doi: 10.1104/pp.109.152520
59. Perez-Perez ME, Lemaire SD, Crespo JL (2012) Reactive oxygen species and autophagy in plants and algae. Plant Physiol 160(1):156-164. doi: 10.1104/pp.112.199992
60. Phillips AR, Suttangkakul A, Vierstra RD (2008) The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 178(3):1339-1353. doi: 10.1534/genetics.107.086199
61. Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10(10):503-509
62. Rea PA (2012) Phytochelatin synthase: of a protease a peptide polymerase made. Physiol Plant 145(1):154-164. doi: 10.1111/j.1399-3054.2012.01571.x
63. Richau KH, Kaschani F, Verdoes M, Pansuriya TC, Niessen S, Stuber K, Colby T, Overkleeft HS, Bogyo M, Van der Hoorn RA (2012) Subclassification and biochemical analysis of plant papain-like cysteine proteases displays subfamily-specific characteristics. Plant Physiol 158(4):1583-1599. doi: 10.1104/pp.112.194001
64. Romero LC, Garcia I, Gotor C (2013) l-Cysteine desulfhydrase 1 modulates the generation of the signaling molecule sulfide in plant cytosol. Plant Signal Behav 8:e24007
65. Romero LC, Aroca MA, Laureano-Marin AM, Moreno I, Garcia I, Gotor C (2014) Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant 7(2):264-276. doi: 10.1093/mp/sst168
66. Rose TL, Bonneau L, Der C, Marty-Mazars D, Marty F (2006) Starvation-induced expression of autophagy-related genes in Arabidopsis. Biol Cell 98(1):53-67. doi: 10.1042/BC20040516
67. Setya A, Murillo M, Leustek T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 93(23):13383-13388
68. Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67-74. doi: 10.1016/j.plaphy.2013.01.003
69. Sutter BM, Wu X, Laxman S, Tu BP (2013) Methionine inhibits autophagy and promotes growth by inducing the SAM-responsive methylation of PP2A. Cell 154(2):403-415. doi: 10.1016/j.cell.2013.06.041
70. Takahashi H (2010) Regulation of sulfate transport and assimilation in plants, Chapter 4. In: Kwang WJ (ed) International review of cell and molecular biology, vol 281. Academic Press, New York, pp 129-159. doi: 10.1016/S1937-6448(10)81004-4
71. Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157-184. doi: 10.1146/annurev-arplant-042110-103921
72. Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8(2):165-173. doi: 10.1016/j.pbi.2005.01.013
73. Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138(4):2097-2110. doi: 10.1104/pp.105.060673
74. Van Hoewyk D, Pilon M, Pilon-Smits EAH (2008) The functions of NifS-like proteins in plant sulfur and selenium metabolism. Plant Sci 174(2):117-123. doi: 10.1016/j.plantsci.2007.10.004
75. Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbuhl U, den Camp RO, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31(6):729-740
76. Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92(2):791-896. doi: 10.1152/physrev.00017.2011
77. Wang BL, Shi L, Li YX, Zhang WH (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231(6):1301-1309. doi: 10.1007/s00425-010-1134-9
78. Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351(1-2):107-119
79. Watanabe M, Kusano M, Oikawa A, Fukushima A, Noji M, Saito K (2008a) Physiological roles of the beta-substituted alanine synthase gene family in Arabidopsis. Plant Physiol 146(1):310-320
80. Watanabe M, Mochida K, Kato T, Tabata S, Yoshimoto N, Noji M, Saito K (2008b) Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis. Plant Cell 20(9):2484-2496
81. Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86(3):345-362
82. Wirtz M, Hell R (2006) Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J Plant Physiol 163(3):273-286
83. Wirtz M, Hell R (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19(2):625-639
84. Wirtz M, Droux M, Hell R (2004) O-acetylserine(thiol)lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 55(404):1785-1798. doi: 10.1093/jxb/erh201
85. Xiong Y, Contento AL, Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 42(4):535-546. doi: 10.1111/j.1365-313X.2005.02397.x
86. Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143(1):291-299. doi: 10.1104/pp.106.092106
87. Yamaguchi Y, Nakamura T, Kusano T, Sano H (2000) Three Arabidopsis genes encoding proteins with differential activities for cysteine synthase and beta-cyanoalanine synthase. Plant Cell Physiol 41(4):465-476
88. Yi H, Galant A, Ravilious GE, Preuss ML, Jez JM (2010) Sensing sulfur conditions: simple to complex protein regulatory mechanisms in plant thiol metabolism. Mol Plant 3(2):269-279. doi: 10.1093/mp/ssp112
89. Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53(8):1355-1365. doi: 10.1093/pcp/pcs099
90. Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16(11):2967-2983. doi: 10.1105/tpc.104.025395
91. Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145(2):378-388. doi: 10.1104/pp.107.105742
92. Yoshimoto K, Takano Y, Sakai Y (2010) Autophagy in plants and phytopathogens. FEBS Lett 584(7):1350-1358. doi: 10.1016/j.febslet.2010.01.007
93. Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50(12):1518-1529. doi: 10.1111/j.1744-7909.2008.00769.x
94. Zhang H, Hu S-L, Zhang Z-J, Hu L-Y, Jiang C-X, Wei Z-J, Liu J, Wang H-L, Jiang S-T (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60:251-257