Comparative analysis of ascorbate peroxidases (APXs) from selected plants with a special focus on Oryza sativa employing public databases

1. Fernandez-Garcia N, de la Garma JG, Olmos E. ROS as Biomarkers in Hyperhydricity. In: Gupta SD, editors. Reactive Oxygen Species Antioxidants in Higher Plants. CRC Press; 2010. pp. 249–274.

2. Bienert GP, Møller AL, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, et al. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem. 2007;282(2):1183–1192. doi: 10.1074/jbc.M603761200 17105724

3. Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U. Plant plasma membrane water channels conduct the signalling molecule H2O2. Biochem J. 2008;414(1):53–61. doi: 10.1042/BJ20080287 18462192

4. Foyer CH, Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plantarum. 2003;119(3):355–364.

5. Reth M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immunol. 2002;3(12):1129–1134. doi: 10.1038/ni1202-1129 12447370

6. Ozyigit II, Filiz E, Vatansever R, Kurtoglu KY, Koc I, Öztürk MX, et al. Identification and comparative analysis of H2O2-scavenging enzymes (ascorbate peroxidase and glutathione peroxidase) in selected plants employing bioinformatics approaches. Front Plant Sci. 2016;7:301. doi: 10.3389/fpls.2016.00301 27047498

7. Bailey-Serres J, Mittler R. The Roles of Reactive Oxygen Species in Plant Cells. Plant Physiol. 2006;141(2):311. doi: 10.1104/pp.104.900191 16760480

8. Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosché M, et al. Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Expl Bot. 2016;67(13):3831–3844.

9. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9(10):490–498. doi: 10.1016/j.tplants.2004.08.009 15465684

10. Miller G, Suzuki N, Ciftci‐Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010;33(4):453–467. doi: 10.1111/j.1365-3040.2009.02041.x 19712065

11. Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, et al. Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci. 2017;8:581. doi: 10.3389/fpls.2017.00581 28473838

12. Souza PVL, Lima-Melo Y, Carvalho FE, Reichheld J-P, Fernie AR, Silveira JAG, et al. Function and compensatory mechanisms among the components of the chloroplastic redox network. Crit Rev Plant Sci. 2019;38(1):1–28.

13. Qin Y-M, Hu C-Y, Zhu Y-X. The ascorbate peroxidase regulated by H2O2 and ethylene is involved in cotton fiber cell elongation by modulating ROS homeostasis. Plant Signal Behav. 2008;3(3):194–196. doi: 10.4161/psb.3.3.5208 19704716

14. Filiz E, Ozyigit II, Saracoglu IA, Uras ME, Sen U, Yalcin B. Abiotic stress-induced regulation of antioxidant genes in different Arabidopsis ecotypes: microarray data evaluation. Biotechnol Biotec Eq. 2019;33(1):128–143.

15. Hiner ANP, Ruiz JH, López JNRg, Cánovas FGa, Brisset NC, Smith AT, et al. Reactions of the class II peroxidases, lignin peroxidase andarthromyces ramosus peroxidase, with hydrogen peroxide: CATALASE-LIKE ACTIVITY, COMPOUND III FORMATION, AND ENZYME INACTIVATION. J Biol Chem. 2002;277(30):26879–26885. doi: 10.1074/jbc.M200002200 11983689

16. Sofo A, Scopa A, Nuzzaci M, Vitti A. Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci. 2015;16(6):13561–13578. doi: 10.3390/ijms160613561 26075872

17. Bonifacio A, Martins MO, Ribeiro CW, Fontenele AV, Carvalho FEL, Margis-Pinheiro M, et al. Role of peroxidases in the compensation of cytosolic ascorbate peroxidase knockdown in rice plants under abiotic stress. Plant Cell Environ. 2011;34(10):1705–1722. doi: 10.1111/j.1365-3040.2011.02366.x 21631533

18. Wu B, Li L, Qiu T, Zhang X, Cui S. Cytosolic APX2 is a pleiotropic protein involved in H2O2 homeostasis, chloroplast protection, plant architecture and fertility maintenance. Plant Cell Rep. 2018;37(6):833–848. doi: 10.1007/s00299-018-2272-y 29549445

19. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, et al. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell. 2005;17(1):268–281. doi: 10.1105/tpc.104.026971 15608336

20. Maruta T, Sawa Y, Shigeoka S, Ishikawa T. Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme? Plant Cell Physiol. 2016;57(7):1377–1386. doi: 10.1093/pcp/pcv203 26738546

21. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, et al. Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot. 2002;53(372):1305–1319. 11997377

22. Wang Y, Wisniewski M, Meilan R, Cui M, Webb R, Fuchigami L. Overexpression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress. J Am Soc for Hortic Sci. 2005;130(2):167–173.

23. Wang J, Zhang H, Allen RD. Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol. 1999;40(7):725–732. doi: 10.1093/oxfordjournals.pcp.a029599 10501032

24. Lu Z, Liu D, Liu S. Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep. 2007;26(10):1909–1917. doi: 10.1007/s00299-007-0395-7 17571267

25. Guan Q, Takano T, Liu S. Genetic transformation and analysis of rice OsAPx2 gene in Medicago sativa. PLoS ONE. 2012;7(7):e41233. doi: 10.1371/journal.pone.0041233 22848448

26. Zhang Q, Cui M, Xin X, Ming X, Jing L, WU J-x. Overexpression of a cytosolic ascorbate peroxidase gene, OsAPX2, increases salt tolerance in transgenic alfalfa. J Integr Agr. 2014;13(11):2500–2507.

27. Rosa SB, Caverzan A, Teixeira FK, Lazzarotto F, Silveira JAG, Ferreira-Silva SL, et al. Cytosolic APx knockdown indicates an ambiguous redox responses in rice. Phytochemistry. 2010;71(5):548–558.

28. Lozano-Juste J, Colom-Moreno R, León J. In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot. 2011;62(10):3501–3517. doi: 10.1093/jxb/err042 21378116

29. Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, et al. Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J. 2012;72(4):585–599. doi: 10.1111/j.1365-313X.2012.05100.x 22780834

30. Clark D, Durner J, Navarre DA, Klessig DF. Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe In. 2000;13(12):1380–1384.

31. Keyster M, Klein A, Egbich I, Jacobs A, Ludidi N. Nitric oxide increases the enzymatic activity of three ascorbate peroxidase isoforms in soybean root nodules. Plant Signal Behav. 2011;6(7):956–961. doi: 10.4161/psb.6.7.14879 21494099

32. Lin C-C, Jih P-J, Lin H-H, Lin J-S, Chang L-L, Shen Y-H, et al. Nitric oxide activates superoxide dismutase and ascorbate peroxidase to repress the cell death induced by wounding. Plant Mol Biol. 2011;77(3):235–249. doi: 10.1007/s11103-011-9805-x 21833542

33. Fares A, Rossignol M, Peltier J-B. Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Bioph Res Co. 2011;416(3):331–336.

34. Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, et al. Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot. 2013;65(2):527–538. doi: 10.1093/jxb/ert396 24288182

35. El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2018;47(D1):D427–D432.

36. Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the ExPASy server. In: Walker JM, editors. The proteomics protocols handbook. Humana press; 2005. pp. 571–607.

37. Yu CS, Chen YC, Lu CH, Hwang JK. Prediction of protein subcellular localization. Proteins: Structure, Function, Bioinformatics. 2006;64(3):643–651.

38. Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier C, et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007;35(suppl_2):W585–W587.

39. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37(suppl_2):W202–W208.

40. Chen C, Xia R, Chen H, He Y. TBtools, a Toolkit for Biologists integrating various biological data handling tools with a user-friendly interface. BioRxiv. 2018:289660.

41. Blom N, Sicheritz‐Pontén T, Gupta R, Gammeltoft S, Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics. 2004;4(6):1633–1649. doi: 10.1002/pmic.200300771 15174133

42. Xue Y, Liu Z, Gao X, Jin C, Wen L, Yao X, et al. GPS-SNO: computational prediction of protein S-nitrosylation sites with a modified GPS algorithm. PloS ONE. 2010;5(6):e11290. doi: 10.1371/journal.pone.0011290 20585580

43. Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X. CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng Des Sel. 2008;21(11):639–644. doi: 10.1093/protein/gzn039 18753194

44. Xie Y, Zheng Y, Li H, Luo X, He Z, Cao S, et al. GPS-Lipid: a robust tool for the prediction of multiple lipid modification sites. Sci Rep-UK. 2016;6:28249.

45. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46(W1):W296–W303. doi: 10.1093/nar/gky427 29788355

46. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22(22):4673–4680. doi: 10.1093/nar/22.22.4673 7984417

47. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, evolution. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–2729. doi: 10.1093/molbev/mst197 24132122

48. Higo K, Ugawa Y, Iwamoto M, Korenaga T. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 1999;27(1):297–300. doi: 10.1093/nar/27.1.297 9847208

49. Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2018;47(D1):D607–D613.

50. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–2504. doi: 10.1101/gr.1239303 14597658

51. Xia L, Zou D, Sang J, Xu X, Yin H, Li M, et al. Rice Expression Database (RED): An integrated RNA-Seq-derived gene expression database for rice. J Genet Genomics. 2017;44(5):235–241. doi: 10.1016/j.jgg.2017.05.003 28529082

52. Pan R, Reumann S, Lisik P, Tietz S, Olsen LJ, Hu J. Proteome analysis of peroxisomes from dark-treated senescent Arabidopsis leaves. J Integr Plant Biol. 2018;60(11):1028–1050. doi: 10.1111/jipb.12670 29877633

53. Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, et al. The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot. 2006;57(12):3033–3042. doi: 10.1093/jxb/erl060 16873450

54. Teixeira FK, Menezes-Benavente L, Galvão VC, Margis R, Margis-Pinheiro M. Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta. 2006;224(2):300–214. doi: 10.1007/s00425-005-0214-8 16397796

55. Wu T-M, Lin K-C, Liau W-S, Chao Y-Y, Yang L-H, Chen S-Y, et al. A set of GFP-based organelle marker lines combined with DsRed-based gateway vectors for subcellular localization study in rice (Oryza sativa L.). Plant Mol Biol. 2016;90(1):107–115.

56. Xu L, Carrie C, Law SR, Murcha MW, Whelan J. Acquisition, conservation, and loss of dual-targeted proteins in land plants. Plant Physiol. 2013;161(2):644–662. doi: 10.1104/pp.112.210997 23257241

57. Pitsch NT, Witsch B, Baier M. Comparison of the chloroplast peroxidase system in the chlorophyte Chlamydomonas reinhardtii, the bryophyte Physcomitrella patens, the lycophyte Selaginella moellendorffii and the seed plant Arabidopsis thaliana. BMC Plant Biol. 2010;10(1):133.

58. Kersten B, Agrawal GK, Durek P, Neigenfind J, Schulze W, Walther D, et al. Plant phosphoproteomics: an update. Proteomics. 2009;9(4):964–988. doi: 10.1002/pmic.200800548 19212952

59. Wang K, Zhao Y, Li M, Gao F, Yang Mk, Wang X, et al. Analysis of phosphoproteome in rice pistil. Proteomics. 2014;14(20):2319–2334. doi: 10.1002/pmic.201400004 25074045

60. de Pinto MC, Locato V, Sgobba A, del Carmen Romero-Puertas M, Gadaleta C, Delledonne M, et al. S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol. 2013;163(4):1766–1775. doi: 10.1104/pp.113.222703 24158396

61. Correa-Aragunde N, Foresi N, Delledonne M, Lamattina L. Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J Exp Bot. 2013;64(11):3339–3349. doi: 10.1093/jxb/ert172 23918967

62. Zhang MM, Hang HC. Protein S-palmitoylation in cellular differentiation. Biochem Soc T. 2017;45(1):275–285.

63. Hemsley PA, Weimar T, Lilley KS, Dupree P, Grierson CS. A proteomic approach identifies many novel palmitoylated proteins in Arabidopsis. New Phytol. 2013;197(3):805–814. doi: 10.1111/nph.12077 23252521

64. Srivastava V, Weber JR, Malm E, Fouke BW, Bulone V. Proteomic analysis of a poplar cell suspension culture suggests a major role of protein S-acylation in diverse cellular processes. Front Plant Sci. 2016;7:477. doi: 10.3389/fpls.2016.00477 27148305

65. Traverso JA, Meinnel T, Giglione C. Expanded impact of protein N-myristoylation in plants. Plant Signal Behav. 2008;3(7):501–502. doi: 10.4161/psb.3.7.6039 19704499

66. Charron G, Li MMH, MacDonald MR, Hang HC. Prenylome profiling reveals S-farnesylation is crucial for membrane targeting and antiviral activity of ZAP long-isoform. P Natl Acad Sci USA. 2013;110(27):11085–11090.

67. Qin F, Shinozaki K, Yamaguchi-Shinozaki K. Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol. 2011;52(9):1569–1582. doi: 10.1093/pcp/pcr106 21828105

68. Agrawal GK, Jwa N-S, Iwahashi H, Rakwal R. Importance of ascorbate peroxidases OsAPX1 and OsAPX2 in the rice pathogen response pathways and growth and reproduction revealed by their transcriptional profiling. Gene. 2003;322:93–103. doi: 10.1016/j.gene.2003.08.017 14644501

69. Swinnen G, Goossens A, Pauwels L. Lessons from domestication: targeting cis-regulatory elements for crop improvement. Trends Plant Sci. 2016;21(6):506–515. doi: 10.1016/j.tplants.2016.01.014 26876195

70. Wang S, Li S, Liu Q, Wu K, Zhang J, Wang S, et al. The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet. 2015;47(8):949–954. doi: 10.1038/ng.3352 26147620

71. Cheng M-C, Liao P-M, Kuo W-W, Lin T-P. The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant physiol. 2013;162(3):1566–1582. doi: 10.1104/pp.113.221911 23719892

72. Kato Y, Urano Ji, Maki Y, Ushimaru T. Purification and characterization of dehydroascorbate reductase from rice. Plant Cell Physiol. 1997;38(2):173–178.

73. Huang T-L, Nguyen QTT, Fu S-F, Lin C-Y, Chen Y-C, Huang H-J. Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots. Plant Mol Biol. 2012;80(6):587–608. doi: 10.1007/s11103-012-9969-z 22987115

74. Noctor G, Arisi A-CM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH. Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot. 1998;49(321):623–647.

75. Bartoli CG, Buet A, Grozeff GG, Galatro A, Simontacchi M. Ascorbate-glutathione cycle and abiotic stress tolerance in plants. In: Hossain M, Munné-Bosch S, Burritt D, Diaz-Vivancos P, Fujita M, Lorence A, editors. Ascorbic Acid in Plant Growth, Development and Stress Tolerance. Springer; 2017. pp. 177–200.

76. El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK. Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma. 2010;245(1):85–96.

77. UniProt C. UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res. 2018;47(D1):D506–D515.

78. Alhagdow M, Mounet F, Gilbert L, Nunes-Nesi A, Garcia V, Just D, et al. Silencing of the mitochondrial ascorbate synthesizing enzyme L-galactono-1, 4-lactone dehydrogenase affects plant and fruit development in tomato. Plant Physiol. 2007;145(4):1408–1422. doi: 10.1104/pp.107.106500 17921340

79. Liu Y, Yu L, Wang R. Level of ascorbic acid in transgenic rice for l-galactono-1,4-lactone dehydrogenase overexpressing or suppressed is associated with plant growth and seed set. ACTA Physiol Plant. 2011;33(4):1353–1363.

80. Zhang Z, Xu Y, Xie Z, Li X, He Z-H, Peng X-X. Association–dissociation of glycolate oxidase with catalase in rice: a potential switch to modulate intracellular H2O2 levels. Mol Plant. 2016;9(5):737–748. doi: 10.1016/j.molp.2016.02.002 26900141

81. Passaia G, Caverzan A, Fonini LS, Carvalho FEL, Silveira JAG, Margis-Pinheiro M. Chloroplastic and mitochondrial GPX genes play a critical role in rice development. Biol Plantarum. 2014;58(2):375–378.

82. Pandey V, Shukla A. Acclimation and tolerance strategies of rice under drought stress. Rice Sci. 2015;22(4):147–161.

83. Maruyama K, Urano K, Yoshiwara K, Morishita Y, Sakurai N, Suzuki H, et al. Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts. Plant Physiol. 2014;164(4):1759–1771. doi: 10.1104/pp.113.231720 24515831

84. Pan W, Wu Y, Xie Q. Regulation of ubiquitination is central to the phosphate starvation response. Trends Plant Sci. 2019. doi: 10.1016/j.tplants.2019.05.002 31176527

85. Mehra P, Pandey BK, Giri J. Comparative morphophysiological analyses and molecular profiling reveal Pi-efficient strategies of a traditional rice genotype. Front Plant Sci. 2016;6:1184. doi: 10.3389/fpls.2015.01184 26779218

86. Oono Y, Kawahara Y, Yazawa T, Kanamori H, Kuramata M, Yamagata H, et al. Diversity in the complexity of phosphate starvation transcriptomes among rice cultivars based on RNA-Seq profiles. Plant Mol Biol. 2013;83(6):523–537. doi: 10.1007/s11103-013-0106-4 23857470

87. Zhao F-J, Huang X-Y. Cadmium phytoremediation: call rice CAL1. Mol Plant. 2018;11(5):640–642. doi: 10.1016/j.molp.2018.03.016 29614318

88. Wilkins KE, Booher NJ, Wang L, Bogdanove AJ. TAL effectors and activation of predicted host targets distinguish Asian from African strains of the rice pathogen Xanthomonas oryzae pv. oryzicola while strict conservation suggests universal importance of five TAL effectors. Front Plant Sci. 2015;6:536. doi: 10.3389/fpls.2015.00536 26257749