Potato annexin STANN1 promotes drought tolerance and mitigates light stress in transgenic Solanum tuberosum L. plants

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Szalonek, Michal ^a   Sierpien, Barbara ^a   Rymaszewski, Wojciech ^a   Gieczewska, Katarzyna ^b   Garstka, Maciej ^b   Lichocka, Malgorzata ^a   Sass, Laszlo ^c   Paul, Kenny ^c   Vass, Imre ^c   Vankova, Radomira ^d   Dobrev, Peter ^d   Szczesny, Pawel ^a   Marczewski, Waldemar ^e   Krusiewicz, Dominika ^e   Strzelczyk Zyta, Danuta ^e   Hennig, Jacek ^a   Konopka Postupolska, Dorota ^a  

^a POLISH ACADEMY OF SCIENCES   (Poland)

^b UNIVERSITY OF WARSAW   (Poland)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^e PLANT BREEDING AND ACCLIMATIZATION INSTITUTE NATIONAL RESEARCH INSTITUTE   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL B; LIPOCORTIN 1; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; XANTHOPHYLL; ZEAXANTHIN; ANNEXIN; CHLOROPHYLL; PHOTOSYSTEM II; PLANT PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; BIOACCUMULATION; CHLOROPLAST; CONTROLLED STUDY; DROUGHT STRESS; DROUGHT TOLERANCE; ELECTRON TRANSPORT; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HARVEST; LIGHT STRESS; LIPID PEROXIDATION; NONHUMAN; PHOTOCHEMICAL EFFICIENCY; PHOTOOXIDATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; PLANT ROOT; PLANT WATER CONTENT; POTATO; PROTEIN EXPRESSION; QUANTUM YIELD; STANN1 GENE; TRANSGENIC PLANT; WILD TYPE; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PLANT GENE;

ANNEXINS; CHLOROPHYLL; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LIGHT; OXIDATIVE STRESS; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RECOMBINANT PROTEINS; SOLANUM TUBEROSUM; STRESS, PHYSIOLOGICAL; XANTHOPHYLLS;

EID: 84940784655     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132683     Document Type: Article

References (173)

1. Bhargava S, Sawant K. Drought stress adaptation: metabolic adjustment and regulation of gene expression. Plant Breed. 2013; 132:21-32.
2. Mittler R, Blumwald E. Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol. 2010; 61:443-462. doi: 10.1146/annurev-arplant-042809-112116 PMID: 20192746
3. Reynolds M, Tuberosa R. Translational research impacting on crop productivity in drought-prone environments. Curr Opin Plant Biol. 2008; 11: 171-179. doi: 10.1016/j.pbi.2008.02.005 PMID: 18329330
4. Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004; 134: 1683-1696. PMID: 15047901
5. Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006; 11: 15-19. PMID: 16359910
6. Asselbergh B De Vieesschauwer D Hofte M Global switches and fine-tuning - ABA modulates plant pathogen defense. Mol Plant Microbe Int. 2008; 21: 709-719.
7. Tripathy BC, Oelmuller R. Reactive oxygen species generation and signaling in plants. Plant Signal Behav. 2012; 7: 1621-1633. doi: 10.4161/psb.22455 PMID: 23072988
8. Baxter A, Mittler R, Suzuki N. ROS as key players in plant stress signaling. J Exp Bot. 2014; 65: 1229-1240. doi: 10.1093/jxb/ert375 PMID: 24253197
9. Schmidt R, Schippers JHM (2015) ROS-mediated redox signaling during cell differentiation in plants. Biochim Biophys Acta http://dx.doi.org/10.1016/j.bbagen.2014.12.020
10. Foyer CH, Noctor G. Redox signaling in plants. Antioxid Redox Signal. 2013; 18: 2087-2090. doi: 10.1089/ars.2013.5278 PMID: 23442120
11. Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 2006; 141: 391-396. PMID: 16760493
12. Foyer CH, Shigeoka S. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 2011; 155: 93-100. doi: 10.1104/pp.110.166181 PMID: 21045124
13. Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. 2012; doi: 10.1155/2012/217037
14. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, et al. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 2003; 22: 2623-2633. PMID: 12773379
15. Voss I, Sunil B, Scheibe R, Raghavendra A.) Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biol (Stuttg). 2013; 15: 713-722.
16. Clark GB, Morgan RO, Fernandez MP, Roux SJ. Evolutionary adaptation of plant annexins has diversified their molecular structures, interactions and functional roles. New Phytol. 2012; 196: 695-712. doi: 10.1111/j.1469-8137.2012.04308.x PMID: 22994944
17. Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, Battey NH, et al. Annexins: multi-functional components of growth and adaptation. J Exp Bot. 2008; 59: 533-44. doi: 10.1093/jxb/erm344 PMID: 18267940
18. Laohavisit A, Brown AT, Cicuta P, Davies JM. Annexins: components of the calcium and reactive oxygen signaling network. Plant Physiol. 2010; 152: 1824-1829. doi: 10.1104/pp.109.145458 PMID: 20154100
19. Laohavisit A, Davies JM. Annexins. New Phytol. 2010; 189: 40-53. doi: 10.1111/j.1469-8137.2010.03533.x PMID: 21083562
20. Konopka-Postupolska D, Clark G, Hofmann A. Structure, function and membrane interactions of plant annexins: An update. Plant Sci. 2011; 181: 230-241. doi: 10.1016/j.plantsci.2011.05.013 PMID: 21763533
21. Gidrol X, Sabelli PA, Fern YS, Kush AK. Annexin-like protein from Arabidopsis thaliana rescues delta oxyR mutant of Escherichia coli from H2O2 stress. Proc Natl Acad Sci USA 1996; 93: 11268-11273. PMID: 8855345
22. Laohavisit A, Richards SL, Shabala L, Chen C, Colaco RD, Swarbreck SM, et al. Salinity-induced calcium signaling and root adaptation in Arabidopsis require the calcium regulatory protein annexin 1. Plant Physiol. 2013; 163: 253-262. doi: 10.1104/pp.113.217810 PMID: 23886625
23. Konopka-Postupolska D, Clark G, Goch G, Debski J, Floras K, Cantero A, et al. The role of annexin 1 in drought stress in Arabidopsis. Plant Physiol. 2009; 150: 1394-1410. doi: 10.1104/pp.109.135228 PMID: 19482919
24. Davies JM. Annexin-mediated calcium signalling in plants. Plants 2014; 3: 128-140.
25. Jami SK, Clark GB, Turlapati SA, Handley C, Roux SJ, Kirti PB. Ectopic expression of an annexin from Brassica juncea confers tolerance to abiotic and biotic stress treatments in transgenic tobacco. Plant Physiol Biochem. 2008; 46: 1019-1030. doi: 10.1016/j.plaphy.2008.07.006 PMID: 18768323
26. Divya K, Jami SK, Kirti PB. Constitutive expression of mustard annexin, BjAnn1 enhances abiotic stress tolerance and fiber quality in cotton under stress. Plant Mol Biol. 2010; 73: 293-308. doi: 10.1007/s11103-010-9615-6 PMID: 20148350
27. Chu P, Chen H, Zhou Y, Li Y, Ding Y, Jiang L, et al. Proteomic and functional analyses of Nelumbo nucifera annexins involved in seed thermotolerance and germination vigor. Planta 2012; 235: 1271-1288. doi: 10.1007/s00425-011-1573-y PMID: 22167260
28. Sareddy GR, Divya K, Kirti PB, Prakash Babu P. Novel antiproliferative and antioxidant role of BJANN1, a mustard annexin protein in human glioblastoma cell lines. J Cancer Sci Ther. 2013; 5: 256-263,
29. Dalal A, Vishwakarma A, Singh NK, Gudla T, Bhattacharyya MK, Padmasree K, et al. Attenuation of hydrogen peroxide-mediated oxidative stress by Brassica juncea annexin-3 counteracts thiol-specific antioxidant (TSA1) deficiency in Saccharomyces cerevisiae. FEBS Lett. 2014; 588: 584-593. doi: 10.1016/j.febslet.2014.01.006 PMID: 24444602
30. Dalal A, Kumar A, Yadav D, Gudla T, Viehhauser A, Dietz KJ, et al. Alleviation of methyl viologen-mediated oxidative stress by Brassica juncea annexin-3 in transgenic Arabidopsis. Plant Sci. 2014; 219-220: 9-18. doi: 10.1016/j.plantsci.2013.12.016 PMID: 24576759
31. Hoekstra AY, Hung PQ (2005) Globalisation of water resources: international virtual water flows in relation to crop trade. Global Environ Change 15: 45-56.
32. Salekdeh GH, Reynolds M, Bennett J, Boyer J. Conceptual framework for drought phenotyping during molecular breeding. Trends Plant Sci. 2009; 14: 488-496. doi: 10.1016/j.tplants.2009.07.007 PMID: 19716744
33. Jefferies R, Mackerron D. Responses of potato genotypes to drought. II. Leaf area index, growth and yield. Ann Appl Biol. 2008; 122: 105-122.
34. Hassanpanah D. Evaluation of potato cultivars for resistance against water deficit stress under in vivo conditions. Potato Res. 2010; 53: 383-392.
35. Monneveux P, Ramírez DA, Pino MT. Drought tolerance in potato (S. tuberosum L.): Can we learn from drought tolerance research in cereals? Plant Sci. 2013; 205-206: 76-86. doi: 10.1016/j.plantsci.2013.01.011 PMID: 23498865
36. Chaves I, Pinheiro C, Paiva JA, Planchon S, Sergeant K, Renaut J, et al. Proteomic evaluation of wound-healing processes in potato (Solanum tuberosum L.) tuber tissue. Proteomics 2009; 9: 4154-4175. doi: 10.1002/pmic.200700649 PMID: 19688748
37. Murphy JP, Kong F, Pinto DM, Wang-Pruski G. Relative quantitative proteomic analysis reveals wound response proteins correlated with after-cooking darkening. Proteomics 2010; 10: 4258-4269. doi: 10.1002/pmic.200900718 PMID: 21058337
38. Urbany C, Colby T, Stich B, Schmidt L, Schmidt J, Gebhardt C. Analysis of natural variation of the potato tuber proteome reveals novel candidate genes for tuber bruising. J Proteome Res. 2012; 11: 703-716. doi: 10.1021/pr2006186 PMID: 22047174
39. Folgado R, Panis B, Sergeant K, Renaut J, Swennen R, Hausman J-F. Differential protein expression in response to abiotic stress in two potato species: Solanum commersonii Dun and Solanum tuberosum L. Int J Mol Sci. 2013; 14: 4912-4933. doi: 10.3390/ijms14034912 PMID: 23455465
40. Aghaei K, Ehsanpour AA, Komatsu S. Proteome analysis of potato under salt stress. J Proteome Res. 2008; 7: 4858-4868. doi: 10.1021/pr800460y PMID: 18855355
41. Lim PO, Kim HJ, Nam HG. Leaf senescence. Ann Rev Plant Biol. 2007; 58: 115-136.
42. Lehesranta SJ, Davies HV, Shepherd LVT, Nunan N, McNicol JW, Auriola S, et al. Comparison of tuber proteomes of potato varieties, landraces, and genetically modified lines. Plant Physiol. 2005 138: 1690-1699. PMID: 15951487
43. Baulcombe DC, Saunders GR, Bevan MW, Mayo MA, Harrison BD. Expression of biologically active viral satellite RNA from the nuclear genome of transformed plants. Nature 1986; 321: 446-449.
44. Mac A, Krzymowska M, Barabasz A, Hennig J. Transcriptional regulation of the gluB promoter during plant response to infection. Cell Mol Biol Lett. 2004; 9: 843-853. PMID: 15647801
45. Nicot N, Hausman JF, Hoffmann L, Evers D. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot. 2005; 56: 2907-2914. PMID: 16188960
46. Vasquez-Robinet C, Mane SP, Ulanov A V, Watkinson JI, Stromberg VK, De Koeyer D, et al. Physiological and molecular adaptations to drought in Andean potato genotypes. J Exp Bot. 2008; 59: 2109-2123. doi: 10.1093/jxb/ern073 PMID: 18535297
47. Dobrev PI, Kaminek M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chrom A. 2002; 950: 21-29.
48. Dobrev PI, Vankova R. Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Meth Mol Biol. 2012; 913: 251-261.
49. Hipkins MF, Baker N. Photosynthesis energy transduction, a practical approach. In: Hipkins MF BN, ed. Spectroscopy. Oxford: Press; 1986. pp 51-101.
50. Seregelyes C, Barna B, Hennig J, Konopka D, Pasternak TP, Lukacs N, et al. Phytoglobins can interfere with nitric oxide functions during plant growth and pathogenic responses: a transgenic approach. Plant Sci. 2003; 165: 541-550.
51. Fotopoulos V, De Tullio MC, Barnes J, Kanellis AK. Altered stomatal dynamics in ascorbate oxidase overexpressing tobacco plants suggest a role for dehydroascorbate signalling. J Exp Bot. 2008; 59: 729-737. doi: 10.1093/jxb/erm359 PMID: 18349048
52. Hodges DM, Delong JM, Forney CF, Prange RK. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 1993; 207: 604-611.
53. Hoser R, Zurczak M, Lichocka M, Zuzga S, Dadlez M, Samuel MA, et al. Nucleocytoplasmic partitioning of tobacco N receptor is modulated by SGT1. New Phytol. 2013; 200: 158-171. doi: 10.1111/nph.12347 PMID: 23731343
54. Jami SK, Clark GB, Ayele BT, Roux SJ, Kirti P. Identification and characterization of annexin gene family in rice. Plant Cell Rep. 2012; 31: 813-825. doi: 10.1007/s00299-011-1201-0 PMID: 22167239
55. Lu Y, Ouyang B, Zhang J, Wang T, Lu C, Han Q, et al. Genomic organization, phylogenetic comparison and expression profiles of annexin gene family in tomato (Solanum lycopersicum). Gene 2012; 499: 14-24. doi: 10.1016/j.gene.2012.03.026 PMID: 22425974
56. Zingaretti SM, Inacio MC, Pereira LM, Paz TA, Franca SC. Water stress and agriculture. In: S. Akinci editors, Responses of organisms to water stress, InTech http://dx.doi.org/10.5772/53877
57. Carvalho MHC. Drought stress and reactive oxygen species: Production, scavenging and signaling. Plant Signal Behav. 2008; 3: 156-165. PMID: 19513210
58. 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: 453-467. doi: 10.1111/j.1365-3040.2009.02041.x PMID: 19712065
59. Pinheiro C, Chaves MM. Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot. 2011; 62: 869-882. doi: 10.1093/jxb/erq340 PMID: 21172816
60. Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, et al. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA. 2007; 104: 19631-19636. PMID: 18048328
61. Hortensteiner S. Chlorophyll degradation during senescence. Ann Rev Plant Biol. 2006; 57: 55-77.
62. Jahns P, Latowski D, Strzalka K. Mechanism and regulation of the violaxanthin cycle: The role of antenna proteins and membrane lipids. Biochim Biophys Acta. 2009; 1787: 3-14. doi: 10.1016/j.bbabio.2008.09.013 PMID: 18976630
63. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot. 2012; 63: 1637-1661. doi: 10.1093/jxb/ers013 PMID: 22371324
64. Bartoli CG, Casalongue CA, Simontacchi M, Marquez-Garcia B, Foyer CH. Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot. 2013; 94: 73-88.
65. Shao HB, Chu LY, Lu ZH, Kang CM. Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci. 2008; 4: 8-14.
66. Yuan S, Lin HH. Role of salicylic acid in plant abiotic stress. Z Naturforsch C. 2008; 63: 313-320. PMID: 18669013
67. Foyer CH, Lelandais M, Kunert KJ. Photooxidative stress in plants. Physiol Plant. 1994; 92: 696-717.
68. Lascano R, Munoz N, Robert GN, Rodriguez M, Melchiorre M, Trippi V, et al. Paraquat: an oxidative stress inducer. In: Hasaneen MN, editor. Herbicides - Properties, Synthesis and Control of Weeds. Rijeka, Croatia: InTech 2012. pp. 135-148.
69. Zhu J, Yuan S, Wei G, Qian D, Wu X, Jia H, et al. Annexin5 is essential for pollen development in Arabidopsis. Mol Plant. 2014; 7: 751-754. doi: 10.1093/mp/sst171 PMID: 24362755
70. Zhu J, Wu X, Yuan S, Qian D, Nan Q, An L, et al. Annexin5 plays a vital role in Arabidopsis pollen development via Ca2+-dependent membrane trafficking. PLoS One. 2014; 9, e102407. doi: 10.1371/journal.pone.0102407 PMID: 25019283
71. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol. 1999; 50: 601-639.
72. Chen S, Yin C, Qiang S, Zhou F, Dai X. Chloroplastic oxidative burst induced by tenuazonic acid, a natural photosynthesis inhibitor, triggers cell necrosis in Eupatorium adenophorum Spreng. Biochim Biophys Acta-Bioenergetics 2010; 1797: 391-405.
73. Kwak JM, Nguyen V, Schroeder JI. The role of reactive oxygen species in hormonal responses. Plant Physiol. 2006; 141: 323-329. PMID: 16760482
74. Ishibashi Y, Tawaratsumida T, Kondo K, Kasa S, Sakamoto M, Aoki N, et al. Reactive oxygen species are involved in gibberellin/abscisic acid signaling in barley aleurone cells. Plant Physiol. 2012; 158: 1705-1714. doi: 10.1104/pp.111.192740 PMID: 22291200
75. Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, et al. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J Exp Bot. 2009; 60: 3221-3238. doi: 10.1093/jxb/erp157 PMID: 19592501
76. Schraudner M, Moeder W, Wiese C, Camp WV, Inze D, Langebartels C, et al. Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. Plant J. 1998; 16: 235-245. doi: 10.1046/j.1365-313x.1998.00294.x PMID: 22507138
77. Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV. Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell. 2005; 17: 957-970. PMID: 15705948
78. Xie Y-J, Xu S, Han B, Wu M-Z, Yuan X-X, Han Y, et al. Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J. 2011; 66: 280-292. doi: 10.1111/j.1365-313X.2011.04488.x PMID: 21205037
79. Pfannschmidt T, Ogrzewalka K, Baginsky S, Sickmann A, Meyer HE, Link G. The multisubunit chloroplast RNA polymerase A from mustard (Sinapis alba L.). Integration of a prokaryotic core into a larger complex with organelle-specific functions. Eur J Biochem. 2000; 261: 253-261.
80. Steiner S, Schroter Y, Pfalz J, Pfannschmidt T. Identification of essential subunits in the plastid-encoded RNA polymerase complex reveals building blocks for proper plastid development. Plant Physiol. 2011; 157: 1043-1055. doi: 10.1104/pp.111.184515 PMID: 21949211
81. 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: 268-281. PMID: 15608336
82. Mano J, Ohno C, Domae Y, Asada K. Chloroplastic ascorbate peroxidase is the primary target of methylviologen-induced photooxidative stress in spinach leaves: its relevance to monodehydroascorbate radical detected with in vivo ESR. Biochim Biophys Acta. 2001; 1504: 275-287. PMID: 11245791
83. Kitajima S. Hydrogen peroxide-mediated inactivation of two chloroplastic peroxidases, ascorbate peroxidase and 2-cys peroxiredoxin. Photochem Photobiol. 2008; 84: 1404-1409. doi: 10.1111/j.1751-1097.2008.00452.x PMID: 19067962
84. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010; 48: 909-930. doi: 10.1016/j.plaphy.2010.08.016 PMID: 20870416
85. Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R. Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol. 2007; 144: 1777-1785. PMID: 17556505
86. Miller G, Shulaev V, Mittler R. Reactive oxygen signalling and abiotic stress. Physiol Plant. 2008; 133: 481-489. doi: 10.1111/j.1399-3054.2008.01090.x PMID: 18346071
87. Gao Q, Zhang L. Ultraviolet-B-induced oxidative stress and antioxidant defense system responses in ascorbate-deficient vtc1 mutants of Arabidopsis thaliana. J Plant Physiol. 2008; 165: 138-148. PMID: 17561306
88. Mhamdi A, Hager J, Chaouch S, Queval G, Han Y, Taconnat L, et al. Arabidopsis GLUTATHIONE REDUCTASE1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol. 2010; 153: 1144-1160. doi: 10.1104/pp.110.153767 PMID: 20488891
89. Perl A, Treves R, Galili S, Aviv D, Shalgi E, Malkin S, et al. Enhanced oxidative-stress defense in transgenic potato expressing tomato Cu, Zn superoxide dismutases. Theor Appl Genet. 1993; 85:568-576. doi: 10.1007/BF00220915 PMID: 24195931
90. Pal AK, Acharya K, Vats SK, Kumar S, Ahuja PS. Over-expression of PaSOD in transgenic potato enhances photosynthetic performance under drought. Biol Plant. 2013; 57: 359-364.
91. Tang L, Kwon SY, Kim SH, Kim JS, Choi JS, Cho KY, et al. Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep. 2006; 25: 1380-1386. PMID: 16841217
92. Broin M, Rey P. Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BAS1 2-cysteine peroxiredoxin and increased lipid peroxidation in thylakoids under photooxidative stress. Plant Physiol. 2003; 132: 1335-1343. PMID: 12857815
93. Schmitz G, Reinhold T, Gobel C, Feussner I, Neuhaus HE, Conrath U. Limitation of nocturnal ATP import into chloroplasts seems to affect hormonal crosstalk, prime defense, and enhance disease resistance in Arabidopsis thaliana. Mol Plant Microbe Interact. 2010; 23: 1584-1591. doi: 10.1094/MPMI-02-10-0045 PMID: 21039274
94. Baier M, Dietz KJ. Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot. 2005; 56: 1449-1462. PMID: 15863449
95. Suzuki N, Mittler R. Reactive oxygen species-dependent wound responses in animals and plants. Free Rad Biol Med. 2012; 53: 2269-2276. doi: 10.1016/j.freeradbiomed.2012.10.538 PMID: 23085520
96. Xia X-J, Zhou Y-K, Shi K, Zhou J, Foyer CH, Yu J-Q. Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot. in press; doi: 10.1093/jxb/erv089
97. Halim VA, Eschen-Lippold L, Altmann S, Birschwilks M, Scheel D, Rosahl S. Salicylic acid is important for basal defense of Solanum tuberosum against Phytophthora infestans. Mol Plant Microbe Interact. 2007; 20: 1346-1352. PMID: 17977146
98. Dempsey DA, Vlot CA, Mary C. Wildermuth MC, Klessig DF. Salicylic acid biosynthesis and metabolism. Arabidopsis Book 2011; 9: e0156. doi: 10.1199/tab.0156 PMID: 22303280
99. Navarre DA, Mayo D. Differential characteristics of salicylic acid-mediated signaling in potato. Physiol Mol Plant Path. 2004; 64: 179-188.
100. Aimar D, Calafat M, Andrade AM, Carassay L, Abdala GI, Molas ML. Drought tolerance and stress hormones: from model organisms to forage crops. Plants and Environment, Dr. Hemanth Vasanthaiah editors, InTech, 2011. Available from: http://www.intechopen.com/books/plants-and-environment/drought-tolerance-and-stress-hormones-frommodel-organisms-to-forage-cropsFrom Model Organisms to Forage Crops
101. Miura K, Tada Y. Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci. 2014; 5: 4. doi: 10.3389/fpls.2014.00004 PMID: 24478784
102. Munne-Bosch S, Penuelas J. Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta 2003; 217: 758-766. PMID: 12698367
103. Xue LJ, Guo W, Yuan Y, Anino EO, Nyamdari B, Wilson MC, et al. Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populus. Plant Cell 2013; 25: 2714-2730. doi: 10.1105/tpc.113.112839 PMID: 23903318
104. Janda T, Gondor OK, Yordanova R, Gabriella Szalai G, Pal M. Salicylic acid and photosynthesis: signalling and effects. Acta Physiol Plant. 2014; 36: 2537-2546.
105. Mateo A, Funck D, Muhlenbock P, Kular B, Mullineaux PM, Karpinski S. Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot. 2006; 57: 1795-1807. PMID: 16698814
106. Sanchez G, Gerhardt N, Siciliano F, Vojnov A, Malcuit I, Marano MR. Salicylic acid is involved in the Nb-mediated defense responses to Potato virus X in Solanum tuberosum. Mol Plant Microbe Interact. 2010; 23: 394-405. doi: 10.1094/MPMI-23-4-0394 PMID: 20192827
107. Baebler S, Stare K, Kovac M, Blejec A, Prezelj N, Stare T, et al. Dynamics of responses in compatible potato - potato virus y interaction are modulated by salicylic acid. PLoS One. 2011; 6(12): e29009. doi: 10.1371/journal.pone.0029009 PMID: 22194976
108. Chen Z, Ricigliano J, Klessig DF. Purification and characterization of a soluble salicylic acid-binding protein from tobacco. Proc Natl Acad Sci USA. 1993; 90: 9533-9537. PMID: 8415736
109. Durner J, Klessig DF. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci USA. 1995; 92: 11312-11316 PMID: 7479986
110. Durner J, Klessig DF. Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem. 1996; 271: 28492-28501. PMID: 8910477
111. Yang Y, Qi M, Mei C. Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J. 2004; 40: 909-919. PMID: 15584956
112. Argueso CT, Ferreira FJ, Kieber JJ. Environmental perception avenues: the interaction of cytokinin and environmental response pathways. Plant Cell Environ. 2009; 32: 1147-1160. doi: 10.1111/j.1365-3040.2009.01940.x PMID: 19183294
113. Jeon J, Kim NY, Kim S, Kang NY, Novak O, Ku SJ, et al. A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem. 2010; 285: 23371-23386. doi: 10.1074/jbc.M109.096644 PMID: 20463025
114. Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP. Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci. 2012; 17: 172-179. doi: 10.1016/j.tplants.2011.12.005 PMID: 22236698
115. O'Brien JA, Benkova E. Cytokinin cross-talking during biotic and abiotic stress responses. Frontiers Plant Sci. 2013; 4: 451.
116. Raspor M, Motyka V, Zizkova E, Dobrev PI, Travnickova A, Zdravkovic-Korac S, et al. Cytokinin profiles of AtCKX2-overexpressing potato plants and the impact of altered cytokinin homeostasis on tuberization in vitro. J Plant Growth Reg. 2012; 31: 460-470.
117. Chow B, McCourt P. Hormone signalling from a developmental context. J Exp Bot. 2004; 55: 247-251. PMID: 14673027
118. Rivero RM, Shulaev V, Blumwald E. Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol. 2009; 150: 1530-1040. doi: 10.1104/pp.109.139378 PMID: 19411371
119. Rivero RM, Gimeno J, Van Deynze A, Walia H, Blumwald E. Enhanced cytokinin synthesis in tobacco plants expressing pSARK:: IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol. 2010; 51: 1929-1941. doi: 10.1093/pcp/pcq143 PMID: 20871100
120. Havlova M, Dobrev PI, Motyka V, Storchova H, Libus J, Dobra J, et al. The role of cytokinins in responses to water deficit in tobacco plants over-expressing trans-zeatin O-glucosyltransferase gene under 35S or SAG12 promoters. Plant Cell Environ. 2008; 31:341-353. PMID: 18088334
121. Gajdosova S, Spichal L, Kaminek M, Hoyerova K, Novak O, Dobrev PI, et al. Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J Ex Bot. 2011; 62: 2827-2840.
122. Merewitz E, Gianfagna T, Huang B. Effects of SAG12-ipt and HSP18.2-ipt. expression on cytokinin production, root growth and leaf senescence in creeping bentgrass exposed to drought stress. J Am Soc Hort Sci. 2010; 135: 230-239.
123. Mackova H, Hronkova M, Dobra J, Tureckova V, Novak O, Lubovska Z, et al. Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot. 2013; 64: 2805-2815. doi: 10.1093/jxb/ert131 PMID: 23669573
124. Merewitz EB, Gianfagna T, Huang B. Protein accumulation in leaves and roots associated with improved drought tolerance in creeping bentgrass expressing an ipt gene for cytokinin synthesis. J Ex Bot. 2011; 62: 5311-5333.
125. Prochazkova D, Haisel D, Wilhelmova N. Antioxidant protection during ageing and senescence in chloroplasts of tobacco with modulated life span. Cell Biochem Funct. 2008; 26: 582-590. doi: 10.1002/cbf.1481 PMID: 18512255
126. Rashotte AM, Carson SDB, To JPC, Kieber JJ. Expression profiling of cytokinin action in Arabidopsis. Plant Physiol. 2003; 132: 1998-2011. PMID: 12913156
127. Bhargava A, Clabaugh I, To JP, Maxwell BB, Chiang YH, Schaller GE, et al. Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 2013; 162: 272-294. doi: 10.1104/pp.113.217026 PMID: 23524861
128. Cortleven A, Nitschke S, Klaumunzer M, Abdelgawad H, Asard H, Grimm B, et al. A novel protective function for cytokinin in the light stress response is mediated by the ARABIDOPSIS HISTIDINE KINASE2 and ARABIDOPSIS HISTIDINE KINASE3 receptors. Plant Physiol. 2014ł 164: 1470-1483. doi: 10.1104/pp.113.224667 PMID: 24424319
129. Finkelstein R. Abscisic acid synthesis and response. Arabidopsis Book 2013; 11: e0166. doi: 10.1199/tab.0166 PMID: 24273463
130. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schunemann D, Finazzi G, et al. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 2008; 132: 273-285. doi: 10.1016/j.cell.2007.12.028 PMID: 18243102
131. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, et al. Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 2003; 15: 939-951. PMID: 12671089
132. Havaux M, Bonfils JP, Lutz C, Niyogi KK. Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. Plant Physiol. 2000; 124: 273-284. PMID: 10982442
133. Veljovic-Jovanovic SD, Pignocchi C, Noctor G, Foyer CH. Low ascorbic acid in the vtc1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol. 2001; 127: 426-435. PMID: 11598218
134. Muller-Moule P, Conklin PL, Niyogi KK. Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol. 2002; 128: 970-977. PMID: 11891252
135. Chen Z, Gallie DR. Dehydroascorbate reductase affects non-photochemical quenching and photosynthetic performance. J Biol Chem. 2008; 283: 21347-21361. doi: 10.1074/jbc.M802601200 PMID: 18539599
136. Sobrino-Plata J, Meyssen D, Cuypers A, Escobar C, Hernandez LH; Glutathione is a key antioxidant metabolite to cope with mercury and cadmium stress. Plant Soil 2014; 377: 369-381.
137. Havaux M, Eymery F, Porfirova S, Rey P, Dormann P. Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 2005; 17: 3451-3469. PMID: 16258032
138. Li Z, Keasling JD, Niyogi KK. Overlapping photoprotective function of vitamin E and carotenoids in Chlamydomonas. Plant Physiol. 2011; 158: 313-323. doi: 10.1104/pp.111.181230 PMID: 22080601
139. Gorecka KM, Konopka-Postupolska D, Hennig J, Buchet R, Pikula S. Peroxidase activity of annexin 1 from Arabidopsis thaliana. Biochem Biophys Res Commun. 2005; 336: 868-875. PMID: 16153598
140. Mortimer JC, Coxon KM, Laohavisit A, Davies JM. Heme-independent soluble and membrane-associated peroxidase activity of a Zea mays annexin preparation. Plant Signal Behav. 2009; 4: 428-30. doi: 10.1105/tpc.108.059550 PMID: 19816107
141. Plieth C, Vollbehr S. Calcium promotes activity and confers heat stability on plant peroxidases. Plant Signal Behav 2012; 7: 650-660. doi: 10.4161/psb.20065 PMID: 22580695
142. Laohavisit A, Mortimer JC, Demidchik V, Coxon KM, Stancombe MA, Macpherson N, et al. Zea mays annexins modulate cytosolic free Ca2+ and generate a Ca2+-permeable conductance. Plant Cell 2009; 21: 479-493. doi: 10.1105/tpc.108.059550 PMID: 19234085
143. Richards SL, Laohavisit A, Mortimer JC, Shabala L, Swarbreck SM, Shabala S, et al. (2014) Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots. Plant J 77: 136-145. doi: 10.1111/tpj.12372 PMID: 24180429
144. Foyer CH, Noctor G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 2011; 155: 2-18. doi: 10.1104/pp.110.167569 PMID: 21205630
145. Queval G, Thominet D, Vanacker H, Miginiac-Maslow M, Gakiere B, Noctor G. H2O2-activated upregulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast. Mol Plant. 2009; 2: 344-356. doi: 10.1093/mp/ssp002 PMID: 19825619
146. Rahantaniaina MS, Tuzet A, Mhamdi A, Noctor G. Missing links in understanding redox signaling via thiol/disulfide modulation: how is glutathione oxidized in plants? Front Plant Sci. 2013; 4: 477. doi: 10.3389/fpls.2013.00477 PMID: 24324478
147. Bick JA, Setterdahl AT, Knaff DB, Chen Y, Pitcher LH, Zilinskas BA, et al. Regulation of the plant-type 5′-adenylyl sulfate reductase by oxidative stress. Biochemistry 2001; 40: 9040-9048. PMID: 11467967
148. Gomez LD, Vanacker H, Buchner P, Noctor G, Foyer CH. Intercellular distribution of glutathione synthesis and its response to chilling in maize. Plant Physiol. 2004; 134: 1662-1671. PMID: 15047902
149. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, et al. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 2008; 147: 1358-1368. doi: 10.1104/pp.108.121392 PMID: 18539774
150. Hossain M, Hasanuzzaman M, Fujita M. Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean. Front Agric China. 2011; 5: 1-14.
151. Hossain MA, Mostofa MG, Fujita M. Heat-shock positively modulates oxidative protection of salt and drought-stressed mustard (Brassica campestris L.) seedlings. J Plant Sci Mol Breed. 2013; 2:1-14.
152. Labudda M, Azam FMS. Glutathione-dependent responses of plants to drought: a review. Acta Soc Bot Pol. 2013; 83: 3-12.
153. Zechmann B. Compartment-specific importance of glutathione during abiotic and biotic stress. Front Plant Sci. 2014; 5: 566. doi: 10.3389/fpls.2014.00566 PMID: 25368627
154. Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, et al. Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J. 2002; 32: 329-342. PMID: 12410811
155. Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gakiere B, Vanacker H, et al. Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J. 2007; 52: 640-657. PMID: 17877712
156. Queval G, Jaillard D, Zechmann B, Noctor G. Increased intracellular H2O2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant Cell Environ. 2011; 34: 21-32. doi: 10.1111/j.1365-3040.2010.02222.x PMID: 20807372
157. Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G. Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot. 2010; 61: 4197-4220. doi: 10.1093/jxb/erq282 PMID: 20876333
158. Zagorchev L, Seal CE, Kranner I, Odjakova M. A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci. 2013; 14: 7405-7432. doi: 10.3390/ijms14047405 PMID: 23549272
159. Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 2005; 17: 1866-1875. PMID: 15987996
160. Zaffagnini M, Bedhomme M, Lemaire SD, Trost P. The emerging roles of protein glutathionylation in chloroplasts. Plant Sci. 2012; 185-186: 86-96. doi: 10.1016/j.plantsci.2012.01.005 PMID: 22325869
161. Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH. Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot. 2012; 89: 841-850.
162. Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ. Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J. 2008; 53: 999-1012. PMID: 18088327
163. Maughan SC, Pasternak M, Cairns N, Kiddle G, Brach T, Jarvis R, et al. Plant homologs of the Plasmodium falciparum chloroquine-resistance transporter, PfCRT, are required for glutathione homeostasis and stress responses. Proc Natl Acad Sci USA. 2010; 107: 2331-2336. doi: 10.1073/pnas.0913689107 PMID: 20080670
164. Caplan JF, Filipenko NR, Fitzpatrick SL, Waisman DM. Regulation of annexin A2 by reversible glutathionylation. J Biol Chem. 2004; 279: 7740-7750. PMID: 14668336
165. Su D, Gaffrey MJ, Guo J, Hatchell KE, Chu RK, Clauss TR, et al. Proteomic identification and quantification of S-glutathionylation in mouse macrophages using resin-assisted enrichment and isobaric labeling. Free Radic Biol Med. 2014; 67: 460-470. doi: 10.1016/j.freeradbiomed.2013.12.004 PMID: 24333276
166. Kwon M, Yoon C, Jeong W, Rhee S, Waisman D. Annexin A2-S100A10 heterotetramer, a novel substrate of thioredoxin. J Biol Chem. 2005; 280: 23584-23592. PMID: 15849182
167. Madureira PA, Hill R, Miller VA, Giacomantonio C, Lee PWK, Waisman DM. Annexin A2 is a novel cellular redox regulatory protein involved in tumorigenesis. Oncotarget 2011; 2: 1075-1093. PMID: 22185818
168. Madureira PA, Waisman DM. Annexin A2: the importance of being redox sensitive. Int J Mol Sci. 2013; 14: 3568-3594. doi: 10.3390/ijms14023568 PMID: 23434659
169. Lindermayr C, Saalbach G, Durner J. Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol. 2005; 137: 921-930. PMID: 15734904
170. Muthuramalingam M, Matros A, Scheibe R, Mock H-P, Dietz K-J. The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Front Plant Sci. 2013; 4: 54. doi: 10.3389/fpls.2013.00054 PMID: 23516120
171. Clark G, Konopka-Postupolska D, Hennig J, Roux S. Is annexin 1 a multifunctional protein during stress responses? Plant Signal Behav. 2010; 5: 303-307. PMID: 20215861
172. Sies H. Glutathione and its role in cellular functions. Free Rad Biol Med. 1999; 27: 916-921. PMID: 10569624
173. Masip L, Veeravalli K, Georgiou G. The many faces of glutathione in bacteria. Antioxid Redox Signal. 2006; 8: 753-762. PMID: 16771667