ASCORBATE PEROXIDASE6 protects arabidopsis desiccating and germinating seeds from stress and mediates cross talk between reactive oxygen species, Abscisic acid, And auxin

Plant Physiology

Volumn 166, Issue 1, 2014, Pages 370-383

  Chen, Changming ^a   Letnik, Ilya ^a   Hacham, Yael ^b,c   Dobrev, Petre ^d   Ben Daniel, Bat Hen ^a   Vanková, Radomíra ^d   Amir, Rachel ^b,c   Miller, Gad ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b MIGAL GALILEE TECHNOLOGY CENTER   (Israel)

^c TEL HAI COLLEGE   (Israel)

^d INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; APX6 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; ASCORBATE PEROXIDASE; INDOLEACETIC ACID DERIVATIVE; REACTIVE OXYGEN METABOLITE; WATER;

ARABIDOPSIS; GENE EXPRESSION; GERMINATION; HEAT; METABOLISM; MUTATION; OXIDATIVE STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCORBATE PEROXIDASES; GENE EXPRESSION; GERMINATION; HOT TEMPERATURE; INDOLEACETIC ACIDS; MUTATION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTOR CROSS-TALK; WATER;

EID: 84907058370     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.245324     Document Type: Article

References (74)

1. Amira G, Ifat M, Tal A, Hana B, Shmuel G, Rachel A (2005) Soluble methionine enhances accumulation of a 15 kDa zein, a methionine-rich storage protein, in transgenic alfalfa but not in transgenic tobacco plants. J Exp Bot 56: 2443–2452
2. Angelovici R, Fait A, Fernie AR, Galili G (2011) A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination. New Phytol 189: 148–159
3. Angelovici R, Galili G, Fernie AR, Fait A (2010) Seed desiccation: a bridge between maturation and germination. Trends Plant Sci 15: 211–218
4. Arrigoni O, De Tullio MC (2000) The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. J Plant Physiol 157: 481–488
5. Baena-González E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13: 474–482
6. Bahin E, Bailly C, Sotta B, Kranner I, Corbineau F, Leymarie J (2011) Crosstalk between reactive oxygen species and hormonal signalling pathways regulates grain dormancy in barley. Plant Cell Environ 34: 980–993
7. Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C R Biol 331: 806–814
8. Bazin J, Langlade N, Vincourt P, Arribat S, Balzergue S, El-Maarouf-Bouteau H, Bailly C (2011) Targeted mRNA oxidation regulates sunflower seed dormancy alleviation during dry after-ripening. Plant Cell 23: 2196–2208
9. Bentsink L, Koornneef M (2008) Seed dormancy and germination. The Arabidopsis Book 6: e0119, doi/10.1199/tab.0050
10. Bouché N, Fait A, Bouchez D, Møller SG, Fromm H (2003) Mitochondrial succinic-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc Natl Acad Sci USA 100: 6843–6848
11. Bournonville CF, Díaz-Ricci JC (2011) Quantitative determination of superoxide in plant leaves using a modified NBT staining method. Phytochem Anal 22: 268–271
12. Chen Q, Yang L, Ahmad P, Wan X, Hu X (2011) Proteomic profiling and redox status alteration of recalcitrant tea (Camellia sinensis) seed in response to desiccation. Planta 233: 583–592
13. Dandoy E, Schyns R, Deltour R, Verly WG (1987) Appearance and repair of apurinic apyrimidinic sites in DNA during early germination of Zea mays. Mutat Res 181: 57–60
14. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17: 268–281
15. Dobrev PI, Kamínek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950: 21–29
16. Dobrev PI, Vankova R (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol Biol 913: 251–261
17. El-Maarouf-Bouteau H, Meimoun P, Job C, Job D, Bailly C (2013) Role of protein and mRNA oxidation in seed dormancy and germination. Front Plant Sci 4: 77
18. Fait A, Nesi AN, Angelovici R, Lehmann M, Pham PA, Song L, Haslam RP, Napier JA, Galili G, Fernie AR (2011) Targeted enhancement of glutamate-to-g-aminobutyrate conversion in Arabidopsis seeds affects carbon-nitrogen balance and storage reserves in a developmentdependent manner. Plant Physiol 157: 1026–1042
19. Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171: 501–523
20. Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59: 387–415
21. Foyer CH, Kerchev PI, Hancock RD (2012) The ABA-INSENSITIVE-4 (ABI4) transcription factor links redox, hormone and sugar signaling pathways. Plant Signal Behav 7: 276–281
22. Galili G (2011) The aspartate-family pathway of plants: linking production of essential amino acids with energy and stress regulation. Plant Signal Behav 6: 192–195
23. Gampala SS, Finkelstein RR, Sun SS, Rock CD (2002) ABI5 interacts with abscisic acid signaling effectors in rice protoplasts. J Biol Chem 277: 1689–1694
24. Gillespie KM, Ainsworth EA (2007) Measurement of reduced, oxidized and total ascorbate content in plants. Nat Protoc 2: 871–874
25. Giraud E, Van Aken O, Ho LH, Whelan J (2009) The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol 150: 1286–1296
26. González-Guzmán M, Apostolova N, Bellés JM, Barrero JM, Piqueras P, Ponce MR, Micol JL, Serrano R, Rodríguez PL (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14: 1833–1846
27. He J, Duan Y, Hua D, Fan G, Wang L, Liu Y, Chen Z, Han L, Qu LJ, Gong Z (2012) DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 24: 1815–1833
28. Holdsworth MJ, Bentsink L, Soppe WJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179: 33–54
29. Ishibashi Y, Tawaratsumida T, Kondo K, Kasa S, Sakamoto M, Aoki N, Zheng SH, Yuasa T, Iwaya-Inoue M (2012) Reactive oxygen species are involved in gibberellin/abscisic acid signaling in barley aleurone cells. Plant Physiol 158: 1705–1714
30. Jiao Y, Sun L, Song Y, Wang L, Liu L, Zhang L, Liu B, Li N, Miao C, Hao F (2013) AtrbohD and AtrbohF positively regulate abscisic acid-inhibited primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis. J Exp Bot 64: 4183–4192
31. Job C, Rajjou L, Lovigny Y, Belghazi M, Job D (2005) Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 138: 790–802
32. Joshi V, Joung JG, Fei Z, Jander G (2010) Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39: 933–947
33. Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64: 2541–2555
34. Krishnamurthy A, Rathinasabapathi B (2013) Oxidative stress tolerance in plants: novel interplay between auxin and reactive oxygen species signaling. Plant Signal Behav 8: 4161, 25761
35. Lariguet P, Ranocha P, De Meyer M, Barbier O, Penel C, Dunand C (2013) Identification of a hydrogen peroxide signalling pathway in the control of light-dependent germination in Arabidopsis. Planta 238: 381–395
36. Lehmann S, Funck D, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids 39: 949–962
37. Leymarie J, Vitkauskaité G, Hoang HH, Gendreau E, Chazoule V, Meimoun P, Corbineau F, El-Maarouf-Bouteau H, Bailly C (2012) Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant Cell Physiol 53: 96–106
38. Lin Y, Yang L, Paul M, Zu Y, Tang Z (2013) Ethylene promotes germination of Arabidopsis seed under salinity by decreasing reactive oxygen species: evidence for the involvement of nitric oxide simulated by sodium nitroprusside. Plant Physiol Biochem 73: 211–218
39. Liu J, Zhou J, XingD(2012) Phosphatidylinositol 3-kinase plays a vital role in regulation of rice seed vigor via altering NADPH oxidase activity. PLoS ONE 7: e33817
40. Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci USA 110: 15485–15490
41. Liu Y, Ye N, Liu R, Chen M, Zhang J (2010) H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. J Exp Bot 61: 2979–2990
42. Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32: 317–328
43. Matityahu I, Godo I, Hacham Y, Amir R (2013) Tobacco seeds expressing feedback-insensitive cystathionine gamma-synthase exhibit elevated content of methionine and altered primary metabolic profile. BMC Plant Biol 13: 206
44. Meng L, Feldman L (2010) A rapid TRIzol-based two-step method for DNA-free RNA extraction from Arabidopsis siliques and dry seeds. Biotechnol J 5: 183–186
45. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2: ra45
46. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133: 481–489
47. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33: 453–467
48. Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) 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 144: 1777–1785
49. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490–498
50. Oracz K, El-Maarouf Bouteau H, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 50: 452–465
51. Oracz K, El-Maarouf-Bouteau H, Kranner I, Bogatek R, Corbineau F, Bailly C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signaling during germination. Plant Physiol 150: 494–505
52. Panchuk II, Volkov RA, Schöffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129: 838–853
53. Parkhey S, Naithani SC, Keshavkant S (2012) ROS production and lipid catabolism in desiccating Shorea robusta seeds during aging. Plant Physiol Biochem 57: 261–267
54. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15: 939–951
55. Quesada V, Ponce MR, Micol JL (2000) Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics 154: 421–436
56. Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63: 507–533
57. Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of a-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134: 1598–1613
58. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide: the response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134: 1683–1696
59. Sarath G, Hou G, Baird LM, Mitchell RB (2007) ABA, ROS and NO are key players during switchgrass seed germination. Plant Signal Behav 2: 492–493
60. Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22: 3560–3573
61. Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Liu C, Feng Y, Cao X, Xie Q (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet 9: e1003577
62. Subbiah V, Reddy KJ (2010) Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis. J Biosci 35: 451–458
63. Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF, Shuman JL, Luo X, Shah J, Schlauch K, et al (2013b) Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25: 3553–3569
64. Suzuki N, Miller G, Sejima H, Harper J, Mittler R (2013a) Enhanced seed production under prolonged heat stress conditions in Arabidopsis thaliana plants deficient in cytosolic ascorbate peroxidase 2. J Exp Bot 64: 253–263
65. Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203: 32–43
66. Tezuka K, Taji T, Hayashi T, Sakata Y (2013) A novel abi5 allele reveals the importance of the conserved Ala in the C3 domain for regulation of downstream genes and salt tolerance during germination in Arabidopsis. Plant Signal Behav 8: e23455
67. Vanderauwera S, Suzuki N, Miller G, van de Cotte B, Morsa S, Ravanat JL, Hegie A, Triantaphylidès C, Shulaev V, Van Montagu MC, et al (2011) Extranuclear protection of chromosomal DNA from oxidative stress. Proc Natl Acad Sci USA 108: 1711–1716
68. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718
69. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS (2012) MetaboAnalyst 2.0: a comprehensive server for metabolomic data analysis. Nucleic Acids Res 40: W127–W133
70. Xia J, Psychogios N, Young N, Wishart DS (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res 37: W652–W660
71. Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143: 291–299
72. Ye N, Zhang J (2012) Antagonism between abscisic acid and gibberellins is partially mediated by ascorbic acid during seed germination in rice. Plant Signal Behav 7: 563–565
73. Ye N, Zhu G, Liu Y, Zhang A, Li Y, Liu R, Shi L, Jia L, Zhang J (2012) Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. J Exp Bot 63: 1809–1822
74. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621–2632