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ASCORBATE PEROXIDASE6 protects Arabidopsis desiccating and germinating seeds from stress and mediates cross talk between reactive oxygen species, abscisic acid, and auxin

. 2014 Sep ; 166 (1) : 370-83. [epub] 20140721

Language English Country United States Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

A seed's ability to properly germinate largely depends on its oxidative poise. The level of reactive oxygen species (ROS) in Arabidopsis (Arabidopsis thaliana) is controlled by a large gene network, which includes the gene coding for the hydrogen peroxide-scavenging enzyme, cytosolic ASCORBATE PEROXIDASE6 (APX6), yet its specific function has remained unknown. In this study, we show that seeds lacking APX6 accumulate higher levels of ROS, exhibit increased oxidative damage, and display reduced germination on soil under control conditions and that these effects are further exacerbated under osmotic, salt, or heat stress. In addition, ripening APX6-deficient seeds exposed to heat stress displayed reduced germination vigor. This, together with the increased abundance of APX6 during late stages of maturation, indicates that APX6 activity is critical for the maturation-drying phase. Metabolic profiling revealed an altered activity of the tricarboxylic acid cycle, changes in amino acid levels, and elevated metabolism of abscisic acid (ABA) and auxin in drying apx6 mutant seeds. Further germination assays showed an impaired response of the apx6 mutants to ABA and to indole-3-acetic acid. Relative suppression of abscisic acid insensitive3 (ABI3) and ABI5 expression, two of the major ABA signaling downstream components controlling dormancy, suggested that an alternative signaling route inhibiting germination was activated. Thus, our study uncovered a new role for APX6, in protecting mature desiccating and germinating seeds from excessive oxidative damage, and suggested that APX6 modulate the ROS signal cross talk with hormone signals to properly execute the germination program in Arabidopsis.

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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 PubMed

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 PubMed

Angelovici R, Galili G, Fernie AR, Fait A. (2010) Seed desiccation: a bridge between maturation and germination. Trends Plant Sci 15: 211–218 PubMed

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

Baena-González E, Sheen J. (2008) Convergent energy and stress signaling. Trends Plant Sci 13: 474–482 PubMed PMC

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 PubMed

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 PubMed

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 PubMed PMC

Bentsink L, Koornneef M. (2008) Seed dormancy and germination. The Arabidopsis Book 6: e0119, /10.1199/tab.0050 PubMed PMC

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 PubMed PMC

Bournonville CF, Díaz-Ricci JC. (2011) Quantitative determination of superoxide in plant leaves using a modified NBT staining method. Phytochem Anal 22: 268–271 PubMed

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 PubMed

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

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 PubMed PMC

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 PubMed

Dobrev PI, Vankova R. (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol Biol 913: 251–261 PubMed

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. PubMed PMC

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-γ-aminobutyrate conversion in Arabidopsis seeds affects carbon-nitrogen balance and storage reserves in a development-dependent manner. Plant Physiol 157: 1026–1042 PubMed PMC

Finch-Savage WE, Leubner-Metzger G. (2006) Seed dormancy and the control of germination. New Phytol 171: 501–523 PubMed

Finkelstein R, Reeves W, Ariizumi T, Steber C. (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59: 387–415 PubMed

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 PubMed PMC

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 PubMed PMC

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 PubMed

Gillespie KM, Ainsworth EA. (2007) Measurement of reduced, oxidized and total ascorbate content in plants. Nat Protoc 2: 871–874 PubMed

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 PubMed PMC

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 PubMed PMC

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 PubMed PMC

Holdsworth MJ, Bentsink L, Soppe WJ. (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179: 33–54 PubMed

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 PubMed PMC

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 PubMed

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 PubMed PMC

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 PubMed

Korasick DA, Enders TA, Strader LC. (2013) Auxin biosynthesis and storage forms. J Exp Bot 64: 2541–2555 PubMed PMC

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. PubMed PMC

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 PubMed

Lehmann S, Funck D, Szabados L, Rentsch D. (2010) Proline metabolism and transport in plant development. Amino Acids 39: 949–962 PubMed

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 PubMed

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 PubMed

Liu J, Zhou J, Xing D. (2012) Phosphatidylinositol 3-kinase plays a vital role in regulation of rice seed vigor via altering NADPH oxidase activity. PLoS ONE 7: e33817. PubMed PMC

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 PubMed PMC

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 PubMed PMC

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 PubMed

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. PubMed PMC

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 PubMed

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. PubMed

Miller G, Shulaev V, Mittler R. (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133: 481–489 PubMed

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 PubMed

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 PubMed PMC

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490–498 PubMed

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 PubMed

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 PubMed PMC

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 PubMed PMC

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 PubMed

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 PubMed PMC

Quesada V, Ponce MR, Micol JL. (2000) Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics 154: 421–436 PubMed PMC

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 PubMed

Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D. (2004) The effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134: 1598–1613 PubMed PMC

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 PubMed PMC

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 PubMed PMC

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 PubMed PMC

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. PubMed PMC

Subbiah V, Reddy KJ. (2010) Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis. J Biosci 35: 451–458 PubMed

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 PubMed PMC

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 PubMed PMC

Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. (2014) Abiotic and biotic stress combinations. New Phytol 203: 32–43 PubMed

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. PubMed PMC

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 PubMed PMC

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. PubMed PMC

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 PubMed PMC

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 PubMed PMC

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 PubMed PMC

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 PubMed PMC

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 PubMed PMC

Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621–2632 PubMed PMC

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