Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Biologia




More options …
Volume 68, Issue 3

Issues

Reactive oxygen species and seed germination

Marcelo Gomes
  • Institut des Sciences de l’environnement, Succ. Centre-Ville, Université du Québec à Montréal, C.P. 8888, H3C 3P8, Montréal, Québec, Canada
  • Departamento de Biologia, Universidade Federal de Lavras, Campus UFLA, 37200-000, Lavras, MG, Brazil
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Queila Garcia
Published Online: 2013-04-13 | DOI: https://doi.org/10.2478/s11756-013-0161-y

Abstract

Reactive oxygen species (ROS) are continuously produced by the metabolically active cells of seeds, and apparently play important roles in biological processes such as germination and dormancy. Germination and ROS accumulation appear to be linked, and seed germination success may be closely associated with internal ROS contents and the activities of ROS-scavenging systems. Although ROS were long considered hazardous molecules, their functions as cell signaling compounds are now well established and widely studied in plants. In seeds, ROS have important roles in endosperm weakening, the mobilization of seed reserves, protection against pathogens, and programmed cell death. ROS may also function as messengers or transmitters of environmental cues during seed germination. Little is currently known, however, about ROS biochemistry or their functions or the signaling pathways during these processes, which are to be considered in the present review.

Keywords: endosperm weakening; ROS signaling; ROS-scavenging systems; seed dormancy

  • [1] Ahmad P., Sarwat M. & Sharma S. 2008. Reactive oxygen species, antioxidants and signaling in plants. J. Plant Biol. 51: 167–173. http://dx.doi.org/10.1007/BF03030694CrossrefGoogle Scholar

  • [2] Bailly C. 2004 Active oxygen species and antioxidants in seed biology. Seed Sci. Res. 14: 93–107. http://dx.doi.org/10.1079/SSR2004159CrossrefGoogle Scholar

  • [3] Bailly C., Audigier C., Ladonne F., Wagner M.H., Coste F., Corbineau F. & Côme D. 2001. Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as re-lated to acquisition of drying tolerance and seed quality. J. Exp. Bot. 52: 701–708. Google Scholar

  • [4] Bailly C., Benamar A., Corbineau F. & Côme D. 1996. Changes in superoxide dismutase, catalase and glutathione reductase activities as related to seed deterioration during accelerated aging of sun-flower seeds. Physiol. Plant. 97: 104–110. http://dx.doi.org/10.1111/j.1399-3054.1996.tb00485.xCrossrefGoogle Scholar

  • [5] 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. Biologies 331: 806–814. 2008 http://dx.doi.org/10.1016/j.crvi.2008.07.022CrossrefGoogle Scholar

  • [6] Bailly C. & Kranner I. 2011. Methods for analyses of reactive oxygen species and antioxidants in relation to seed longevity and germination. Methods Mol. Biol. 773: 343–367. http://dx.doi.org/10.1007/978-1-61779-231-1_20CrossrefGoogle Scholar

  • [7] Barba-Espín G., Diaz-Vivancos P., Job D., Belghazi M., Job C. & Hernandes J.A. 2011. Understanding the role of H2O2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ. 34: 1907–1919. http://dx.doi.org/10.1111/j.1365-3040.2011.02386.xCrossrefGoogle Scholar

  • [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 http://dx.doi.org/10.1105/tpc.111.086694CrossrefGoogle Scholar

  • [9] Buetler T.M., Krauskopf A. & Ruegg U.T. 2004. Role of superoxide as a signaling molecule. News Physiol. Sci. 19: 120–123. Google Scholar

  • [10] Carol R.J. & Dolan L. 2006. The role of reactive oxygen species in cell growth: Lessons from root hairs. J. Exp. Bot. 57: 1829–1834. http://dx.doi.org/10.1093/jxb/erj201CrossrefGoogle Scholar

  • [11] Côme D. & Corbineau F. 1996. Metabolic damage related to desiccation sensitivity, pp. 107–120. In: Ouédrago A.S.S., Poulsen K. & Stubsgaard, F. (eds), Intermediate/Recalcitrant Tropical Forest Tree Seeds. IP-GRI, Roma. Google Scholar

  • [12] Corbineau F., Gay-Mathieu C., Vinel D. & Côme D. 2002. Decrease in sunflower (Helianthus annuus L.) seed viability caused by high temperature as related to energy metabolism, membrane damage and lipid composition. Physiol. Plant. 116: 489–496. http://dx.doi.org/10.1034/j.1399-3054.2002.1160407.xCrossrefGoogle Scholar

  • [13] Dat J., Vandenabeele S., Vranová E., Van Montagu M., Inzé D. & Van Breusegem F. 2000. Dual action of the active oxygen species during plant stress responses. Cell. Mol. Life Sci. 57: 779–795. http://dx.doi.org/10.1007/s000180050041CrossrefGoogle Scholar

  • [14] del Río L.A., Sandalio L.M., Corpas F.J., Palma J.M. & Barroso J.B. 2006. Reactive oxygen species and reactive nitrogen species in peroxisomes: production, scavenging, and role in cell signaling. Plant Physiol. 141: 330–335. http://dx.doi.org/10.1104/pp.106.078204CrossrefGoogle Scholar

  • [15] Desikan R., Hancock J.T., Coffey M.J. & Neill N.J. 1996. Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett. 382: 213–217. http://dx.doi.org/10.1016/0014-5793(96)00177-9CrossrefGoogle Scholar

  • [16] Doke N., Miura Y., Sanchez L.M. & Kawakita K. 1994. Involvement of superoxide in signal transduction: responses to attack by pathogens, physical and chemical shocks and UV irradiation, pp. 177–218. In: Foyer C.H. & Mullineaux P. (eds), Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, Boca Raton, CRC Press. Google Scholar

  • [17] El-Maarouf-Bouteau H. & Bailly C. 2008. Oxidative signaling in seed germination and dormancy. Plant Signal. Behav. 3: 175–182. http://dx.doi.org/10.4161/psb.3.3.5539CrossrefGoogle Scholar

  • [18] Fath A., Bethke P., Beligni V. & Jones R. 2002. Active oxygen and cell death in cereal aleurone cells. J. Exp. Bot. 53: 1273–82. http://dx.doi.org/10.1093/jexbot/53.372.1273CrossrefGoogle Scholar

  • [19] Farrant J.M., Bailly C., Leymarie J., Hamman B., Côme D. & Corbineau F. 2004. Wheat seedlings as a model to understand desiccation tolerance and sensitivity. Physiol. Plant. 120: 563–574. http://dx.doi.org/10.1111/j.0031-9317.2004.0281.xCrossrefGoogle Scholar

  • [20] Finch-Savage W.E., Cadman C.S.C., Toorop P.E., Lynn J.R. & Hilhorst H.W.M. 2007. Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J. 51: 60–78. http://dx.doi.org/10.1111/j.1365-313X.2007.03118.xCrossrefGoogle Scholar

  • [21] Foyer C. & Noctor G. 2009. Redox regulation in photosynthetic organisms: signaling, acclimation and practical implications. Antioxid. Redox Signal. 11: 861–905. http://dx.doi.org/10.1089/ars.2008.2177CrossrefGoogle Scholar

  • [22] Gapper C. & Dolan L. 2006. Control of plant development by reactive oxygen species. Plant Physiol. 141: 341–345. http://dx.doi.org/10.1104/pp.106.079079CrossrefGoogle Scholar

  • [23] Gill S.S. & Tuteta N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48: 909–930. http://dx.doi.org/10.1016/j.plaphy.2010.08.016CrossrefGoogle Scholar

  • [24] Gomes M.P., Carneiro M.M.L.C, Nogueira C.O.G., Soares A.M. & Garcia Q.S. 2012. The system modulating ROS content in germinating seeds of two Brazilian savanna tree species exposed to As and Zn. Acta Physiol. Plant. DOI: 10.1007/s11738-012-1140-6 CrossrefGoogle Scholar

  • [25] Grant J.J. & Loake G.J. 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124: 21–29. http://dx.doi.org/10.1104/pp.124.1.21CrossrefGoogle Scholar

  • [26] Jabs T., Dietrich R.A. & Dangl J.L. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 27: 1853–1856. http://dx.doi.org/10.1126/science.273.5283.1853CrossrefGoogle Scholar

  • [27] Job C., Laugel S., Duval M., Gallardo K. & Job D. 2001. Biochemical characterization of atypical biotinylation domains in seed proteins. Seed Sci. Res. 11: 149–16. Google Scholar

  • [28] 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. http://dx.doi.org/10.1104/pp.105.062778CrossrefGoogle Scholar

  • [29] Karpinski S., Reynolds H., Karpinska B., Wingsle G., Creis-sen G. & Mullineaux P. 1999. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654–657. http://dx.doi.org/10.1126/science.284.5414.654CrossrefGoogle Scholar

  • [30] Kermode A.R. & Finch-Savage B.E. 2002. Desiccation sensitivity in orthodox and recalcitrant seeds in relation to development, pp 149–184. In: Black M. & Pritchard H.W. (eds), Desiccation and Survival in Plants: Drying without Dying, CABI Publishing, Wallingford. http://dx.doi.org/10.1079/9780851995342.0149CrossrefGoogle Scholar

  • [31] Kovtun Y., Chiu W.L., Tena G. & Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97: 2940–2945. http://dx.doi.org/10.1073/pnas.97.6.2940CrossrefGoogle Scholar

  • [32] Kranner I. & Colville L.E. 2011. Metals and seeds: biochemical and molecular implications and their significance for seed germination. Environ. Exp. Bot. 72: 93–105. http://dx.doi.org/10.1016/j.envexpbot.2010.05.005CrossrefGoogle Scholar

  • [33] Kruger N.J. & von Schaewen A. 2003. The oxidative pentose phosphate pathway: structure and organization. Curr. Opin. Plant Biol. 6: 236–246. http://dx.doi.org/10.1016/S1369-5266(03)00039-6CrossrefGoogle Scholar

  • [34] Laloi C., Apel K. & Danon A. 2004. Reactive oxygen signalling: the latest news. Curr. Opin. Plant Biol. 7: 323–328. http://dx.doi.org/10.1016/j.pbi.2004.03.005CrossrefGoogle Scholar

  • [35] Lefevre I., Marchal G., Correal E., Zanuzzi A. & Lutts S. 2009. Variation in response to heavy metals during vegetative growth in Dorycnium pentaphyllum Scop. Plant Growth Regul. 59: 1–11. http://dx.doi.org/10.1007/s10725-009-9382-zCrossrefGoogle Scholar

  • [36] Lehner A., Bailly C., Flechel B., Poels P., Côme D. & Corbineau F. 2006. Changes in wheat seed germination ability, soluble carbohydrate and antioxidant enzyme activities in the embryo during the desiccation phase of maturation. J. Cereal Sci. 43: 175–182. http://dx.doi.org/10.1016/j.jcs.2005.07.005CrossrefGoogle Scholar

  • [37] Levine A., Tenhaken R., Dixon R. & Lamb C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593. http://dx.doi.org/10.1016/0092-8674(94)90544-4CrossrefGoogle Scholar

  • [38] Leymarie J., Vitkauskaité G., Hoang H.H., 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. http://dx.doi.org/10.1093/pcp/pcr129CrossrefGoogle Scholar

  • [39] Liszkay A., van der Zalm E. & Schopfer P. 2004. Production of reactive oxygen intermediates (O (2)(•−), H(2)O(2), and (·)OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol. 136: 3114–3123. http://dx.doi.org/10.1104/pp.104.044784CrossrefGoogle Scholar

  • [40] McDonald M.B. 1999. Seed deterioration: physiology, repair and assessment. Seed Sci. Tech. 27: 177–237. Google Scholar

  • [41] Miller G., Shulaev, V. & Mittler R. 2008. Reactive oxygen signaling and abiotic stress. Physiol. Plant. 133: 481–489. http://dx.doi.org/10.1111/j.1399-3054.2008.01090.xCrossrefGoogle Scholar

  • [42] Mou Z., Fan, W.H. & Dong X.N. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935–944. http://dx.doi.org/10.1016/S0092-8674(03)00429-XGoogle Scholar

  • [43] Müller K., Carstens A.C., Linkies A., Torres M.A. & Leubner-Metzger G. 2009. The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytol. 184: 885–897. http://dx.doi.org/10.1111/j.1469-8137.2009.03005.xCrossrefGoogle Scholar

  • [44] Munné-Bosch S., Ońate M., Oliveira P.G. & Garcia Q.S.2011. Changes in phytohormones and oxidative stress markers in buried seeds of Vellozia alata. Flora 206: 704–711. http://dx.doi.org/10.1016/j.flora.2010.11.012CrossrefGoogle Scholar

  • [45] Neill S., Desikan R. & Hancock J. 2002. Hydrogen peroxide signalling. Curr. Opin. Plant Biol. 5: 388–395. http://dx.doi.org/10.1016/S1369-5266(02)00282-0CrossrefGoogle Scholar

  • [46] Noctor G., De Paepe R. & Foyer C.H. 2007. Mitochondrial redox biology and homeostasis in plants. Trends Plant. Sci. 12: 125–134. http://dx.doi.org/10.1016/j.tplants.2007.01.005CrossrefGoogle Scholar

  • [47] 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. http://dx.doi.org/10.1104/pp.109.138107CrossrefGoogle Scholar

  • [48] Oracz K., El-Maarouf-Bouteau H., Farrant J.M., 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. http://dx.doi.org/10.1111/j.1365-313X.2007.03063.xCrossrefGoogle Scholar

  • [49] Pergo E.M. & Ishii-Iwamoto E.L. 2011. Changes in energy metabolism and antioxidant defense systems during seed germination of the weed species Ipomoea triloba L. and the responses to allelochemicals. J. Chem. Ecol. 37: 500–513. http://dx.doi.org/10.1007/s10886-011-9945-0CrossrefGoogle Scholar

  • [50] Prasad T.K., Anderson M.D., Martin B.A. & Stewart C.R. 1994. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6: 65–74. CrossrefGoogle Scholar

  • [51] Pukacka S. & Ratajczak E. 2007. Age-related biochemical changes during storage of beech (Fagus sylvatica L.) seeds. Seed Sci. Res. 17: 45–53. http://dx.doi.org/10.1017/S0960258507629432CrossrefGoogle Scholar

  • [52] Puntarulo S., Sanchez R.A. & Boveris A. 1988. Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination. Plant Physiol. 86: 626–30. http://dx.doi.org/10.1104/pp.86.2.626CrossrefGoogle Scholar

  • [53] Rajjou L., Lovigny Y., Groot S.P.C., Belghazi M., Job C. & Job D. 2008. Proteome-wide characterization of seed aging in Arabidopsis: A comparison between artificial and natural aging protocols. Plant Physiol 148: 620–641. http://dx.doi.org/10.1104/pp.108.123141CrossrefGoogle Scholar

  • [54] 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. http://dx.doi.org/10.1146/annurev-arplant-042811-105550CrossrefGoogle Scholar

  • [55] Rhoads D.M., Umbach A.L., Subbaiah C.C. & Siedow J.N. 2006. Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 141: 357–366. Google Scholar

  • [56] Rodriguez-Serrano M., Romero-Puertas M.C., Pazmino D.M., Testillano P.S., Risueno M.C., del Rio L.A. & Sandalio L.M. 2009. Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol. 150: 229–243. http://dx.doi.org/10.1104/pp.108.131524CrossrefGoogle Scholar

  • [57] Schweikert C., Liszkay A. & Schopfer P. 2002. Polysaccharide degradation by Fenton reaction- or peroxidase-generated hydroxyl radicals in isolated plant cell walls. Phytochem. 61: 31–35. http://dx.doi.org/10.1016/S0031-9422(02)00183-8CrossrefGoogle Scholar

  • [58] Sharma I. 2012. Arsenic induced oxidative stress in plants. Biologia 67: 447–453. http://dx.doi.org/10.2478/s11756-012-0024-yCrossrefGoogle Scholar

  • [59] Shetty N.P., Jørgensen H.J.L., Jensen J.D., Collinge D.B. & Shetty H.S. 2008. Roles of reactive oxygen species in interactions between plants and pathogens. Eur. J. Plant Pathol. 121: 267–280. http://dx.doi.org/10.1007/s10658-008-9302-5CrossrefGoogle Scholar

  • [60] Sun W.K. & Leopold A.C. 1995. The Maillard reaction and oxidative stress during aging of soybean seeds. Physiol. Plant. 94: 94–104. http://dx.doi.org/10.1111/j.1399-3054.1995.tb00789.xCrossrefGoogle Scholar

  • [61] Tanou G., Job C., Belghazi M., Molassiotis A. & Job D. 2010. Proteomic signatures uncover hydrogen peroxide and nitric oxide in cross-talk signaling network in citrus plants. J. Proteome Res. 9: 5994–6006. http://dx.doi.org/10.1021/pr100782hCrossrefGoogle Scholar

  • [62] Van Breusegem F., Vranová E., Dat J.F. & Inzé D. 2001. The role of active oxygen species in plant signal transduction. Plant Sci. 161: 405–414. http://dx.doi.org/10.1016/S0168-9452(01)00452-6CrossrefGoogle Scholar

  • [63] Vertucci C.W. & Farrant J.M. 1995. Acquisition and loss of desiccation tolerance, pp. 237–271. In: Kigel J. & Galili G. (eds), Seed Development and Germination, Marcel Dekker, New York. Google Scholar

  • [64] Wisniewski J.P., Cornille P., Agnel J.P. & Montillet J.L. 1999. The extensin multigene family responds differentially to superoxide or hydrogen peroxide in tomato cell cultures. — FEBS Lett. 447: 264–268. http://dx.doi.org/10.1016/S0014-5793(99)00315-4CrossrefGoogle Scholar

  • [65] Xu H.N., Li K.Z., Yang F.J., Shi Q. & Wang X. 2010. Overexpression of CsNMAPK in tobacco enhanced seed germination under salt and osmotic stresses. Mol. Biol. Rep. 37: 3157–3163. http://dx.doi.org/10.1007/s11033-009-9895-6CrossrefGoogle Scholar

About the article

Published Online: 2013-04-13

Published in Print: 2013-06-01


Citation Information: Biologia, Volume 68, Issue 3, Pages 351–357, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: https://doi.org/10.2478/s11756-013-0161-y.

Export Citation

© 2013 Slovak Academy of Sciences. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Rekha Kannaujia, Chandra Mohan Srivastava, Vivek Prasad, Brahma N. Singh, and Vivek Pandey
Plant Physiology and Biochemistry, 2019, Volume 142, Page 460
[2]
Sahar A FADHLALMAWLA, Abdel-Aleam H MOHAMED, Jamal Q M ALMARASHI, and Tahar BOUTRAA
Plasma Science and Technology, 2019, Volume 21, Number 10, Page 105503
[3]
Maria A Komkova, Angelika Holzinger, Andreas Hartmann, Alexei R Khokhlov, Christine Kranz, Arkady A Karyakin, and Oleg G Voronin
Beilstein Journal of Nanotechnology, 2013, Volume 4, Page 649
[4]
Paulo Roberto de Moura Souza-Filho, Sarah Bayod Bianchessi, Lydia F. Yamaguchi, Massuo J. Kato, Alessandra Ike Coan, and Massanori Takaki
Flora, 2019, Volume 257, Page 151426
[5]
Ana P. Lando, W. G. Viana, R. A. da Silva, C. D. D. Costa, Hugo P. F. Fraga, Marisa Santos, Paulo T. Mioto, Miguel P. Guerra, and N. Steiner
Journal of Plant Growth Regulation, 2019
[6]
Marcelo Pedrosa Gomes, Elisa Monteze Bicalho, Fernanda Vieira da Silva Cruz, Amanda Miranda Souza, Brenda Maisa Rodrigues Silva, Cíntia de Almeida Gonçalves, Talita Raissa Silva dos Santos, and Queila Souza Garcia
Chemosphere, 2019, Volume 233, Page 905
[7]
Martha Freire da Silva, Eduardo Fontes Araújo, Laércio Junio da Silva, Hugo Tiago Ribeiro Amaro, Luiz Antônio dos Santos Dias, and Denise Cunha Fernandes dos Santos Dias
Ciência e Agrotecnologia, 2019, Volume 43, Number 0
[8]
Satish K. Verma, Ravindra N. Kharwar, and James F. White
Symbiosis, 2019, Volume 78, Number 2, Page 107
[9]
Arruje Hameed, Amjad Hameed, Tahir Farooq, Razia Noreen, Sadia Javed, Shaheera Batool, Ashfaq Ahmad, Tahsin Gulzar, and Matloob Ahmad
BMC Chemistry, 2019, Volume 13, Number 1
[10]
Minwei Xu, Jiajia Rao, and Bingcan Chen
Critical Reviews in Food Science and Nutrition, 2019, Page 1
[11]
Milena Trajković, Dragana Antonić, Aleksandar Cingel, Nabil Ghalawenji, Angelina Subotić, and Slađana Jevremović
3 Biotech, 2019, Volume 9, Number 1
[12]
Tatiana Mamontova, Elena Lukasheva, Gregory Mavropolo-Stolyarenko, Carsten Proksch, Tatiana Bilova, Ahyoung Kim, Vladimir Babakov, Tatiana Grishina, Wolfgang Hoehenwarter, Sergei Medvedev, Galina Smolikova, and Andrej Frolov
International Journal of Molecular Sciences, 2018, Volume 19, Number 12, Page 4066
[13]
Marcelo Pedrosa Gomes, Vinícius Sobrinho Richardi, Elisa Monteze Bicalho, Daiane Cristina da Rocha, Mário Antônio Navarro-Silva, Patrícia Soffiatti, Queila Souza Garcia, and Bruno Francisco Sant'Anna-Santos
Science of The Total Environment, 2019, Volume 651, Page 2671
[14]
Zhan Li, Yue Gao, Yuchan Zhang, Cheng Lin, Dongting Gong, Yajing Guan, and Jin Hu
Frontiers in Plant Science, 2018, Volume 9
[15]
Martin Černý, Hana Habánová, Miroslav Berka, Markéta Luklová, and Břetislav Brzobohatý
International Journal of Molecular Sciences, 2018, Volume 19, Number 9, Page 2812
[16]
Shu Liu, Seiichi Oshita, Dang Quoc Thuyet, Masanao Saito, and Takahiko Yoshimoto
Langmuir, 2018
[17]
Antonia Vidal, Daniel Cantabella, Agustina Bernal-Vicente, Pedro Díaz-Vivancos, and Jose A. Hernández
Journal of Plant Physiology, 2018
[18]
Yanran Ma, Fangqing Chen, Shaohua Chen, Shoupeng Guan, and Chen Chen
Ecohydrology, 2018, Page e2008
[19]
GENAINA A. DE SOUZA, DENISE C.F.S. DIAS, THALINE M. PIMENTA, AMANDA Á. CARDOSO, RAQUEL M.O. PIRES, ANTÔNIO P. ALVARENGA, and EDGARD A.T. PÍCOLI
Anais da Academia Brasileira de Ciências, 2018, Volume 90, Number 2, Page 1625
[20]
Kouichi Nakagawa, Kazuhiro Matsumoto, Nattakan Chaiserm, and Aroonsri Priprem
Journal of Oleo Science, 2017, Volume 66, Number 12, Page 1375
[21]
Marcus Vinicius Prado Alves, Edila Vilela De Resende Von Pinho, Heloisa Oliveira Dos Santos, Gustavo Costa Prado Alves, and Rucyan Walace Pereira
American Journal of Plant Sciences, 2017, Volume 08, Number 10, Page 2569
[22]
W. R. Macedo, G. H. Silva, M. F. C. Santos, A. P. S. Oliveira, and D. S. Souza
Natural Product Research, 2017, Page 1
[23]
Marcelo Pedrosa Gomes and Philippe Juneau
Frontiers in Environmental Science, 2017, Volume 5
[24]
Saeid Khomari, Saeid Golshan-Doust, Raouf Seyed-Sharifi, and Mahdi Davari
New Zealand Journal of Crop and Horticultural Science, 2017, Page 1
[26]
Stefania Vilas Boas Coelho, Sttela Dellyzete Veiga Franco da Rosa, Aline da Consolação Sampaio Clemente, Cristiane Carvalho Pereira, Madeleine Alves de Figueiredo, and Leandro Vilela Reis
Ciência e Agrotecnologia, 2017, Volume 41, Number 3, Page 312
[27]
Antônio César Batista Matos, Eduardo Euclydes de Lima e Borges, and Marcelo Coelho Sekita
Journal of Seed Science, 2014, Volume 36, Number 3, Page 282
[28]
Eduardo Euclydes de Lima e Borges, Glauciana da Mata Ataíde, and Antônio César Batista Matos
Journal of Seed Science, 2015, Volume 37, Number 3, Page 192
[29]
M. R. Panuccio, A. Fazio, C. M. Musarella, A. J. Mendoza-fernández, J. F. Mota, and G. Spampinato
Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, 2017, Page 1
[30]
Marcelo Pedrosa Gomes, Elisa Monteze Bicalho, Élise Smedbol, Fernanda Vieira da Silva Cruz, Marc Lucotte, and Queila Souza Garcia
Journal of Agricultural and Food Chemistry, 2017, Volume 65, Number 11, Page 2279
[31]
Wen-Yan Li, Bing-Xian Chen, Zhong-Jian Chen, Yin-Tao Gao, Zhuang Chen, and Jun Liu
International Journal of Molecular Sciences, 2017, Volume 18, Number 1, Page 110
[32]
Oon Ha Shin, Dae Yeon Kim, and Yong Weon Seo
Journal of the Science of Food and Agriculture, 2017, Volume 97, Number 9, Page 2750
[33]
Marcelo Pedrosa Gomes, Fernanda Vieira da Silva Cruz, Elisa Monteze Bicalho, Felipe Viègas Borges, Marcia Bacelar Fonseca, Philippe Juneau, and Queila Souza Garcia
Environmental Pollution, 2017, Volume 220, Page 452
[34]
Bing-Xian Chen, Wen-Yan Li, Yin-Tao Gao, Zhong-Jian Chen, Wei-Na Zhang, Qin-Jian Liu, Zhuang Chen, and Jun Liu
Frontiers in Plant Science, 2016, Volume 07
[35]
Anushka Moothoo-Padayachie, Boby Varghese, Norman W. Pammenter, Patrick Govender, and Sershen
Botany, 2016, Volume 94, Number 12, Page 1103
[36]
Marcelo Pedrosa Gomes, Fernanda Vieira da Silva Cruz, Felipe Viégas Borges, Márcia Bacelar Fonseca, and Queila Souza Garcia
Environmental and Experimental Botany, 2016, Volume 128, Page 51
[37]
Anna Manara, Giovanni DalCorso, and Antonella Furini
Frontiers in Plant Science, 2016, Volume 7
[38]
S. P. Jeevan Kumar, S. Rajendra Prasad, Rintu Banerjee, and Chakradhar Thammineni
Annals of Botany, 2015, Volume 116, Number 4, Page 663
[39]
Xuan Yao, Juanjuan Li, Jianping Liu, and Kede Liu
Journal of Experimental Botany, 2015, Volume 66, Number 20, Page 6431
[40]
D. Easwar Rao and K.V. Chaitanya
Journal of Food Biochemistry, 2015, Volume 39, Number 4, Page 398
[41]
Amal F.M. Zein Eldin and Hemmat A. Ibrahim
Annals of Agricultural Sciences, 2015, Volume 60, Number 1, Page 121
[42]
Md. Abdullah Yousuf Al Harun, Randall W. Robinson, Joshua Johnson, and Md. Nazim Uddin
South African Journal of Botany, 2014, Volume 93, Page 157
[43]
Leah Rosental, Hiroyuki Nonogaki, and Aaron Fait
Seed Science Research, 2014, Volume 24, Number 01, Page 1

Comments (0)

Please log in or register to comment.
Log in