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Germination responses in Zephyranthes tubispatha seeds exposed to different thermal conditions and the role of antioxidant metabolism and several phytohormones in their control

Published online by Cambridge University Press:  02 November 2022

María Cecilia Acosta
Facultad de Agronomía, Universidad Nacional del Centro de la Provincia de Buenos Aires (UNCPBA), República Italia 780, 7300 Azul, Buenos Aires, Argentina
Vilma Teresa Manfreda
Facultad de Agronomía, Universidad Nacional del Centro de la Provincia de Buenos Aires (UNCPBA), República Italia 780, 7300 Azul, Buenos Aires, Argentina
María Luciana Alcaraz
Facultad de Agronomía, Universidad Nacional del Centro de la Provincia de Buenos Aires (UNCPBA), República Italia 780, 7300 Azul, Buenos Aires, Argentina
Sergio Alemano
Laboratorio de Fisiología Vegetal, Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, UNRC, Instituto de Investigaciones Agrobiotecnológicas-Consejo Nacional de Investigaciones Científicas y Técnicas (INIAB-CONICET), 5800 Río Cuarto, Córdoba, Argentina
Humberto Fabio Causin*
Instituto de Biodiversidad y Biología Experimental (IBBEA), CONICET-UBA, Departamento de Biodiversidad y Biologia Experimental (DBBE), F.C.E.N., Universidad de Buenos Aires, Ciudad Universitaria, Pab. II, C.A.B.A. C1428EGA, Argentina
*Author for Correspondence: Humberto Fabio Causin, E-mail:


Zephyranthes tubispatha is an ornamental species distributed along several countries of South America. Although it can be multiplied through bulbs or scales, seed germination is a simpler and more cost-effective process. Temperature plays a major role in the control of germination; however, its effect has been scarcely investigated in this species. In the present work, we characterized the germination responses of Z. tubispatha seeds to different temperatures and analyzed the role of key components of the antioxidant metabolism and phytohormones in their control. Seeds showed an optimal temperature range for germination between 14 and 20°C, with higher temperatures (HTs) being progressively inhibitory. While germination was almost nil above 28°C, it could be recovered after transferring the seeds to 20°C, suggesting that thermoinhibition was the underlying phenomenon. The duration of the HT incubation period affected both the time to germination onset and the germination rate at 20°C. Similarly, the activity of antioxidant enzymes, the production of reactive oxygen species in the embryo and the sensitivity to some germination promoters varied depending on the duration of the HT treatment. The addition of 20 μM fluridone was sufficient to recover germination dynamics as in the control treatment when given after a long-term incubation period (25 d) at HT. Ethephon supply was more effective than gibberellins to suppress thermoinhibition, suggesting that changes in the balance and/or sensitivity to ethylene and abscisic acid over time play an important role in the regulation of germination responses to thermal cues in this species.

Research Paper
Copyright © The Author(s), 2022. Published by Cambridge University Press

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Acosta, MC, Alcaraz, ML, Scaramuzzino, RL and Manfreda, VT (2021) Fisiología de la germinación de Rhodophiala bifida. Revista FAVE: Sección Ciencias Agrarias 20, 159173. doi:10.14409/fa.v20i1.10256. (in Spanish).Google Scholar
Afroz, S, Rahman, M and Hassan, M (2018) Taxonomy and reproductive biology of the genus Zephyranthes Herb. (Liliaceae) in Bangladesh. Bangladesh Journal of Plant Taxonomy 25, 5769. doi:10.3329/bjpt.v25i1.37181.CrossRefGoogle Scholar
Anjum, NA, Sharma, P, Gill, SS, Hasanuzzaman, M, Khan, EA, Kachhap, K, Mohamed, AA, Thangavel, P, Devi, GD, Vasudhevan, P, Sofo, A, Khan, NA, Misra, AN, Lukatkin, AS, Singh, HP, Pereira, E and Tuteja, N (2016) Catalase and ascorbate peroxidase-representative H2O2-detoxifying heme enzymes in plants. Environmental Science and Pollution Research International 23, 1900219029. doi:10.1007/s11356-016-7309-6.CrossRefGoogle ScholarPubMed
Argyris, J, Dahal, P, Hayashi, E, Still, DW and Bradford, KJ (2008) Genetic variation for lettuce seed thermoinhibition is associated with temperature-sensitive expression of abscisic acid, gibberellin, and ethylene biosynthesis, metabolism, and response genes. Plant Physiology 148, 926947. doi:10.1104/pp.108.125807.CrossRefGoogle ScholarPubMed
Bahin, E, Bailly, C, Sotta, B, Kranner, I, Corbineau, F and Leymarie, J (2011) Crosstalk between reactive oxygen species and hormonal signalling pathways regulates grain dormancy in barley. Plant, Cell & Environment 34, 980993. doi:10.1111/j.1365-3040.2011.02298.x.CrossRefGoogle ScholarPubMed
Bailly, C (2019) The signalling role of ROS in the regulation of seed germination and dormancy. Biochemical Journal 476, 30193032. doi:10.1042/BCJ20190159.CrossRefGoogle ScholarPubMed
Batlla, D and Benech-Arnold, RL (2014) Weed seed germination and the light environment: implications for weed management. Weed Biology and Management 14, 7787. doi:10.1111/wbm.12039.CrossRefGoogle Scholar
Bewley, JD, Bradford, KJ, Hilhorst, HWM and Nonogaki, H (2013) Seeds: physiology of development, germination and dormancy. New York/Heidelberg/Dordrecht/London, Springer.CrossRefGoogle Scholar
Blokhina, O, Virolainen-Arne, E and Fagerstedt, K (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179194. doi:10.1093/aob/mcf118.CrossRefGoogle ScholarPubMed
Bouzo, CA, Favaro, JC and Pilatti, RA (2007) Improving the germination of celery seeds at high temperature. Journal of Agriculture and Social Sciences 3, 769.Google Scholar
Bradford, MM (1976) A rapid and sensitive method for the estimation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254. doi:10.1016/0003-2697(76)90527-3G.CrossRefGoogle Scholar
Burhan, N, Shaukat, SS and Tahira, A (2001) Effect of zinc and cobalt on germination and seedling growth of Pennisetum americanum (L.) Schumann and Parkinsonia aculeata L. Pakistan Journal of Biological Sciences 4, 575580. doi:10.3923/pjbs.2001.575.580.Google Scholar
Candan, N and Tarhan, L (2003) Changes in chlorophyll-carotenoid contents, antioxidant enzyme activities and lipid peroxidation levels in Zn-stressed Mentha pulegium. Turkish Journal of Chemistry 27, 2130.Google Scholar
Carol, RJ and Dolan, L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. Journal of Experimental Botany 57, 18291834. doi: 10.1093/jxb/erj201.CrossRefGoogle ScholarPubMed
Causin, HF, Roqueiro, G, Petrillo, E, Láinez, V, Pena, LB, Marchetti, CF, Gallego, SM and Maldonado, SB (2012) The control of root growth by reactive oxygen species in Salix nigra Marsh seedlings. Plant Science 183, 197205. doi:10.1016/j.plantsci.2011.08.012.CrossRefGoogle ScholarPubMed
Causin, HF, Bordón, DAE and Burrieza, H (2020) Salinity tolerance mechanisms during germination and early seedling growth in Chenopodium quinoa wild. genotypes with different sensitivity to saline stress. Environmental and Experimental Botany 172, 103995. (1–12). doi:10.1016/j.envexpbot.2020.103995.CrossRefGoogle Scholar
Cavallaro, V, Alza, NP, Murray, MG and Murray, AP (2014) Alkaloids from Habranthus tubispathus and H. jamesonii, two Amaryllidaceae with acetyl- and butyrylcholinesterase inhibition activity. Natural Product Communications 9, 159162. doi:10.1177/1934578X1400900206.CrossRefGoogle Scholar
Çavusoglu, K and Kabar, K (2010) Effects of hydrogen peroxide on the germination and early seedling growth of barley under NaCl and high temperature stresses. Eurasia Journal of Biosciences 4, 7079. doi:10.5053/ejobios.2010.4.0.9.CrossRefGoogle Scholar
Corbineau, F, Xia, Q, Bailly, C and El-Maarouf-Bouteau, H (2014) Ethylene, a key factor in the regulation of seed dormancy. Frontiers in Plant Science 5, 539. doi:10.3389/fpls.2014.00539.CrossRefGoogle ScholarPubMed
da Silva, TA, Baldini, LFG, Ferreira, G, Nakagawa, J and da Silva, EAA (2017) Thermoinhibition in parsley seeds. Bioscience Journal 33, 14121418. doi:10.14393/BJ-v33n6a2017-37192.CrossRefGoogle Scholar
De Gara, L, Paciolla, C, Liso, R, Stefani, A and Arrigoni, O (1991) Correlation between ascorbate peroxidase activity and some anomalies of seedlings from aged caryopses of Dasypyrum villosum (L.) Borb. Journal of Plant Physiology 137, 697700. doi:10.1016/S0176-1617(11)81224-1.CrossRefGoogle Scholar
De Gara, L, Paciolla, C, De Tullio, MC, Motto, M and Arrigoni, O (2000) Ascorbate-dependent hydrogen peroxide detoxification and ascorbate regeneration during germination of a highly productive maize hybrid: evidence of an improved detoxification mechanism against reactive oxygen species. Physiologia Plantarum 109, 713. doi:10.1034/j.1399-3054.2000.100102.x.CrossRefGoogle Scholar
Demidchik, V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environmental and Experimental Botany 109, 212218. doi:10.1016/j.envexpbot.2014.06.021.CrossRefGoogle Scholar
Deng, Z and Song, S (2012) Sodium nitroprusside, ferricyanide, nitrite and nitrate decrease the thermo-dormancy of lettuce seed germination in a nitric oxide-dependent manner in light. South African Journal of Botany 78, 139146. doi:10.1016/j.sajb.2011.06.009.CrossRefGoogle Scholar
Derakhshan, A, Bakhshandeh, A, Siadat, SA, Moradi-Telavat, MR and Andarzian, SB (2018) Quantification of thermoinhibition response of seed germination in different oilseed rape cultivars. Environmental Stresses in Crop Sciences 11, 459469.Google Scholar
De Tullio, M and Arrigoni, O (2003) The ascorbic acid system in seeds: to protect and to serve. Seed Science Research 13, 249260. doi:10.1079/SSR2003143.CrossRefGoogle Scholar
Di Rienzo, JA, Casanoves, F, Balzarini, MG, Gonzalez, L, Tablada, M and Robledo, CW (2017). Infostat. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available at: Scholar
Dunand, C, Crèvecoeur, M and Penel, C (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytologist 174, 332341. doi:10.1111/j.1469-8137.2007.01995.x.CrossRefGoogle ScholarPubMed
Durgbanshi, A, Arbona, V, Pozo, O, Miersch, O, Sancho, JV and Gómez-Cádenas, A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tándem mass spectometry. Journal of Agriculture and Food Chemistry 53, 84378442. doi:10.1021/jf050884b.CrossRefGoogle Scholar
Echeverría, ML and Alonso, SI (2010) Germinación y crecimiento inicial de Habranthus gracilifolius y Rhodophiala bifida, amarilidáceas nativas con potencial ornamental. Revista de la Facultad de Ciencias Agrarias 42, 2337.Google Scholar
El-Maarouf-Bouteau, H and Bailly, C (2008) Oxidative signaling in seed germination and dormancy. Plant Signaling & Behavior 3, 175182. doi:10.4161/psb.3.3.5539.CrossRefGoogle ScholarPubMed
El-Maarouf-Bouteau, H, Meimoun, P, Job, C, Job, D and Bailly, C (2013) Role of protein and mRNA oxidation in seed dormancy and germination. Frontiers in Plant Science 4, 77. doi:10.3389/fpls.2013.00077.CrossRefGoogle ScholarPubMed
Fernández, AC, Marinangeli, P, Curvetto, N and Facciuto, G (2013) Reproductive biology of Habranthus tubispathus. Acta Horticulturae 1000, 183188. doi:10.17660/ActaHortic.2013.1000.23.CrossRefGoogle Scholar
Gallardo, M, Delgado Mdel, M, Sánchez-Calle, IM and Matilla, AJ (1991) Ethylene production and 1-aminocyclopropane-1-carboxylic acid conjugation in thermoinhibited Cicer arietinum L. seeds. Plant Physiology 97, 122127. doi:10.1104/pp.97.1.122.CrossRefGoogle ScholarPubMed
García, N, Meerow, AW, Arroyo-Leuenberger, S, de Oliveira, RS, Dutilh, JH, Soltis, PS and Judd, WS (2019) Generic classification of Amaryllidaceae tribe Hippeastreae. Taxon 68, 481498. doi:10.1002/tax.12062.CrossRefGoogle Scholar
Geshnizjani, N, Ghaderi-Far, F, Willems, LAJ, Hilhorst, HWM and Ligterink, W (2018) Characterization of and genetic variation for tomato seed thermo-inhibition and thermo-dormancy. BMC Plant Biology 18, 229. doi:10.1186/s12870-018-1455-6.CrossRefGoogle ScholarPubMed
Gomes, MP, Bicalho, EM and Garcia, QS (2022) Integrative signaling of hydrogen peroxide and gibberellin on Zn-mediated alleviation of thermodormancy in sorghum seeds. Physiologia Plantarum 174, e13595. doi:10.1111/ppl.13595.CrossRefGoogle ScholarPubMed
Gonai, T, Kawahara, S, Tougou, M, Satoh, S, Hashiba, T, Hirai, N, Kawaide, H, Kamiya, Y and Yoshioka, T (2004) Abscisic acid in the thermoinhibition of lettuce seed germination and enhancement of its catabolism by gibberellin. Journal of Experimental Botany 55, 111118. doi:10.1093/jxb/erh02.CrossRefGoogle ScholarPubMed
Hedden, P and Graebe, JE (1985) Inhibition of gibberellin biosynthesis by paclobutrazol in cell-free homogenates of Cucurbita maxima endosperm and Malus pumila embryos. Journal of Plant Growth Regulation 4, 111. doi:10.1007/BF02266949.CrossRefGoogle Scholar
Hills, PN and van Staden, J (2003) Thermoinhibition of seed germination. South African Journal of Botany 69, 455461.CrossRefGoogle Scholar
Hodges, DM, DeLong, JM, Forney, CF and Prange, RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604611. doi:10.1007/s004250050524.CrossRefGoogle Scholar
Hossain, K, Itoh, R, Yoshimura, G, Tokuda, G, Oku, H, Cohen, M and Yamasaki, H (2010) Effects of nitric oxide scavengers on thermoinhibition of seed germination in Arabidopsis thaliana. Russian Journal of Plant Physiology 57, 222232. doi:10.1134/S1021443710020093.CrossRefGoogle Scholar
Huo, H and Bradford, K (2015) Molecular and hormonal regulation of thermoinhibition of seed germination, pp. 333 in Anderson, J (Ed.), Advances in plant dormancy, Cham, Springer. doi:10.1007/978-3-319-14451-1_1.Google Scholar
Huo, H, Wei, S and Bradford, KJ (2016) Delay of germination (DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proceedings of the National Academy of Sciences USA 113, 21992206. doi:10.1073/pnas.1600558113.CrossRefGoogle ScholarPubMed
Hurrell, JA, Bazzano, DH and Delucci, G (2005) Monocotiledóneas Herbáceas. Nativas y exóticas. In Hurell, JA (ed.), Biota Rioplatense. Vol. X., 320 p. Editorial LOLA (Literature of Latin America), Buenos Aires, Argentina.Google Scholar
Ishibashi, Y, Tawaratsumida, T, Zheng, S-H, Yuasa, T and Iwaya-Inoue, M (2010) NADPH oxidases act as key enzyme on germination and seedling growth in barley (Hordeum vulgare L. Plant Production Science 13, 4552. doi:10.1626/ pps.13.45.CrossRefGoogle Scholar
Ishibashi, Y, Kasa, S, Sakamoto, M, Aoki, N, Kai, K, Yuasa, T, Hanada, A, Yamaguchi, S and Iwaya-Inoue, M (2015) A role for reactive oxygen species produced by NADPH oxidases in the embryo and aleurone cells in barley seed germination. PLoS One 10, e0143173. doi:10.1371/journal.pone.0143173.CrossRefGoogle ScholarPubMed
Ishibashi, Y, Aoki, N, Kasa, S, Sakamoto, M, Kai, K, Tomokiyo, R, Watabe, G, Yuasa, T and Iwaya-Inoue, M (2017) Interrelationship between abscisic acid and reactive oxygen species plays a key role in barley seed dormancy and germination. Frontiers in Plant Science 8, 275. doi:10.3389/fpls.2017.00275.CrossRefGoogle Scholar
ISTA (2006) International rules for seed testing. Rules. Seed Science & Technology 13, 299355.Google Scholar
Jabs, T, Dietrich, RA and Dangl, JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 18531856. doi:10.1126/science.273.5283.1853.CrossRefGoogle Scholar
Kendall, S and Penfield, S (2012) Maternal and zygotic temperature signalling in the control of seed dormancy and germination. Seed Science Research 22, S23S29. doi:10.1017/S0960258511000390.CrossRefGoogle Scholar
Keys, RD, Orrin, ES, Kumamoto, J and Lyon, JL (1975) Effect of gibberellic acid, kinetin, and ethylene plus carbon dioxide on the thermodormancy of lettuce seed (Lactuca sativa L. Cv. Mesa 659). Plant Physiology 56, 826829.CrossRefGoogle ScholarPubMed
Kokila, M, Bhaskaran, M, Sathish, S and Lakshmi Prasanna, K (2014) Review on positive role of reactive oxygen species (ROS) in seed germination. International Journal of Development Research 4, 105109.Google Scholar
Kolářová, P, Bezděčková, L and Procházková, Z (2010) Effect of gibberellic acid and ethephon on the germination of European beech dormant and chilled beechnuts. Journal of Forest Science 56, 389396. doi:10.17221/32/2010-JFS.CrossRefGoogle Scholar
Leymarie, J, Robayo-Romero, ME, Gendreau, E, Benech-Arnold, RL and Corbineau, F (2008) Involvement of ABA in induction of secondary dormancy in barley (Hordeum vulgare L.) seeds. Plant & Cell Physiology 49, 18301838. doi:10.1093/pcp/pcn164.CrossRefGoogle ScholarPubMed
Leymarie, J, Benech-Arnold R, L, Farrant J, M and Corbineau, F (2009) Thermodormancy and ABA metabolism in barley grains. Plant Signaling & Behavior 4, 205207. doi:10.4161/psb.4.3.7797.CrossRefGoogle ScholarPubMed
Leymarie, J, Vitkauskaité, G, Hoang, HH, Gendreau, E, Chazoule, V, Meimoun, P and Bailly, C (2012) Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant & Cell Physiology 53, 96106. doi:10.1093/pcp/pcr129.CrossRefGoogle Scholar
Li, RS, Zhi, JZ and Fu, SH (2019) NADPH oxidases, essential players of hormone signaling in plant development and response to stresses. Plant Signaling & Behavior 14, 11. doi:10.1080/15592324.2019.1657343.Google Scholar
Linkies, A and Leubner-Metzger, G (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Reports 31, 253270. doi:10.1007/s00299-011-1180-1.CrossRefGoogle ScholarPubMed
Liszkay, A, van der Zalm, E and Schopfer, PM (2004) Production of reactive oxygen intermediates (O2•−, H2O2, and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiology 136, 31143123. doi:10.1104/pp.104.044784.CrossRefGoogle Scholar
Liu, J, Zhou, J and 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. doi:10.1371/journal.pone.0033817.CrossRefGoogle Scholar
Liu, J, Hasanuzzaman, M, Wen, H, Zhang, J, Peng, T, Sun, H and Zhao, Q (2019) High temperature and drought stress cause abscisic acid and reactive oxygen species accumulation and suppress seed germination growth in rice. Protoplasma 256, 12171227. doi:10.1007/s00709-019-01354-6.CrossRefGoogle ScholarPubMed
Ma, W, Guan, X, Li, J, Pan, R, Wang, L, Liu, F, Ma, H, Zhu, S, Hu, J, Ruan, Y-L, Chen, X and Zhang, T (2019) Mitochondrial small heat shock protein mediates seed germination via thermal sensing. Proceedings of the National Academy of Sciences USA 116, 4716–4472. doi:10.1073/pnas.1815790116.CrossRefGoogle ScholarPubMed
Manfreda, VT, Acosta, MC and Alcaráz, ML (2019). Germination of Habranthus tubispathus at high temperature. Boletín de la Sociedad Argentina de Botánica. Abstract. XXXVII jornadas Argentinas de Botánica. (in Spanish). Available at: Scholar
Manfreda, VT, Alcaraz, ML and Scaramuzzino, RL (2020) Germinación de Baccharis dracunculifolia subsp. tandilensis: caracterización basada en la temperatura, la luz y la salinidad. Rodriguesia 71, e02642017. doi:10.1590/2175-7860202071035.CrossRefGoogle Scholar
Maza, IM, Uría, R and Roitman, GG (2004) Propagación sexual de diferentes especies nativas del género Habranthus, p. 4345. in Actas del II Congreso Argentino de Floricultura y Plantas Ornamentales, VI Jornadas Nacionales de Floricultura y I Encuentro Latinoamericano de Floricultura. INTA, Buenos Aires.Google Scholar
Nambara, E, Okamoto, M, Tatematsu, K, Yano, R, Seo, M and Kamiya, Y (2010) Abscisic acid and the control of seed dormancy and germination. Seed Science Research 20, 5567. doi:10.1017/S0960258510000012.CrossRefGoogle Scholar
Orabi, SA and Abou-Hussein, SD (2019) Antioxidant defense mechanisms enhance oxidative stress tolerance in plants. A review. Current Science International 8, 565576.Google Scholar
Oracz, K, Bouteau, HE-M, Farrant, JM, Cooper, K, Belghazi, M, Job, C, Job, D, Corbineau, F and Bailly, C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. The Plant Journal 50, 452465. doi:10.1111/j.1365-313X.2007.03063.x.CrossRefGoogle ScholarPubMed
Pedrosa Gomes, M and Souza Garcia, Q (2013) Reactive oxygen species and seed germination. Biologia (Section Botany) 68, 351357. doi:10.2478/s11756-013-0161-y.CrossRefGoogle Scholar
Prieto, P, Pineda, M and Aguilar, M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Analytical Biochemistry 269, 337341. doi:10.1006/abio.1999.4019.CrossRefGoogle Scholar
Rao, VS, Sankhla, N and Khan, AA (1975) Additive and synergistic effects of kinetin and ethrel on germination, thermodormany, and polyribosome formation in lettuce seeds. Plant Physiology 56, 263266. doi: 10.1104/pp.56.2.263.CrossRefGoogle ScholarPubMed
Renew, S, Heyno, E, Schopfer, P and Liszkay, A (2005) Sensitive detection and localization of hydroxyl radical production in cucumber roots and Arabidopsis seedlings by spin trapping electron paramagnetic resonance spectroscopy. The Plant Journal 44, 342347. doi:10.1111/j.1365-313X.2005.02528.x.CrossRefGoogle ScholarPubMed
Rosselló, FJ, Marinangeli, PA, Rodrigo, JM and Curvetto, NR (2006) Propagación vegetativa de Habranthus tubispathus Herb. (Amarilidaceae), in Congreso Argentino de Floricultura. 3. Jornadas Nacionales de Floricultura. La Plata, Buenos Aires, Argentina.Google Scholar
Saini, HS, Consolacion, ED, Bassi, PK and Spencer, MS (1989) Control processes in the induction and relief of thermoinhibition of lettuce seed germination. Actions of phytochrome and endogenous ethylene. Plant Physiology 90, 311315.CrossRefGoogle ScholarPubMed
Santa Cruz, RH, Tapia, AM, Romero, A and Quiroga, A (2011) Propagación por semilla de Zephyranthes mesochloa, especie nativa con potencial ornamental. Biología en Agronomía 1, 1723.Google Scholar
Schaller, GE and Binder, BM (2017) Inhibitors of ethylene biosynthesis and signaling. In Ethylene Signaling. Humana Press, New York, NY, pp. 223235.CrossRefGoogle Scholar
Singh, KL, Chaudhuri, A and Kar, RK (2014) Superoxide and its metabolism during germination and axis growth of Vigna radiata (L.) Wilczek seeds. Plant Signaling & Behavior 9, e29278. doi:10.4161/psb.29278.CrossRefGoogle ScholarPubMed
Sofo, A, Scopa, A, Nuzzaci, M and Vitti, A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences 16, 1356113578. doi:10.3390/ijms160613561.CrossRefGoogle ScholarPubMed
Tamura, N, Yoshida, T, Tanaka, A, Sasaki, R, Bando, A, Toh, S and Kawakami, N (2006) Isolation and characterization of high temperature-resistant germination mutants of Arabidopsis thaliana. Plant & Cell Physiology 47, 10811094. doi:10.1093/pcp/pcj078.CrossRefGoogle ScholarPubMed
Thomas, TH, Dearman, AS and Biddington, NL (1986) Evidence for the accumulation of a germination inhibitor during progressive thermoinhibition of seeds of celery (Apium graveolens L. Plant Growth Regulation 4, 177184. doi:10.1007/BF00025199.CrossRefGoogle Scholar
Thordal-Christensen, H, Zhang, ZG, Wei, YD and Collinge, DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal 11, 11871194. doi:10.1046/j.1365-313X.1997.11061187.x.CrossRefGoogle Scholar
Tillich, H-J (1995) Seedlings and systematics in monocotyledons, pp. 303352 in Rudall, PJ; Cribb, PJ; Cutler, DF and Humphries, C (Eds.), Monocotyledons: systematics and evolution, Kew, Royal Botanic Gardens.Google Scholar
Toh, S, Imamura, A, Watanabe, A, Nakabayashi, K, Okamoto, M, Jikumaru, Y, Hanada, A, Aso, Y, Ishiyama, K, Tamura, N, Iuchi, S, Kobayashi, M, Yamaguchi, S, Kamiya, Y, Nambara, E and Kawakami, N (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiology 146, 13681385. doi:10.1104/pp.107.113738.CrossRefGoogle ScholarPubMed
Toh, S, Kamiya, Y, Kawakami, N, Nambara, E, McCourt, P and Tsuchiya, Y (2012) Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant & Cell Physiology 53, 107117. doi:10.1093/pcp/pcr176.CrossRefGoogle ScholarPubMed
Vavilin, D, Ducruet, JM, Matorin, D, Venediktov, P and Rubin, A (1998) Membrane lipid peroxidation, cell viability and photosystem II activity in the green alga Chlorella pyrenoidosa subjected to various stress conditions. Journal of Photochemistry and Photobiology B: Biology 42, 233239. doi:10.1016/S1011-1344(98)00076-1.CrossRefGoogle Scholar
Vishal, B and Kumar, PP (2018) Regulation of seed germination and abiotic stresses by gibberellins and abscisic acid. Frontiers in Plant Science 9, 838. doi:10.3389/fpls.2018.00838.CrossRefGoogle ScholarPubMed
Wei, S, Yang, X, Huo, G, Ge, G, Liu, H, Luo, L, Hu, J, Huang, D and Long, P (2020) Distinct metabolome changes during seed germination of lettuce (Lactuca sativa L.) in response to thermal stress as revealed by untargeted metabolomics analysis. International Journal of Molecular Sciences 21, 1481. doi:10.3390/ijms21041481.CrossRefGoogle ScholarPubMed
Wesley da Silva, M, Guerra Barbosa, L, Barboza da Silva, JES, Silva Guirra, K, da Silva Gama, DR, Moreira de Oliveira, G and França Dantas, B (2014) Characterization of seed germination of Zephyranthes sylvatica (Mart.) Baker (Amaryllidaceae). Journal of Seed Science 36, 178185. doi:10.1590/2317-1545v32n2923.CrossRefGoogle Scholar
Xia, Q, Ponnaiah, M, Thanikathansubramanian, K, Corbineau, F, Bailly, C, Nambara, E, Meimoun, P and El-Maarouf-Bouteau, H (2019) Re-localization of hormone effectors is associated with dormancy alleviation by temperature and after-ripening in sunflower seeds. Scientific Reports 9, 4861. doi:10.1038/s41598-019-40494-w.CrossRefGoogle ScholarPubMed
Yan, A and Chen, Z (2020) The control of seed dormancy and germination by temperature, light and nitrate. The Botanical Review 86, 3975. doi:10.1007/s12229-020-09220-4.CrossRefGoogle Scholar
Ye, N, Zhu, G, Liu, Y, Zhang, A, Li, Y, Liu, R, Shi, L, Jia, L and Zhang, J (2012) Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. Journal of Experimental Botany 63, 18091822. doi:10.1093/jxb/err336.CrossRefGoogle ScholarPubMed
Yoong, FY, O'Brien, LK, Truco, MJ, Huo, H, Sideman, R, Hayes, R and Bradford, KJ (2016) Genetic variation for thermotolerance in lettuce seed germination is associated with temperature-sensitive regulation of ethylene response factor1 (ERF1). Plant Physiology 170, 472488. doi:10.1104/pp.15.01251.CrossRefGoogle ScholarPubMed
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