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Oxidant system and ABA drive germination in seeds of palm species with differences in desiccation tolerance

Published online by Cambridge University Press:  01 June 2022

Talita Raissa Silva Santos
Affiliation:
Laboratório de Fisiologia Vegetal, Departamento de Botânica, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Pampulha, Belo Horizonte, Minas Gerais, 31270-901, Brazil
Elisa Monteze Bicalho
Affiliation:
Laboratório de Crescimento e Desenvolvimento de Plantas, Fisiologia Vegetal, Universidade Federal de Lavras, Campus Universitário, Lavras, Minas Gerais 37200-900, Brazil
Queila Souza Garcia*
Affiliation:
Laboratório de Fisiologia Vegetal, Departamento de Botânica, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Pampulha, Belo Horizonte, Minas Gerais, 31270-901, Brazil
*
*Author for Correspondence: Queila Souza Garcia, E-mail: queilagarcia@gmail.com

Abstract

We investigated the thermal thresholds to seed germination and the variations in abscisic acid (ABA) levels and oxidative metabolism during seed dormancy-breaking and germination in two palm species with differences in desiccation tolerance. We used Mauritia flexuosa (buriti palm, desiccation-sensitive seeds) from swampy habitats (Veredas) and Attalea speciosa (babassu, desiccation-tolerant seeds) from the transition zone between the forest and semi-arid region (drained soils). Germination was evaluated at 15–40°C after dormancy-breaking (operculum removal). At optimal temperature for both species (30°C), embryos were sampled in distinct germination phases – dry, imbibed, after operculum removal and at early germination – and used for quantifying ABA and hydrogen peroxide (H2O2) content, antioxidant enzyme activities and for histolocalization of superoxide anion (O2). Seeds of M. flexuosa germinated only in a narrow temperature range (25–35°C), while A. speciosa seeds germinated between 15 and 40°C. After operculum removal, reduced ABA levels in embryos of M. flexuosa were accompanied by constant H2O2 levels, while in A. speciosa, similar levels of ABA and H2O2 were maintained throughout all germination phases. The presence of O2 was restricted to the haustorium, and an increase in O2 accumulation was observed in both species after operculum removal. Similarities were noted between both species regarding enzyme activities; however, the activities were higher in embryos from M. flexuosa. The presence of O2 only in the haustorium indicates that this region of the embryo is an active structure following imbibition and is involved in germination itself, not just functioning in reserve mobilization.

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

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References

Aebi, H (1984) Catalase in vitro. Methods in Enzymology 105, 121126.10.1016/S0076-6879(84)05016-3CrossRefGoogle ScholarPubMed
Allen, PS, Benech-Arnold, RL, Batlla, D, Bradford, KJ, Bradford, K and Nonogaki, H (2007) Modeling of seed dormancy, pp. 72112 in Bradford, KJ and Nonogaki, H (Eds) Seed development, dormancy and germination. Oxford, UK, CAB International.CrossRefGoogle Scholar
Bailly, C (2019) The signalling role of ROS in the regulation of seed germination and dormancy. Biochemical Journal 476, 30193032.CrossRefGoogle ScholarPubMed
Bailly, C, Benamar, A, Corbineau, F and Come, D (1996) Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiologia Plantarum 97, 104110.10.1111/j.1399-3054.1996.tb00485.xCrossRefGoogle Scholar
Baskin, CC and Baskin, JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination. San Diego, Academic Press.Google Scholar
Batlla, D and Benech-Arnold, RL (2010) Predicting changes in dormancy level in natural seed soil banks. Plant Molecular Biology 73, 313.CrossRefGoogle ScholarPubMed
Berjak, P and Pammenter, NW (2001) Seed recalcitrance – current perspectives. South African Journal of Botany 67, 7989.CrossRefGoogle Scholar
Bicalho, EM, Pintó-Marijuan, M, Morales, M, Müller, M, Munné-Bosch, S and Garcia, QS (2015) Control of macaw palm seed germination by the gibberellin/abscisic acid balance. Plant Biology 17, 990996.CrossRefGoogle ScholarPubMed
Bicalho, EM, Motoike, SY, Borges, EEL, Ataíde, GDM and Guimarães, VM (2016) Enzyme activity and reserve mobilization during Macaw palm (Acrocomia aculeata) seed germination. Acta Botanica Brasilica 30, 438444.CrossRefGoogle Scholar
Bicalho, EM, Santos, TR and Garcia, QS (2018) Abscisic acid and the antioxidant system are involved in germination of Butia capitata seeds. Acta Botanica Brasilica 33, 174178.CrossRefGoogle Scholar
Campos, JLA, da Silva, TLL, Albuquerque, UP, Peroni, N and Araújo, EL (2015) Knowledge, use, and management of the Babassu palm (Attalea speciosa Mart. ex Spreng) in the Araripe region (Northeastern Brazil). Economic Botany 69, 240250.CrossRefGoogle Scholar
Chin, HF and Roberts, EH (1980) Recalcitrant crop seeds. Kuala Lumpur, Tropical Press.Google Scholar
Considine, MJ and Foyer, CH (2021) Oxygen and reactive oxygen species-dependent regulation of plant growth and development. Plant Physiology 186, 7992.CrossRefGoogle ScholarPubMed
Coolbear, P, Francis, A and Grierson, D (1984) The effect of low temperature pre-sowing treatment on the germination performance and membrane integrity of artificially aged tomato seeds. Journal of Experimental Botany 35, 16091617.CrossRefGoogle Scholar
DeMason, DA (1988) Embryo structure and storage reserve histochemistry in the palm Washingtonia filifera. American Journal of Botany 75, 330337.CrossRefGoogle Scholar
Diaz-Vivancos, P, Barba-Espín, G and Hernández, JA (2013) Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Reports 32, 14911502.CrossRefGoogle Scholar
El-Maarouf-Bouteau, H and Bailly, C (2008) Oxidative signaling in seed germination and dormancy. Plant Signaling & Behavior 3, 175182.CrossRefGoogle ScholarPubMed
Farooq, M, Basra, SMA, Ahmad, N and Hafeez, K (2005) Thermal hardening: a new seed vigor enhancement tool in rice. Journal of Integrative Plant Biology 47, 187193.CrossRefGoogle Scholar
Finch-Savage, WE and Footitt, S (2012) To germinate or not to germinate: a question of dormancy relief not germination stimulation. Seed Science Research 22, 243248.CrossRefGoogle Scholar
Footitt, S, Douterelo-Soler, I, Clay, H and Finch-Savage, WE (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proceedings of the National Academy of Sciences of the United States of America 108, 2023620241.CrossRefGoogle ScholarPubMed
Foyer, CH and Halliwell, B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 2125.CrossRefGoogle ScholarPubMed
Gehring, C, Zelarayán, MLC, Almeida, RB and Moraes, FHR (2011) Allometry of the babassu palm growing on a slash-and-burn agroecosystem of the eastern periphery of Amazonia. Acta Amazonica 41, 127134.CrossRefGoogle Scholar
Giannopolitis, CN and Ries, SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309314.CrossRefGoogle ScholarPubMed
Giorni, VT, Bicalho, EM and Garcia, QS (2018) Seed germination of Xyris spp. from Brazilian campo rupestre is not associated to geographic distribution and microhabitat. Flora 238, 102109.CrossRefGoogle Scholar
Gomes, MP and Garcia, QS (2013) Reactive oxygen species and seed germination. Biologia 68, 351357.CrossRefGoogle Scholar
Gomes, MP, Carneiro, MMLC, Nogueira, COG, Soares, AM and Garcia, QS (2013) The system modulating ROS content in germinating seeds of two Brazilian savanna tree species exposed to As and Zn. Acta Physiologiae Plantarum 35, 10111022.CrossRefGoogle Scholar
Joët, T, Ourcival, JM and Dussert, S (2013) Ecological significance of seed desiccation sensitivity in Quercus ilex. Annals of Botany 111, 693701.CrossRefGoogle ScholarPubMed
Labouriau, LG (1983) A germinação das sementes. Washington, DC: Secretaria Geral da Organização dos Estados Americanos.Google Scholar
Leprince, O and Buitink, J (2010) Desiccation tolerance: from genomics to the field. Plant Science 179, 554564.CrossRefGoogle Scholar
Liu, Y, Ye, N, Liu, R, Chen, M and Zhang, J (2010) H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. Journal of Experimental Botany 61, 29792990.CrossRefGoogle ScholarPubMed
Lorenzi, H, Noblick, L, Kahn, and Ferreira, EJL (2010) Flora Brasilieira: Arecaceae (Palmeiras). Nova Odessa, Instituto Plantarum.Google Scholar
Maguire, JD (1962) Speed of germination – aid in selection and evaluation for seedling emergence and vigor. Crop Science 2, 176177.CrossRefGoogle Scholar
May, PH, Anderson, AB, Balick, MJ and Frazão, JM (1985) Subsistence benefits from the babassu palm (Orbignya martiana). Economic Botany 39, 113129.CrossRefGoogle Scholar
Miller, GAD, Suzuki, N, Ciftci-Yilmaz, S and Mittler, R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33, 453467.CrossRefGoogle ScholarPubMed
Mittler, R, Vanderauwera, S, Gollery, M and Van Breusegem, F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490498.CrossRefGoogle Scholar
Moura, EF, Ventrella, MC and Motoike, SY (2010) Anatomy, histochemistry and ultrastructure of seed and somatic embryo of Acrocomia aculeata (Arecaceae). Scientia Agricola 67, 399407.CrossRefGoogle Scholar
Nakano, Y and Asada, K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867880.Google Scholar
Oliveira, PG and Garcia, QS (2011) Germination characteristics of Syngonanthus seeds (Eriocaulaceae) in campos rupestres vegetation in South-Eastern Brazil. Seed Science Research 21, 3945.CrossRefGoogle Scholar
Oracz, K, El-Maarouf-Bouteau, H, Kranner, I, Bogatek, R, Corbineau, F and 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 Physiology 150, 494505.CrossRefGoogle ScholarPubMed
Oracz, K, Voegele, A, Tarkowská, D, Jacquemoud, D, Turečková, V, Urbanová, T, Strnad, M, Sliwinska, E and Leubner-Metzger, G (2012) Myrigalone A inhibits Lepidium sativum seed germination by interference with gibberellin metabolism and apoplastic superoxide production required for embryo extension growth and endosperm rupture. Plant and Cell Physiology 53, 8195.CrossRefGoogle ScholarPubMed
Panza, V, Pighin, D, Láinez, V, Pollero, RJ and Maldonado, S (2009) Storage lipids and proteins of Euterpe edulis seeds. Biocell 33, 99106.CrossRefGoogle ScholarPubMed
Ribeiro, JF and Walter, BMT (1998) Fitofisionomias do bioma Cerrado, pp. 89166 in Sano, SM and Almeida, SP (Eds) Cerrado: ambiente e flora. Planaltina, BR, Embrapa – CPAC.Google Scholar
Roach, T, Beckett, RP, Minibayeva, FV, Colville, L, Whitaker, C, Chen, H, Bailly, C and Kranner, I (2010) Extracellular superoxide production, viability, and redox poise in response to desiccation in recalcitrant Castanea sativa seeds. Plant, Cell & Environment 33, 5975.Google ScholarPubMed
Saleh, EOL, Luis, ZG and Scherwinski-Pereira, JE (2017) Determination of physiological and environmental conditions for the storage of babassu palm seeds (Attalea speciosa). Seed Science and Technology 45, 139150.CrossRefGoogle Scholar
Sharma, P, Jha, AB, Dubey, RS and Pessarakli, M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012, 126.CrossRefGoogle Scholar
Spera, MRN, Cunha, R and Teixeira, JB (2001) Quebra de dormência, viabilidade e conservação de sementes de buriti (Mauritia flexuosa). Pesquisa Agropecuária Brasileira 36, 15671572.CrossRefGoogle Scholar
Svenning, JC (2001) On the role of microenvironmental heterogeneity in the ecology and diversification of neotropical rain-forest palms (Arecaceae). The Botanical Review 67, 153.CrossRefGoogle Scholar
Tommasi, F, Paciolla, C and Arrigoni, O (1999) The ascorbate system in recalcitrant and orthodox seeds. Physiologia Plantarum 105, 193198.CrossRefGoogle Scholar
Tweddle, JC, Dickie, JB, Baskin, CC and Baskin, JM (2003) Ecological aspects of seed desiccation sensitivity. Journal of Ecology 91, 294304.CrossRefGoogle Scholar
Umarani, R, Aadhavan, EK and Faisal, MM (2015) Understanding poor storage potential of recalcitrant seeds. Current Science 108, 20232034.Google Scholar
Velikova, V, Yordanov, I and Edreva, A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science 151, 5966.CrossRefGoogle Scholar
Verma, G, Mishra, S, Sangwan, N and Sharma, S (2015) Reactive oxygen species mediate axis-cotyledon signaling to induce reserve mobilization during germination and seedling establishment in Vigna radiata. Journal of Plant Physiology 184, 7988.CrossRefGoogle ScholarPubMed
Virapongse, A, Endress, BA, Gilmore, MP, Horn, C and Romulo, C (2017) Ecology, livelihoods, and management of the Mauritia flexuosa palm in South America. Global Ecology and Conservation 10, 7092.CrossRefGoogle Scholar
Weiler, EW (1980) Radioimmunoassays for the differential and direct analysis of free and conjugated abscisic acid in plant extracts. Planta 148, 262272.CrossRefGoogle ScholarPubMed