Conservation and physiological quality of Handroanthus spongiosus (Rizzini) S. Grose (Bignoniaceae) seeds

Jailton de Jesus Silva Sara de Souza Alencar Raquel Araujo Gomes Janete Rodrigues Matias Claudinéia Regina Pelacani Bárbara França Dantas About the authors

Abstract:

Handroanthus spongiosus (Rizzini) S. Grose is an endangered tree species. However, its seed quality, storage, and conservation strategies are issues still unexplored. This study aimed to evaluate the physiological quality of H. spongiosus seeds subjected to different storage times, packaging, and environments for their conservation. A completely randomized experimental design was used, in a double factorial arrangement with an additional treatment (recently-harvested seeds), consisted of five storage times (up to 24 months) and six storage conditions, combining packaging types (permeable and impermeable) and environments (room, cold chamber, freezer, and liquid nitrogen conditions). Seed germination percentage and normal seedling percentage, shoot length, root length, and root to shoot dry weight ratio were evaluated. The seed germination and normal seedling percentages of H. spongiosus seeds conserved under room conditions decreased over the storage time. Normal seedling percentages decreased from the 12th month of storage onwards. Low and ultralow temperatures are recommended for short and medium-term conservation of H. spongiosus seeds, since they did not affect the growth of seedlings.

Index terms:
Caatinga; dry forest; germination; longevity; storage

Resumo:

Handroanthus spongiosus (Rizzini) S. Grose é uma espécie arbórea ameaçada. No entanto, a qualidade de suas sementes, o armazenamento e as estratégias de conservação ainda são questões inexploradas. O objetivo deste trabalho foi avaliar a resposta temporal a diferentes embalagens e ambientes de armazenamento na conservação da qualidade fisiológica das sementes de H. spongiosus. O delineamento experimental foi inteiramente casualizado em esquema fatorial duplo com tratamento adicional (sementes recém-colhidas), considerando cinco períodos de armazenamento (até 24 meses) e seis condições de armazenamento, combinando embalagens (permeável ou impermeável) e ambientes (laboratório, câmara fria, freezer e nitrogênio líquido). Germinação, plântulas normais, comprimento da parte aérea e raiz e relação entre a massa seca de raiz e parte aérea foram avaliadas. As sementes de H. spongiosus mantidas em ambiente de laboratório apresentaram decréscimo na porcentagem de germinação e de plântulas normais ao longo do armazenamento. A porcentagem de plântulas normais diminuiu apenas a partir de 12 meses de armazenamento. Temperaturas baixas e ultrabaixas podem ser indicadas para a conservação da qualidade das sementes em armazenamento a curto e médio prazo, uma vez que o crescimento de plântulas não foi afetado.

Termos para indexação:
Caatinga; floresta seca; germinação; longevidade; armazenamento

INTRODUCTION

Anthropogenic actions have contributed for the degradation of the Caatinga biome through practices characterized by the exploratory process of this region, such as the removal and burning of native vegetation and agricultural and livestock activities (Ferreira et al., 2014FERREIRA, C.D.; SOUTO, P.C.; LUCENA, D.S.; SALES, S.C.V.; SOUTO, J.S. Florística do banco de sementes no solo em diferentes estágios de regeneração natural de Caatinga. Revista Brasileira de Ciências Agrárias, v.9, n.4, p.562-569, 2014. https://www.redalyc.org/pdf/1190/119032902015.pdf
https://www.redalyc.org/pdf/1190/1190329...
). In addition, many plant species have been threatened around the world due to aggression to ecosystems and impoverishment of biodiversity caused by these actions (Voronkova et al., 2018VORONKOVA, N.M.; KHOLINA, A.B.; KOLDAEVA, M.N.; NAKONECHNAYA, O.; NECHAEV, V.A. Morphophysiological dormancy, germination, and cryopreservation in Aristolochia contorta seeds. Plant Ecology and Evolution, v.151, n.1, p.77-86, 2018. https://doi.org/10.5091/plecevo.2018.1351
https://doi.org/10.5091/plecevo.2018.135...
).

Thus, conservationist strategies for threatened species have been developed and applied as alternatives for ex situ conservation through seed or seedling production in different times of the year (Shen et al., 2015SHEN, S.K.; WU, F.Q.; YANG, G.S.; WANG, Y.H.; SUN, W.B. Seed germination and seedling emergence in the extremely endangered species Rhododendron protistum var. giganteum-the world’s largest Rhododendron. Flora-Morphology, Distribution, Functional Ecology of Plants, v.216, p.65-70, 2015. https://doi.org/10.1016/j.flora.2015.08.006
https://doi.org/10.1016/j.flora.2015.08....
). Therefore, determining conservation strategies for seeds of threatened wild species is required and involves the maintenance of their viability and physiological potential during storage (Araujo et al., 2017ARAUJO, M.D.N.; FERRAZ, M.; AMÉRICO, F.K.A.; SILVA, F.F.S.; DANTAS, B.F.; CRUZ, C.R.P. Seed quality of Amburana cearensis (Allemão) AC Sm. (Fabaceae) is influenced by storage condition. Journal of Seed Science , v.39, n.4, p.401-409, 2017. https://doi.org/10.1590/2317-1545v39n4179328
https://doi.org/10.1590/2317-1545v39n417...
).

The storage environment and packaging affect the maintenance of viability and vigor of seeds in the short-, medium-, and long-terms. Successfully conserving forest seeds require previous information on physiological characteristics, since seeds from different species require different conditions for conservation (Vitis et al., 2020VITIS, M.; HAY, F.R.; DICKIE, J.B.; TRIVEDI, C.; CHOI, J.; FIEGENER, R. Seed storage: maintaining seed viability and vigor for restoration use. Restoration Ecology, v.28, n.3, p.249-255, 2020. https://doi.org/10.1111/rec.13174
https://doi.org/10.1111/rec.13174...
; Walters and Pence, 2021WALTERS, C.; PENCE, V.C. The unique role of seed banking and cryobiotechnologies in plant conservation. Plants, People, Planet, v.3, n.1, p.83-91, 2021. https://doi.org/10.1002/ppp3.10121
https://doi.org/10.1002/ppp3.10121...
).

Determining ideal environmental conditions, such as relative air humidity and temperature, for the conservation of seeds is needed to maintain their physiological quality during storage (Veiga-Barbosa et al., 2013VEIGA-BARBOSA, L.; MIRA, S.; GONZÁLEZ-BENITO, M.E.; SOUZA, M.M.; MELETTI, L.M.M.; PÉREZ-GARCÍA, F. Seed germination, desiccation tolerance and cryopreservation of Passiflora species. Seed Science and Technology , v.41, n.1, p.89-97, 2013. https://doi.org/10.15258/sst.2013.41.1.08
https://doi.org/10.15258/sst.2013.41.1.0...
; Tonetto et al., 2015TONETTO, T.D.S.; ARAUJO, M.M.; MUNIZ, M.F.B.; WALKER, C.; BERGHETTI, A.L.P. Storage and germination of seeds of Handroanthus heptaphyllus (Mart.) Mattos. Journal of Seed Science , v.37, p.40-46, 2015. https://doi.org/10.1590/2317-1545v37n1141116
https://doi.org/10.1590/2317-1545v37n114...
). An adequate storage environment can minimize the speed deterioration, allowing the maintenance of viability of seeds for a longer period than that obtained under natural non-controlled conditions (Torres et al., 2020TORRES, M.F.O.; FERREIRA, R.A.; PRATA, L.C.D.; SILVA-MANN, R. Seed Longevity of Enterolobium contortisiliquum (Vell.) Morong. Journal of Seed Science , v.42, 2020. https://doi.org/10.1590/2317-1545v42239618
https://doi.org/10.1590/2317-1545v422396...
). In addition, initial seed water content and storage packaging affect the maintenance of the seed physiological quality due to gas exchanges between seeds and the environment (Reis et al., 2012REIS, R.C.R.; PELACANI, C.R.; ANTUNES, C.G.C.; DANTAS, B.F.; CASTRO, R.D. Physiological quality of Gliricidia sepium (Jacq.) Steud. (Leguminosae - Papilionoideae) seeds subjected to different storage conditions. Revista Árvore, v.36, n.2, p.229-235, 2012. https://doi.org/10.1590/S0100-67622012000200004
https://doi.org/10.1590/S0100-6762201200...
; Lúcio et al., 2016LÚCIO, A.A.; ARAUJO, M.N.; SILVA, F.F.S.; DANTAS, B.F. Effect of storage in different environments and packages on germination of Amburana cearensis (Allemao) A. C. Sm. seeds. International Journal of Environment, Agriculture and Biotechnology, v.1, n.4, p. 1037-1040, 2016. http://dx.doi.org/10.22161/ijeab/1.4.57
http://dx.doi.org/10.22161/ijeab/1.4.57...
; Gomes et al., 2018GOMES, S.E.V.; SANTOS, K.C.; OLIVEIRA, G.M.; ARAÚJO, M.N.; DANTAS, B.F. Sementes de Myracrodruon urundeuva podem ser armazenadas por até dois anos em ambiente seco. Informativo Abrates , v.28, n.1, p.102-106, 2018. https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1109071/1/Barbara.pdf
https://www.alice.cnptia.embrapa.br/alic...
; Ribeiro et al., 2018RIBEIRO, R.C.; GOMES, S.E. V.; DANTAS, B.F. Physiological quality of Erythrina velutina Willd. (FABACEAE) seeds under different storage conditions. Scientia Forestalis, v.46, n.120, p. 562-570, 2018. https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1104185/1/bARBARA.pdf
https://www.alice.cnptia.embrapa.br/alic...
).

The plant species Handroanthus spongiosus (Rizzini) S. Grose, popularly known in Brazil as cascudo, ipê-cascudo or sete-cascas, belongs to the Bignoniaceae family. It is endemic to the Caatinga biome and is classified as an endangered species, according to the official national list of threatened flora species (Lohmann et al., 2013LOHMANN, L.G.; SFAIR, J.C.; MONTEIRO, N.P.; SANTOS-FILHO, L.A.F. Bignoniaceae. In: MARTINELLI, G.; MORAES, M.A. (Eds.). Livro vermelho da flora do Brasil. 1. ed. Rio de Janeiro: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro 2013. p. 303-314.; Lohmann, 2020LOHMANN, L.G. Handroanthus in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. 2020. Disponível em: Disponível em: http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB117471 . Acesso em: 05 dez. 2021.
http://floradobrasil.jbrj.gov.br/reflora...
).

Seeds from plants of the Handroanthus genus present a relatively short natural viability period, which hinders the conservation and, consequently, the production of seedlings for these species (Cabral et al., 2003CABRAL, E.L.; BARBOSA, D.C.A.; SIMABUKURO, E.A. Armazenamento e germinação de sementes de Tabebuia aurea (Manso) Benth. & Hook. f. ex. S. Moore. Acta Botanica Brasilica, v.17, n.4, p.609-617, 2003. https://doi.org/10.1590/S0102-33062003000400013
https://doi.org/10.1590/S0102-3306200300...
). Researchers have developed and published works involving the storage of different Handroanthus species over the last years due to the importance of these species (Shibata et al., 2012SHIBATA, M.; COELHO, C.M.M.; OLIVEIRA, L.M.D.; GARCIA, C. Accelerated aging of ipê seeds under controlled conditions of storage. Revista Brasileira de Sementes , v.34, p.247-254, 2012. https://www.scielo.br/j/rbs/a/vg4KLkZW7gyJwT5RVQYvMCF/?format=pdf⟨=en
https://www.scielo.br/j/rbs/a/vg4KLkZW7g...
; Abbade and Takaki, 2014ABBADE, L.C.; TAKAKI, M. Biochemical and physiological changes of Tabebuia roseoalba (Ridl.) Sandwith (Bignoniaceae) seeds under storage. Journal of Seed Science, v.36, p. 100-107, 2014. https://www.scielo.br/j/jss/a/9RwhTDnCrXbRPg7ZmXDyHYd/?lang=en
https://www.scielo.br/j/jss/a/9RwhTDnCrX...
; Martins and Pinto, 2014MARTINS, C.C.; PINTO, M.A.D.S.C. Armazenamento de sementes de ipê-amarelo-do-brejo (Handroanthus umbellatus (Sond.) Mattos. Bignoniaceae). Ciência Florestal , v.24, n.3, p. 533-539, 2014. https://www.scielo.br/j/cflo/a/FbGxGzjjRqW9YJ8dzjF7GTJ/abstract/?lang=pt
https://www.scielo.br/j/cflo/a/FbGxGzjjR...
; Tonetto et al., 2015TONETTO, T.D.S.; ARAUJO, M.M.; MUNIZ, M.F.B.; WALKER, C.; BERGHETTI, A.L.P. Storage and germination of seeds of Handroanthus heptaphyllus (Mart.) Mattos. Journal of Seed Science , v.37, p.40-46, 2015. https://doi.org/10.1590/2317-1545v37n1141116
https://doi.org/10.1590/2317-1545v37n114...
; Maciel et al., 2020MACIEL, C.G.; RIBEIRO, G.M.S.; LIMA, D.S.S.; OLIVEIRA, S.L.A.; PESSOA, A. C. Storage of ipê seeds in different packages and environments. Scientific Electronic Archives, v.13, n.6, p.36-39, 2020. https://doi.org/10.36560/13620201002
https://doi.org/10.36560/13620201002...
; Araujo et al., 2021ARAUJO, R.F.; ZONTA, J.B.; ARAUJO, E.F.; PINTO, C.M.F. Qualidades fisiológica e sanitária de sementes de pinhão-manso submetidas a tratamentos alternativos e químico, e ao armazenamento. Summa Phytopathologica, v.47, n.3, p.173-179, 2021. https://doi.org/10.1590/0100-5405/251465
https://doi.org/10.1590/0100-5405/251465...
). However, information on longevity, storage, or conservation is not available for H. spongiosus seeds. Moreover, there is no information on the quality of H. spongiosus seeds stored under room, low, and ultralow temperatures. Thus, this study aimed to evaluate the physiological quality of H. spongiosus seeds subjected to different storage times, packaging, and environments for their conservation.

MATERIAL AND METHODS

Seed collection

Handroanthus spongiosus (Rizzini) S. Grose (HUEFS-259093) seeds were obtained by harvesting mature fruits (brownish) at the seed dispersion stage from nine plants in Lagoa Grande, PE, Brazil (8°34’4’’S, 40°10’18’’W), in December 2017. The fruits were processed to remove branches, leaves, damaged seeds, and other impurities, generating the recently-harvested seed lot.

Seed storage

The experiment was conducted in a completely randomized experimental design, in a double factorial arrangement, with an additional treatment (5×6+1). The factors consisted of storage times (6, 9, 12, 18, and 24 months) and storage environmental conditions, considering the packaging (permeable or impermeable) and environments (room, cold chamber, freezer, and liquid nitrogen conditions).

Recently-harvested seeds were placed in polyethylene bags (PB) and cotton bags (CB) for room condition storage (RC), with mean temperature of 25 ± 4 °C and 45 ± 3% relative air humidity, or in cold chamber (CC), set to 10 ± 3 °C and 60 ± 4% relative air humidity. Seeds were placed in PB for the freezer storage (FS; -20 °C and 66% relative air humidity). The seeds stored in liquid nitrogen (LN) (-196 °C) were kept in polyethylene cryogenic tubes. Thus, six storage conditions were tested: polyethylene bag and room condition storage (PB-RC), cotton bag and room condition storage (CB-RC), polyethylene bag and cold chamber storage (PB-CC), cotton bag and cold chamber storage (CB-CC), polyethylene bag and freezer storage (FS), and cryotube and liquid nitrogen storage (LN).

The recently-harvested seeds and seeds stored for 6, 9, 12, 18, and 24 months were evaluated for physiological quality (seed water content, germination, and vigor). The seeds stored in FS and LN were subjected to slow thawing for 4 hours in a refrigerator (10 oC) and 1 hour at room temperature (Alencar et al., 2018ALENCAR, S.S.; FREIRE, J.T.; GOMES, R.A.; SILVA, J.J.; ARAUJO, M.N.; DANTAS, B.F. Descongelamento de sementes crioconservadas de Handroanthus spongiosus (Rizzini) S. Grose. Informativo Abrates, v.28, n.1, 2018. https://ainfo.cnptia.embrapa.br/digital/bitstream/item/197387/1/Barbara-2.pdf
https://ainfo.cnptia.embrapa.br/digital/...
), before evaluating the seed quality.

Seed physiological quality evaluations

The water contents of recently-harvested and stored seeds were obtained by the oven method at 105 ± 3 °C for 24 hours using two samples of 50 seeds (Brasil, 2013BRASIL, Ministério da Agricultura, Pecuária e Abastecimento. Instruções para análise de sementes de espécies florestais. Brasília: MAPA, 2013. 98 p. https://www.gov.br/agricultura/pt-br/assuntos/laboratorios/arquivos-publicacoes-laboratorio/florestal_documento_pdf-ilovepdf-compressed.pdf
https://www.gov.br/agricultura/pt-br/ass...
).

The physiological quality of recently-harvested and stored seeds were evaluated through germination tests carried out using four replications of 50 seeds for each treatment. The seeds were distributed between three Germitest paper sheets, moistened with distilled water at the proportion of 2.5-fold the dry paper weight, individually placed in polyethylene bags, and incubated in a BOD (biochemical oxygen demand) chamber at constant temperature of 25 ± 1 °C and photoperiod of 12 hours (adapted from Brasil, 2013BRASIL, Ministério da Agricultura, Pecuária e Abastecimento. Instruções para análise de sementes de espécies florestais. Brasília: MAPA, 2013. 98 p. https://www.gov.br/agricultura/pt-br/assuntos/laboratorios/arquivos-publicacoes-laboratorio/florestal_documento_pdf-ilovepdf-compressed.pdf
https://www.gov.br/agricultura/pt-br/ass...
) for 14 days. Then, the germination percentage (%G) and normal seedling percentage (%NS) were obtained, considering seeds with radicle lengths equal to or higher than 2.5 mm as germinated.

The seed vigor was evaluated by the performance of ten normal seedlings of each replication, considering the root and shoot lengths (cm) and root and shoot dry weights (mg), according to Nakagawa (2020NAKAGAWA, J. Testes de vigor baseados em desempenho de plântulas. In: KRZYZANOWSKI, F.C.; VIEIRA, R.D.; FRANÇA-NETO, J.B.; MARCOS-FILHO, J. (Eds.) Vigor de sementes: conceitos e testes. 2. ed. Londrina: ABRATES, p. 601, 2020. https://www.bdpa.cnptia.embrapa.br/consulta/busca?b=pc&biblioteca=vazio&busca=autoria:%22KRZYZANOWSKI,%20F.%20C.%22
https://www.bdpa.cnptia.embrapa.br/consu...
).

Statistical analysis of the data

The data were analyzed to verify the assumptions of analysis of variance through the normality of residues and homogeneity of variances by the Shapiro-Wilk (Shapiro and Wilk, 1965SHAPIRO, S.S.; WILK, M.B. An Analysis of variance test for normality. Biometrika, v.52, n.3, p. 591-611, 1965. https://www.jstor.org/stable/2333709?seq=1#metadata_info_tab_contents
https://www.jstor.org/stable/2333709?seq...
) and Levene (1960LEVENE, H. Robust tests for equality of variances. In: Contributions to probability and statistics: essays in honor of harold hotelling. Stanford University, 1960, p. 278-292.) tests, respectively, at 0.05 probability level. The data did not meet the assumptions of ANOVA and it was chosen not to use the angular transformation for the dependent variable; thus, they were fitted to Generalized Linear Models (GLM). The GLM were analyzed and the significant differences within each storage time, storage condition, and variables studied were analyzed through comparisons of means pairs by the post-hoc Tukey’s test at 5% significance. The means were fitted by the method of Šidák (1967ŠIDÀK, Z. Rectangular confidence region for the means of multivariate normal distributions. Journal of the American Statistical Association , v.62, n.318, p.626-633, 1967. https://doi.org/10.1080/01621459.1967.10482935
https://doi.org/10.1080/01621459.1967.10...
). The results found for the stored and recently-harvested seeds were compared by the Dunnett test (Dunnett, 1955DUNNETT, C.W. A multiple comparison procedure for comparing several treatments with a control. Journal of the American Statistical Association, v.50, n.272, p.1096-1121, 1955. https://www.tandfonline.com/doi/abs/10.1080/01621459.1955.10501294?journalCode=uasa20
https://www.tandfonline.com/doi/abs/10.1...
) at 0.05 probability level. The analyses were carried out using the R program (R Core Team, 2020R CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2020. Disponível em: Disponível em: https://www.R-project.org/ . Acesso em: 09 set. 2021.
https://www.R-project.org/...
).

RESULTS AND DISCUSSION

The data of germination percentage (%G) (p = 0.0814) and percentage of normal seedlings (%NS) (p = 0.6037) presented normality of residues by the Shapiro-Wilk test, but only %NS presented homogeneous variance (p = 0.0504) by the Levene test. The GLM showed that the interaction between the studied factors was significant for all variables, except for shoot length (p = 0.2473), for which only the effects of isolated factors were significant.

The recently-harvested seeds presented initial water content of 5.67%, which varied from 3.18% to 8.94% in the different storage conditions, mainly considering the packaging used (Table 1). Different seed structures presented different water levels; the water content obtained represents the mean of the whole seed (McDonald et al., 1994McDONALD, M. B.; SULLIVAN, J. L.; LAUER, M. J. The pathway of water uptake in maize seeds. Seed Science and Technology, v.22, n.1, p.79-90, 1994.; Bewley et al., 2013BEWLEY, J.D.; BRADFORD, K.J.; HILHORST, H.W.M.; NONOGAKI, H. Seeds: physiology of development, germination and dormancy. 3. ed. New York: Springer, 2013, 392p.). Water levels lower than 10% represent the water responsible for maintaining the structural integrity and property of macromolecules and are affected by the seed chemical composition and temperature (Vertucci, 1993VERTUCCI, C.W. Predicting the optimum storage conditions for seeds using thermodynamic principles. Journal of Seed Technology, v.17, n.2, p.41-53, 1993. ; Bewley et al., 2013BEWLEY, J.D.; BRADFORD, K.J.; HILHORST, H.W.M.; NONOGAKI, H. Seeds: physiology of development, germination and dormancy. 3. ed. New York: Springer, 2013, 392p.; Marcos-Filho, 2015MARCOS-FILHO, J. Fisiologia de sementes de plantas cultivadas. ABRATES, 2015, 660p.). Oscillations in these levels depend on the species and storage environment, which can affect the cell physiological status, including the conformation of proteins and organic compounds consisted of polymers of amino acids, which are water sorption sites (Bewley et al., 2013BEWLEY, J.D.; BRADFORD, K.J.; HILHORST, H.W.M.; NONOGAKI, H. Seeds: physiology of development, germination and dormancy. 3. ed. New York: Springer, 2013, 392p.; Marcos-Filho, 2015MARCOS-FILHO, J. Fisiologia de sementes de plantas cultivadas. ABRATES, 2015, 660p.).

Table 1
Water contents (%) in Handroanthus spongiosus seeds subjected to different storage conditions and times.

Seeds conserved under CB-RC presented a lower water content than the recently-harvested seed lot up to the 12nd month, followed by a significant increase of 3.27% in the 18th, and 0.65% in the 24th month of storage, different from the polyethylene bag packaging and room condition storage (PB-RC), which presented a 1.34% decrease in these two last times. In the cold chamber (CC) and freezer storage (FS) environments the seed water content decreased only in the 20th month; the cotton bag packaging and cold chamber storage (CB-CC) stood out with a 2.49% decrease. However, the liquid nitrogen storage (LN) kept the water content above that of the recently-harvested seed lot over the storage time (Table 1).

Regarding the physiological quality of seeds, the cryostorage in liquid nitrogen (LN) was the only condition that prevented the deterioration of H. spongiosus seeds up to 24 months, presenting similar results or superior results to those of recently-harvested seeds. However, the storage in permeable packaging and room temperature (CB-RC) presented the greatest seed deterioration after 24 months, with lower seed germination and seedling performance (Table 2). This is due the non-controlled conditions in the CB-RC, with seeds exposed to oscillations of temperature and relative air humidity, that can increase deterioration and loss of integrity of membranes, compromising RNA and protein syntheses, causing degradation of RNA and even disintegration of cell nuclei (Corbineau, 2012CORBINEAU, F. Markers of seed quality: from present to future. Seed Science Research, v.22, n.1, p. 61-68, 2012. https://doi.org/10.1017/S0960258511000419
https://doi.org/10.1017/S096025851100041...
; Jyoti and Malik, 2013JYOTI; MALIK, C. P. Seed deterioration: a review. International Journal of Life Sciences Biotechnology and Pharma Research, v.2, n.3, p.374-385, 2013.; Demidchik, 2015DEMIDCHIK, V. Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environmental and Experimental Botany, v.109, p.212-228, 2015. https://doi.org/10.1016/j.envexpbot.2014.06.021
https://doi.org/10.1016/j.envexpbot.2014...
; Capilheira et al., 2019CAPILHEIRA, A.F.; CAVALCANTE, J.A.; GADOTTI, G.I.; BEZERRA, B.R.; HORNKE, N.F.; VILLELA, F.A. Storage of soybean seeds: Packaging and modified atmosphere technology. Revista Brasileira de Engenharia Agrícola e Ambiental, v. 23, p. 876-882, 2019. https://doi.org/10.1590/1807-1929/agriambi.v23n11p876-882
https://doi.org/10.1590/1807-1929/agriam...
).

After 12 months of storage, decreases in %G and %NS of seeds stored in permeable packaging was higher than 50%. However, the packaging did not affect the quality of seeds stored in cold chamber (Table 2).

Table 2
Physiological quality of Handroanthus spongiosus seeds subjected to different storage conditions and times.

Seeds conserved under low temperatures in CC and FS presented germinations above 80% until the 18th month of storage, and did not differ from recently-harvested seeds. In addition, the %NS and performance (shoot and root lengths) of seedlings from seeds stored in these conditions were statistically equal to or better than those of recently-harvested seeds (Table 2).

The results found for root to shoot dry weight ratio, calculated using the dry biomass of seedlings, where similar those found for the other evaluated variables. The root to shoot dry weight ratio of seedlings from seeds stored in LN for up to 24 months were similar to that of recently-harvested seeds and, according to the seed deterioration, it was higher, denoting a higher investment in roots by the seedlings. The cold storage (CC and FS) presented intermediate responses and the CB-RC condition resulted in higher deterioration of seeds and higher root to shoot dry weight ratio than the other treatments (Table 2).

Seeds can be classified by their tolerance to desiccation and low-temperature storage into three groups, orthodox, intermediate, and recalcitrant (Walters, 2015WALTERS, C. Orthodoxy, recalcitrance and in-between: describing variation in seed storage characteristics using threshold responses to water loss. Planta, v.242, n.2, p.397-406, 2015. https://doi.org/10.1007/s00425-015-2312-6
https://doi.org/10.1007/s00425-015-2312-...
). Seeds of several species of the Handroanthus and Tabebuia genera are orthodox, they can disperse and be dried to water contents from 14.17% to 5.6% (Martins et al., 2009MARTINS, L.; LAGO, A.A.; SALES, W.R.M. Conservação de sementes de ipê-amarelo (Tabebuia chrysotricha (Mart. ex A. DC.) Standl.) em função do teor de água das sementes e da temperatura do armazenamento. Revista Brasileira de Sementes , v.31, n.2, p.86-95, 2009a. https://doi.org/10.1590/S0101-31222009000200010
https://doi.org/10.1590/S0101-3122200900...
a; Silva et al., 2011SILVA, D.G.; CARVALHO, M.L.M.; NERY, M.C.; OLIVEIRA, L.M.; CALDEIRA, C.M. Alterações fisiológicas e bioquímicas durante o armazenamento de sementes de Tabebuia serratifolia. Cerne, v.17, n.1, p.1-7, 2011. https://doi.org/10.1590/S0104-77602011000100001
https://doi.org/10.1590/S0104-7760201100...
; Guedes et al., 2012GUEDES, R.S.; ALVES, E.U.; MELO, P.A.F.R.; MOURA, S.S.S.; SILVA, R.S. Storage of Tabebuia caraiba (Mart.) Bureau seeds in different packaging and temperatures. Revista Brasileira de Sementes, v.34, n.3, p.433-440, 2012. https://www.scielo.br/j/rbs/a/XtSfmXP4DTwdYJ7GvHkLCQq/?format=pdf⟨=en
https://www.scielo.br/j/rbs/a/XtSfmXP4DT...
; Martins and Pinto, 2014MARTINS, C.C.; PINTO, M.A.D.S.C. Armazenamento de sementes de ipê-amarelo-do-brejo (Handroanthus umbellatus (Sond.) Mattos. Bignoniaceae). Ciência Florestal , v.24, n.3, p. 533-539, 2014. https://www.scielo.br/j/cflo/a/FbGxGzjjRqW9YJ8dzjF7GTJ/abstract/?lang=pt
https://www.scielo.br/j/cflo/a/FbGxGzjjR...
; Gonçalves et al., 2015GONÇALVES, L.H.D.N.; SANTOS, H.O.D.; VON PINHO, É.V.R.; ANDRADE, T.D.; VON PINHO, I.V.; PEREIRA, R.W. Physiological quality and expression of genes in seeds of Handroanthus serratifolius subjected to drying. Journal of Seed Science , v.37, p.102-110, 2015. https://doi.org/10.1590/2317-1545v37n2144303
https://doi.org/10.1590/2317-1545v37n214...
; Alencar et al., 2018ALENCAR, S.S.; FREIRE, J.T.; GOMES, R.A.; SILVA, J.J.; ARAUJO, M.N.; DANTAS, B.F. Descongelamento de sementes crioconservadas de Handroanthus spongiosus (Rizzini) S. Grose. Informativo Abrates, v.28, n.1, 2018. https://ainfo.cnptia.embrapa.br/digital/bitstream/item/197387/1/Barbara-2.pdf
https://ainfo.cnptia.embrapa.br/digital/...
), which allows their storage under low (-20 °C) and ultralow (-196 °C) temperatures, maintaining them viable for many years (Walters et al., 2013WALTERS, C.; BERJAK, P.; PAMMENTER, N.; KENNEDY, K.; RAVEN, P. Preservation of recalcitrant seeds. Science, v.339, n.6122, p.915-916, 2013. https://www.science.org/doi/abs/10.1126/science.1230935
https://www.science.org/doi/abs/10.1126/...
; Ballesteros et al., 2021BALLESTEROS, D.; FANEGA-SLEZIAK, N.; DAVIES, R.M. Cryopreservation of seeds and seed embryos in orthodox-, intermediate-, and recalcitrant-seeded species. In: WOLKERS, W.F.; OLDENHOF, H. (Ed.). Cryopreservation and Freeze-Drying Protocols. New York: Humana, 2021. p.663-682. https://link.springer.com/protocol/10.1007/978-1-0716-0783-1_36
https://link.springer.com/protocol/10.10...
).

Seed water content is one of the most important factors for seed storage in LN; high water contents in the cells can disrupt membranes during freezing (Panis et al., 2005PANIS, B.; PIETTE, B.; SWENNEN, R. Droplet vitrification of apical meristems: a cryopreservation protocol applicable to all Musaceae. Plant Science, v.168, n.1, p.45-55, 2005. https://doi.org/10.1016/j.plantsci.2004.07.022
https://doi.org/10.1016/j.plantsci.2004....
). H. spongiosus seeds with water content of 7.18% stored in liquid nitrogen for two years maintained a high physiological quality, which was a similar result to that of recently-harvested seeds (Table 2). This denotes an advantage of this species, since not all seeds tolerate temperatures below zero, as found for Handroanthus impetiginosus (Mart. ex DC) (= T. impetiginous) seeds with 4.2% water content stored in liquid nitrogen, whose physiological quality decrease after 360 days (Martins et al. 2009MARTINS, L.; LAGO, A.A.D.; ANDRADE, A.C.S.D.; SALES, W.R.M. Conservação de sementes de ipê-roxo (Tabebuia impetiginosa) (Mart. ex DC.) Standl. em nitrogênio líquido. Revista Brasileira de Sementes , v.31, n.2 p.71-76, 2009b. https://www.scielo.br/j/rbs/a/fcFzLtZhxd5Mz7pQF4kYVLk/?format=pdf⟨=pt
https://www.scielo.br/j/rbs/a/fcFzLtZhxd...
b).

Seeds of some species of the Caatinga biome tolerate liquid nitrogen storage for periods above 24 months without losing their physiological quality, as is the case of Amburana cearensis (Allemão) AC Sm. (Araujo et al., 2017ARAUJO, M.D.N.; FERRAZ, M.; AMÉRICO, F.K.A.; SILVA, F.F.S.; DANTAS, B.F.; CRUZ, C.R.P. Seed quality of Amburana cearensis (Allemão) AC Sm. (Fabaceae) is influenced by storage condition. Journal of Seed Science , v.39, n.4, p.401-409, 2017. https://doi.org/10.1590/2317-1545v39n4179328
https://doi.org/10.1590/2317-1545v39n417...
). This is probably because ultralow temperatures practically cease cell metabolism (Garcia et al., 2014GARCIA, C.; COELHO, C.M.M.; MARASCHIN, M.; OLIVEIRA, L.M. Conservação da viabilidade e vigor de sementes de Araucaria angustifolia (Bert.) O. Kuntze durante o armazenamento. Ciência Florestal, v.24, n.4, p.857-867, 2014. https://doi.org/10.5902/1980509816586
https://doi.org/10.5902/1980509816586...
). The storage of seeds in LN is an alternative for medium- and long-term conservation, since it is possible to maintain the seed viability and vigor for several years under low temperatures (-196 °C), although this process has a high cost (Kaviani, 2011KAVIANI, B. Conservation of plant genetic resources by cryopreservation. Australian Journal of Crop Science, v. 5, n. 6, p. 778-800, 2011. http://www.cropj.com/kaviani_5_6_2011_778_800.pdf
http://www.cropj.com/kaviani_5_6_2011_77...
; Walters et al., 2013WALTERS, C.; BERJAK, P.; PAMMENTER, N.; KENNEDY, K.; RAVEN, P. Preservation of recalcitrant seeds. Science, v.339, n.6122, p.915-916, 2013. https://www.science.org/doi/abs/10.1126/science.1230935
https://www.science.org/doi/abs/10.1126/...
).

Despite the water content of H. spongiosus seeds conserved in LN increase after six months, no loss in seed or seedling quality was found. This increase in seed water content after the storage period in low temperatures (CC, FS, and LN) was caused by the water vapor condensation process that occurs between the seed contact surface (lower temperature) and the surrounding air at thawing (higher temperature) when the seeds were removed from the cold storage (Delouche, 1968DELOUCHE, J.C. Precepts for seed storage. In: Proceedings of the Short Course for Seedsmen, 1968, p.85-119. https://scholarsjunction.msstate.edu/seedsmen-short-course/187
https://scholarsjunction.msstate.edu/see...
). These seeds are hygroscopic, they absorb or lose water to the environment until a balance is established between the seed water content and relative air humidity (Delouche, 1968; Oliveira et al., 2014OLIVEIRA, D.E.C.; RESENDE, O.; CAMPOS, R.C.; DONADON, J.R. Obtenção e modelagem das isotermas de dessorção e do calor isostérico para sementes de arroz em casca. Científica, v.42, n.3, p.203-210, 2014. http://dx.doi.org/10.15361/1984-5529.2014v42n3p203-210
http://dx.doi.org/10.15361/1984-5529.201...
); the period between the thawing and weighing of seeds was enough for them to absorb the water.

A test for measuring water content of cryo-conserved seeds was carried out using two replications of 50 seeds, which were directly placed in the oven after the LN or subjected to a thawing process. The water contents were similar to those obtained during the storage: 7.15% for seeds directly placed in the oven and 7.24% for those subjected to a thawing process, confirming that they absorb water soon after their removal from the LN.

Despite some species of the Caatinga biome conserve their seed physiological quality for more than 12 months under room conditions (>25 °C) (Lúcio et al., 2016LÚCIO, A.A.; ARAUJO, M.N.; SILVA, F.F.S.; DANTAS, B.F. Effect of storage in different environments and packages on germination of Amburana cearensis (Allemao) A. C. Sm. seeds. International Journal of Environment, Agriculture and Biotechnology, v.1, n.4, p. 1037-1040, 2016. http://dx.doi.org/10.22161/ijeab/1.4.57
http://dx.doi.org/10.22161/ijeab/1.4.57...
; Gomes et al., 2018GOMES, S.E.V.; SANTOS, K.C.; OLIVEIRA, G.M.; ARAÚJO, M.N.; DANTAS, B.F. Sementes de Myracrodruon urundeuva podem ser armazenadas por até dois anos em ambiente seco. Informativo Abrates , v.28, n.1, p.102-106, 2018. https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1109071/1/Barbara.pdf
https://www.alice.cnptia.embrapa.br/alic...
; Ribeiro et al., 2018RIBEIRO, R.C.; GOMES, S.E. V.; DANTAS, B.F. Physiological quality of Erythrina velutina Willd. (FABACEAE) seeds under different storage conditions. Scientia Forestalis, v.46, n.120, p. 562-570, 2018. https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1104185/1/bARBARA.pdf
https://www.alice.cnptia.embrapa.br/alic...
), in general, storing under temperatures above 20 °C and relative air humidity higher than 70% are not recommended, as they compromise the seed physiological quality and promote the action of microorganisms and insects (Carvalho and Nakagawa, 2012CARVALHO, N.M.; NAKAGAWA, J. Sementes: ciência, tecnologia e produção. 5.ed. Jaboticabal: FUNEP, 2012. 590p.). The combination of high temperatures with great water contents (usually above 12%) accelerates cell respiration, which leads to the consumption of the reserve material, oxidation of cell membranes, and degeneration of biological systems. Thus, the seeds rapidly lose their vigor and viability (Smaniotto et al., 2014SMANIOTTO, T.A.D.S.; RESENDE, O.; MARÇAL, K.A.; OLIVEIRA, D.E.; SIMON, G.A. Qualidade fisiológica das sementes de soja armazenadas em diferentes condições. Revista Brasileira de Engenharia Agrícola e Ambiental , v.18, n.4, p.446-453, 2014. https://doi.org/10.1590/S1415-43662014000400013
https://doi.org/10.1590/S1415-4366201400...
).

The storage of seeds under room conditions (RC) presented the lowest seedling sizes, regardless of the type of packaging, denoting that this environment favored the maintenance of their respiratory metabolism and consumption of reserves, affecting the vigor and formation of seedlings (Dias et al., 2016DIAS, D.C.F.S.; OLIVEIRA, G.L.; VALLORY, G.G.; SILVA, L.J.D.; SOARES, M.M. Physiological changes in Jatropha curcas L. seeds during storage. Journal of Seed Science , v.38, n.1, p.41-49, 2016. https://doi.org/10.1590/2317-1545v38n1155449
https://doi.org/10.1590/2317-1545v38n115...
; Araujo et al., 2021ARAUJO, R.F.; ZONTA, J.B.; ARAUJO, E.F.; PINTO, C.M.F. Qualidades fisiológica e sanitária de sementes de pinhão-manso submetidas a tratamentos alternativos e químico, e ao armazenamento. Summa Phytopathologica, v.47, n.3, p.173-179, 2021. https://doi.org/10.1590/0100-5405/251465
https://doi.org/10.1590/0100-5405/251465...
). This combination of factors involving continuous and not controlled vapor exchange between the medium and the seed with high temperatures can increase the respiratory rate and affect the development of structures and biomass allocation, even when the water contents do not oscillate. Similar results were found for H. chrysotrichus seeds, which could not be stored at room temperature for periods longer than 30 days, whereas H. impetiginosus and Handroanthus serratifolius (Vahl) S.Grose seeds did not germinate after four and nine months of storage, respectively (Silva et al., 2011SILVA, D.G.; CARVALHO, M.L.M.; NERY, M.C.; OLIVEIRA, L.M.; CALDEIRA, C.M. Alterações fisiológicas e bioquímicas durante o armazenamento de sementes de Tabebuia serratifolia. Cerne, v.17, n.1, p.1-7, 2011. https://doi.org/10.1590/S0104-77602011000100001
https://doi.org/10.1590/S0104-7760201100...
; Maciel et al., 2020MACIEL, C.G.; RIBEIRO, G.M.S.; LIMA, D.S.S.; OLIVEIRA, S.L.A.; PESSOA, A. C. Storage of ipê seeds in different packages and environments. Scientific Electronic Archives, v.13, n.6, p.36-39, 2020. https://doi.org/10.36560/13620201002
https://doi.org/10.36560/13620201002...
; Araujo et al., 2021ARAUJO, M.E.S.; NEGREIROS, M.L.; SHIBATA, M. Secagem e armazenamento de sementes de Handroanthus impetiginosus (Mart. ex DC.) Mattos (Bignoniaceae). Revista de Ciências Agrárias Amazonian Journal of Agricultural and Environmental Sciences, v.64, 2021. http://200.129.150.26/index.php/ajaes/article/view/3420
http://200.129.150.26/index.php/ajaes/ar...
).

Handroanthus heptaphyllus (Vell.) Mattos and H. impetiginosus seeds presented germination above 70% after 6 months of storage in CC and refrigerator, respectively (Maciel et al., 2020MACIEL, C.G.; RIBEIRO, G.M.S.; LIMA, D.S.S.; OLIVEIRA, S.L.A.; PESSOA, A. C. Storage of ipê seeds in different packages and environments. Scientific Electronic Archives, v.13, n.6, p.36-39, 2020. https://doi.org/10.36560/13620201002
https://doi.org/10.36560/13620201002...
; Araujo et al., 2021ARAUJO, R.F.; ZONTA, J.B.; ARAUJO, E.F.; PINTO, C.M.F. Qualidades fisiológica e sanitária de sementes de pinhão-manso submetidas a tratamentos alternativos e químico, e ao armazenamento. Summa Phytopathologica, v.47, n.3, p.173-179, 2021. https://doi.org/10.1590/0100-5405/251465
https://doi.org/10.1590/0100-5405/251465...
), and Handroanthus chrysotrichus (Mart. ex dc.) stored in FS presented 54% germination after 10 months (Tonetto et al., 2015TONETTO, T.D.S.; ARAUJO, M.M.; MUNIZ, M.F.B.; WALKER, C.; BERGHETTI, A.L.P. Storage and germination of seeds of Handroanthus heptaphyllus (Mart.) Mattos. Journal of Seed Science , v.37, p.40-46, 2015. https://doi.org/10.1590/2317-1545v37n1141116
https://doi.org/10.1590/2317-1545v37n114...
). H. spongiosus seeds presented germination of approximately 90% when stored in CC and FS after 12 months (Table 2), higher than those obtained for other species of the same genus that present very similar morphological characteristics. These environments (CC and FS) can be used by seedling and plant growers as viable strategies for ex situ conservation of seeds, since they are more accessible.

The root system can be significantly compromised depending on the storage conditions and time, with negative consequences to seed quality and seedling vigor (Table 2). It was reported by Mucha et al. (2015MUCHA, J.; SZYMAŃSKA, A.K.; ZADWORNY, M.; TYLKOWSKI, T.; MICHALAK, M.; SUSZKA, J. Effect of seed storage temperature on fine root development and mycorrhizal colonization of young Populus nigra L. seedlings. Annals of Forest Science, v.72, p.539-547, 2015. https://doi.org/10.1007/s13595-015-0470-0
https://doi.org/10.1007/s13595-015-0470-...
), who found that the seed storage temperature affected the root anatomy of Populus nigra L. plants and reported that the storage at high temperatures decreased the proportion of roots with absorptive function (with primary development). Seedlings with higher root systems can explore a greater soil volume and have greater potential to absorb water and promote nutrient cycling and absorption (Finér et al., 2007FINÉR, L.; HELMISAARI, H.S.; LÕHMUS, K.; MAJDI, H.; BRUNNER, I.; BØRJA, I.; ELDHUSET, T.; GODBOLD, D.; GREBENC, T.; KONÔPKA, B.; KRAIGHER, H.M.R.; MÖTTÖNEN, M.; OHASHI, J.; OLEKSYN, I.; OSTONEN, V.; URI, E.; VANGUELOVA, E. Variation in fine root biomass of three European tree species: Beech (Fagus sylvatica L.), Norway spruce (Picea abies L. Karst.), and Scots pine (Pinus sylvestris L.). Plant Biosystems, v.141, n.3, p.394-405, 2007. https://doi.org/10.1080/11263500701625897
https://doi.org/10.1080/1126350070162589...
; Betegón-Putze et al., 2019BETEGÓN-PUTZE, I.; GONZÁLEZ, A.; SEVILLANO, X.; BLASCO-ESCÁMEZ, D.; CAÑO-DELGADO, A.I. My ROOT: a method and software for the semiautomatic measurement of primary root length in Arabidopsis seedlings. The Plant Journal, v.98, n.6, p.1145-1156, 2019. https://doi.org/10.1111/tpj.14297
https://doi.org/10.1111/tpj.14297...
; Thorup-Kristensen et al., 2020THORUP-KRISTENSEN, K.; HALBERG, N.; NICOLAISEN, M.; OLESEN, J.E.; CREWS, T.E.; HINSINGER, P.; KIRKEGAARD, J.; PIERRET, A.; DRESBØLL, D.B. Digging deeper for agricultural resources, the value of deep rooting. Trends in Plant Science , v.25, n.4, p.406-417, 2020. https://doi.org/10.1016/j.tplants.2019.12.007
https://doi.org/10.1016/j.tplants.2019.1...
).

The H. spongiosus seedlings presented higher dry matter allocation in the shoots during the post-seeding development. This can be attributed to higher investment of seedlings in thin roots at this initial stage of development as a strategy to explore a greater volume of the substrate and maximize water absorption for their development (Gransee and Führs, 2013GRANSEE, A.; FÜHRS, H. Magnesium mobility in soils as a challenge for soil and plant analysis, magnesium fertilization and root uptake under adverse growth conditions. Plant and Soil, v.368, n.1, p.5-21, 2013. https://doi.org/10.1007/s11104-012-1567-y
https://doi.org/10.1007/s11104-012-1567-...
; Yuan et al., 2016YUAN, H.M.; BLACKWELL, M.; MCGRATH, S.; GEORGE, T.S.; GRANGER, S.H.; HAWKINS, J.M.B.; DUNHAM, S.; SHEN, J.B. Morphological responses of wheat (Triticum aestivum L.) roots to phosphorus supply in two contrasting soils. The Journal of Agricultural Science, v.154, n.1, p.98-108, 2016. https://doi.org/10.1017/S0021859615000702
https://doi.org/10.1017/S002185961500070...
). However, these thinner roots little contribute to the root to shoot dry weight ratio. Species adapted to seasonally dry environments present a genetic trend of allocating greater biomass in the root system as a form to reach deeper soil waters faster and efficiently while using the variable water from rainfall events (Markesteijn and Poorter, 2009MARKESTEIJN, L.; POORTER, L. Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought-and shade-tolerance. Journal of Ecology, v.97, n.2, p.311-325, 2009. https://doi.org/10.1111/j.1365-2745.2008.01466.x
https://doi.org/10.1111/j.1365-2745.2008...
; Tomlinson et al., 2012TOMLINSON, K.W.; STERCK, F.J.; BONGERS, F.; SILVA, D.A.S.; BARBOSA, E.R.M.; WARD, D.; BAKKER, F.T.; KAAUWEN, M.V.; PRINS, H.H.T.; BIE, S.; LANGEVELDE, F.V. Biomass partitioning and root morphology of savanna trees across a water gradient. Journal of Ecology , v. 100, n.5, p.1113-1121, 2012. https://doi.org/10.1111/j.1365-2745.2012.01975.x
https://doi.org/10.1111/j.1365-2745.2012...
; Qi et al., 2019QI, Y.; WEI, W.; CHEN, C.; CHEN, L. Plant root-shoot biomass allocation over diverse biomes: A global synthesis. Global Ecology and Conservation, v.18, p.e00606, 2019. https://doi.org/10.1016/j.gecco.2019.e00606
https://doi.org/10.1016/j.gecco.2019.e00...
), but it was not found for H. spongiosus at the seedling stage.

Seeds with low water content (lower than 10%) placed in impermeable packaging and stored at low temperatures (< 10 oC) presented higher longevity, as also found for Tabebuia aurea (Silva Manso) Benth & Hook ex S. Moore, Tabebuia caraiba (Mart.) Bureau, H. chrysotrichus (= T. chrysotricha), H. impetiginosus (= T. impetiginous), and Handroanthus umbellatus (Sond.) Mattos (Martins et al., 2009MARTINS, L.; LAGO, A.A.; SALES, W.R.M. Conservação de sementes de ipê-amarelo (Tabebuia chrysotricha (Mart. ex A. DC.) Standl.) em função do teor de água das sementes e da temperatura do armazenamento. Revista Brasileira de Sementes , v.31, n.2, p.86-95, 2009a. https://doi.org/10.1590/S0101-31222009000200010
https://doi.org/10.1590/S0101-3122200900...
a; Guedes et al., 2012GUEDES, R.S.; ALVES, E.U.; MELO, P.A.F.R.; MOURA, S.S.S.; SILVA, R.S. Storage of Tabebuia caraiba (Mart.) Bureau seeds in different packaging and temperatures. Revista Brasileira de Sementes, v.34, n.3, p.433-440, 2012. https://www.scielo.br/j/rbs/a/XtSfmXP4DTwdYJ7GvHkLCQq/?format=pdf⟨=en
https://www.scielo.br/j/rbs/a/XtSfmXP4DT...
; Martins and Pinto, 2014MARTINS, C.C.; PINTO, M.A.D.S.C. Armazenamento de sementes de ipê-amarelo-do-brejo (Handroanthus umbellatus (Sond.) Mattos. Bignoniaceae). Ciência Florestal , v.24, n.3, p. 533-539, 2014. https://www.scielo.br/j/cflo/a/FbGxGzjjRqW9YJ8dzjF7GTJ/abstract/?lang=pt
https://www.scielo.br/j/cflo/a/FbGxGzjjR...
; Neves et al., 2014NEVES, G.; SERIGATTO, E.M.; DALCHIAVON, F.C.; SILVA, C.A. Viabilidade e longevidade de sementes de Tabebuia aurea benth. & hook. submetidas a diferentes métodos de armazenamento. Bioscience Journal, v.30, n.3. p.737-742, 2014. https://repositorio.unesp.br/bitstream/handle/11449/111579/WOS000333425100015.pdf?sequence=1&isAllowed=y
https://repositorio.unesp.br/bitstream/h...
; Araujo et al., 2021ARAUJO, R.F.; ZONTA, J.B.; ARAUJO, E.F.; PINTO, C.M.F. Qualidades fisiológica e sanitária de sementes de pinhão-manso submetidas a tratamentos alternativos e químico, e ao armazenamento. Summa Phytopathologica, v.47, n.3, p.173-179, 2021. https://doi.org/10.1590/0100-5405/251465
https://doi.org/10.1590/0100-5405/251465...
). In these conditions, there is a resistance of the packaging to water vapor exchanges between the seeds and the medium, and a low promotion of development of microorganisms that produce heat through their many metabolic reactions, thus avoiding energetic losses (Cardoso et al., 2012CARDOSO, R.B.; BINOTTI, F.F.S.; CARDOSO, E.D. Potencial fisiológico de sementes de crambe em função de embalagens e armazenamento. Pesquisa Agropecuária Tropical, v.42, n.3, p.272-278, 2012. https://doi.org/10.1590/S1983-40632012000300006
https://doi.org/10.1590/S1983-4063201200...
; Lopes and Lima, 2015LOPES, N.F.; LIMA, M.G.S. Fisiologia da produção. Viçosa-MG: Editora UFV, 492 p. 2015.).

The conservation of physiological quality of H. spongiosus seeds during the storage is connected to the conditions used; environments with low temperatures can conserve seed viability and vigor for longer periods. This information could be used to subsidize the development of appropriate strategies for ex situ seed conservation for H. spongiosus and other related species from different origins.

CONCLUSION

Storing Handroanthus spongiosus seeds under room conditions is not recommended, since it causes losses in seed germination and vigor. The most adequate conditions for their conservation are provided by cold chamber, freezer, and liquid nitrogen environments. The use of impermeable packaging and low temperatures is the most indicated method for the maintenance of the physiological quality of H. spongiosus seeds.

ACKNOWLEDGEMENTS

The authors thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE) for granting scholarships; and the Embrapa Semiárido for supporting the research project that generated this work.

REFERENCES

  • ABBADE, L.C.; TAKAKI, M. Biochemical and physiological changes of Tabebuia roseoalba (Ridl.) Sandwith (Bignoniaceae) seeds under storage. Journal of Seed Science, v.36, p. 100-107, 2014. https://www.scielo.br/j/jss/a/9RwhTDnCrXbRPg7ZmXDyHYd/?lang=en
    » https://www.scielo.br/j/jss/a/9RwhTDnCrXbRPg7ZmXDyHYd/?lang=en
  • ALENCAR, S.S.; FREIRE, J.T.; GOMES, R.A.; SILVA, J.J.; ARAUJO, M.N.; DANTAS, B.F. Descongelamento de sementes crioconservadas de Handroanthus spongiosus (Rizzini) S. Grose. Informativo Abrates, v.28, n.1, 2018. https://ainfo.cnptia.embrapa.br/digital/bitstream/item/197387/1/Barbara-2.pdf
    » https://ainfo.cnptia.embrapa.br/digital/bitstream/item/197387/1/Barbara-2.pdf
  • ARAUJO, M.D.N.; FERRAZ, M.; AMÉRICO, F.K.A.; SILVA, F.F.S.; DANTAS, B.F.; CRUZ, C.R.P. Seed quality of Amburana cearensis (Allemão) AC Sm. (Fabaceae) is influenced by storage condition. Journal of Seed Science , v.39, n.4, p.401-409, 2017. https://doi.org/10.1590/2317-1545v39n4179328
    » https://doi.org/10.1590/2317-1545v39n4179328
  • ARAUJO, M.E.S.; NEGREIROS, M.L.; SHIBATA, M. Secagem e armazenamento de sementes de Handroanthus impetiginosus (Mart. ex DC.) Mattos (Bignoniaceae). Revista de Ciências Agrárias Amazonian Journal of Agricultural and Environmental Sciences, v.64, 2021. http://200.129.150.26/index.php/ajaes/article/view/3420
    » http://200.129.150.26/index.php/ajaes/article/view/3420
  • ARAUJO, R.F.; ZONTA, J.B.; ARAUJO, E.F.; PINTO, C.M.F. Qualidades fisiológica e sanitária de sementes de pinhão-manso submetidas a tratamentos alternativos e químico, e ao armazenamento. Summa Phytopathologica, v.47, n.3, p.173-179, 2021. https://doi.org/10.1590/0100-5405/251465
    » https://doi.org/10.1590/0100-5405/251465
  • BALLESTEROS, D.; FANEGA-SLEZIAK, N.; DAVIES, R.M. Cryopreservation of seeds and seed embryos in orthodox-, intermediate-, and recalcitrant-seeded species In: WOLKERS, W.F.; OLDENHOF, H. (Ed.). Cryopreservation and Freeze-Drying Protocols. New York: Humana, 2021. p.663-682. https://link.springer.com/protocol/10.1007/978-1-0716-0783-1_36
    » https://link.springer.com/protocol/10.1007/978-1-0716-0783-1_36
  • BETEGÓN-PUTZE, I.; GONZÁLEZ, A.; SEVILLANO, X.; BLASCO-ESCÁMEZ, D.; CAÑO-DELGADO, A.I. My ROOT: a method and software for the semiautomatic measurement of primary root length in Arabidopsis seedlings. The Plant Journal, v.98, n.6, p.1145-1156, 2019. https://doi.org/10.1111/tpj.14297
    » https://doi.org/10.1111/tpj.14297
  • BEWLEY, J.D.; BRADFORD, K.J.; HILHORST, H.W.M.; NONOGAKI, H. Seeds: physiology of development, germination and dormancy 3. ed. New York: Springer, 2013, 392p.
  • BRASIL, Ministério da Agricultura, Pecuária e Abastecimento. Instruções para análise de sementes de espécies florestais. Brasília: MAPA, 2013. 98 p. https://www.gov.br/agricultura/pt-br/assuntos/laboratorios/arquivos-publicacoes-laboratorio/florestal_documento_pdf-ilovepdf-compressed.pdf
    » https://www.gov.br/agricultura/pt-br/assuntos/laboratorios/arquivos-publicacoes-laboratorio/florestal_documento_pdf-ilovepdf-compressed.pdf
  • CABRAL, E.L.; BARBOSA, D.C.A.; SIMABUKURO, E.A. Armazenamento e germinação de sementes de Tabebuia aurea (Manso) Benth. & Hook. f. ex. S. Moore. Acta Botanica Brasilica, v.17, n.4, p.609-617, 2003. https://doi.org/10.1590/S0102-33062003000400013
    » https://doi.org/10.1590/S0102-33062003000400013
  • CAPILHEIRA, A.F.; CAVALCANTE, J.A.; GADOTTI, G.I.; BEZERRA, B.R.; HORNKE, N.F.; VILLELA, F.A. Storage of soybean seeds: Packaging and modified atmosphere technology. Revista Brasileira de Engenharia Agrícola e Ambiental, v. 23, p. 876-882, 2019. https://doi.org/10.1590/1807-1929/agriambi.v23n11p876-882
    » https://doi.org/10.1590/1807-1929/agriambi.v23n11p876-882
  • CARDOSO, R.B.; BINOTTI, F.F.S.; CARDOSO, E.D. Potencial fisiológico de sementes de crambe em função de embalagens e armazenamento. Pesquisa Agropecuária Tropical, v.42, n.3, p.272-278, 2012. https://doi.org/10.1590/S1983-40632012000300006
    » https://doi.org/10.1590/S1983-40632012000300006
  • CARVALHO, N.M.; NAKAGAWA, J. Sementes: ciência, tecnologia e produção 5.ed. Jaboticabal: FUNEP, 2012. 590p.
  • CORBINEAU, F. Markers of seed quality: from present to future. Seed Science Research, v.22, n.1, p. 61-68, 2012. https://doi.org/10.1017/S0960258511000419
    » https://doi.org/10.1017/S0960258511000419
  • DELOUCHE, J.C. Precepts for seed storage. In: Proceedings of the Short Course for Seedsmen, 1968, p.85-119. https://scholarsjunction.msstate.edu/seedsmen-short-course/187
    » https://scholarsjunction.msstate.edu/seedsmen-short-course/187
  • DEMIDCHIK, V. Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environmental and Experimental Botany, v.109, p.212-228, 2015. https://doi.org/10.1016/j.envexpbot.2014.06.021
    » https://doi.org/10.1016/j.envexpbot.2014.06.021
  • DIAS, D.C.F.S.; OLIVEIRA, G.L.; VALLORY, G.G.; SILVA, L.J.D.; SOARES, M.M. Physiological changes in Jatropha curcas L. seeds during storage. Journal of Seed Science , v.38, n.1, p.41-49, 2016. https://doi.org/10.1590/2317-1545v38n1155449
    » https://doi.org/10.1590/2317-1545v38n1155449
  • DUNNETT, C.W. A multiple comparison procedure for comparing several treatments with a control. Journal of the American Statistical Association, v.50, n.272, p.1096-1121, 1955. https://www.tandfonline.com/doi/abs/10.1080/01621459.1955.10501294?journalCode=uasa20
    » https://www.tandfonline.com/doi/abs/10.1080/01621459.1955.10501294?journalCode=uasa20
  • FERREIRA, C.D.; SOUTO, P.C.; LUCENA, D.S.; SALES, S.C.V.; SOUTO, J.S. Florística do banco de sementes no solo em diferentes estágios de regeneração natural de Caatinga. Revista Brasileira de Ciências Agrárias, v.9, n.4, p.562-569, 2014. https://www.redalyc.org/pdf/1190/119032902015.pdf
    » https://www.redalyc.org/pdf/1190/119032902015.pdf
  • FINÉR, L.; HELMISAARI, H.S.; LÕHMUS, K.; MAJDI, H.; BRUNNER, I.; BØRJA, I.; ELDHUSET, T.; GODBOLD, D.; GREBENC, T.; KONÔPKA, B.; KRAIGHER, H.M.R.; MÖTTÖNEN, M.; OHASHI, J.; OLEKSYN, I.; OSTONEN, V.; URI, E.; VANGUELOVA, E. Variation in fine root biomass of three European tree species: Beech (Fagus sylvatica L.), Norway spruce (Picea abies L. Karst.), and Scots pine (Pinus sylvestris L.). Plant Biosystems, v.141, n.3, p.394-405, 2007. https://doi.org/10.1080/11263500701625897
    » https://doi.org/10.1080/11263500701625897
  • GARCIA, C.; COELHO, C.M.M.; MARASCHIN, M.; OLIVEIRA, L.M. Conservação da viabilidade e vigor de sementes de Araucaria angustifolia (Bert.) O. Kuntze durante o armazenamento. Ciência Florestal, v.24, n.4, p.857-867, 2014. https://doi.org/10.5902/1980509816586
    » https://doi.org/10.5902/1980509816586
  • GOMES, S.E.V.; SANTOS, K.C.; OLIVEIRA, G.M.; ARAÚJO, M.N.; DANTAS, B.F. Sementes de Myracrodruon urundeuva podem ser armazenadas por até dois anos em ambiente seco. Informativo Abrates , v.28, n.1, p.102-106, 2018. https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1109071/1/Barbara.pdf
    » https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1109071/1/Barbara.pdf
  • GONÇALVES, L.H.D.N.; SANTOS, H.O.D.; VON PINHO, É.V.R.; ANDRADE, T.D.; VON PINHO, I.V.; PEREIRA, R.W. Physiological quality and expression of genes in seeds of Handroanthus serratifolius subjected to drying. Journal of Seed Science , v.37, p.102-110, 2015. https://doi.org/10.1590/2317-1545v37n2144303
    » https://doi.org/10.1590/2317-1545v37n2144303
  • GRANSEE, A.; FÜHRS, H. Magnesium mobility in soils as a challenge for soil and plant analysis, magnesium fertilization and root uptake under adverse growth conditions. Plant and Soil, v.368, n.1, p.5-21, 2013. https://doi.org/10.1007/s11104-012-1567-y
    » https://doi.org/10.1007/s11104-012-1567-y
  • GUEDES, R.S.; ALVES, E.U.; MELO, P.A.F.R.; MOURA, S.S.S.; SILVA, R.S. Storage of Tabebuia caraiba (Mart.) Bureau seeds in different packaging and temperatures. Revista Brasileira de Sementes, v.34, n.3, p.433-440, 2012. https://www.scielo.br/j/rbs/a/XtSfmXP4DTwdYJ7GvHkLCQq/?format=pdf⟨=en
    » https://www.scielo.br/j/rbs/a/XtSfmXP4DTwdYJ7GvHkLCQq/?format=pdf⟨=en
  • JYOTI; MALIK, C. P. Seed deterioration: a review. International Journal of Life Sciences Biotechnology and Pharma Research, v.2, n.3, p.374-385, 2013.
  • KAVIANI, B. Conservation of plant genetic resources by cryopreservation. Australian Journal of Crop Science, v. 5, n. 6, p. 778-800, 2011. http://www.cropj.com/kaviani_5_6_2011_778_800.pdf
    » http://www.cropj.com/kaviani_5_6_2011_778_800.pdf
  • LEVENE, H. Robust tests for equality of variances. In: Contributions to probability and statistics: essays in honor of harold hotelling. Stanford University, 1960, p. 278-292.
  • LOHMANN, L.G.; SFAIR, J.C.; MONTEIRO, N.P.; SANTOS-FILHO, L.A.F. Bignoniaceae. In: MARTINELLI, G.; MORAES, M.A. (Eds.). Livro vermelho da flora do Brasil. 1. ed. Rio de Janeiro: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro 2013. p. 303-314.
  • LOHMANN, L.G. Handroanthus in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. 2020. Disponível em: Disponível em: http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB117471 Acesso em: 05 dez. 2021.
    » http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB117471
  • LOPES, N.F.; LIMA, M.G.S. Fisiologia da produção. Viçosa-MG: Editora UFV, 492 p. 2015.
  • LÚCIO, A.A.; ARAUJO, M.N.; SILVA, F.F.S.; DANTAS, B.F. Effect of storage in different environments and packages on germination of Amburana cearensis (Allemao) A. C. Sm. seeds. International Journal of Environment, Agriculture and Biotechnology, v.1, n.4, p. 1037-1040, 2016. http://dx.doi.org/10.22161/ijeab/1.4.57
    » http://dx.doi.org/10.22161/ijeab/1.4.57
  • MACIEL, C.G.; RIBEIRO, G.M.S.; LIMA, D.S.S.; OLIVEIRA, S.L.A.; PESSOA, A. C. Storage of ipê seeds in different packages and environments. Scientific Electronic Archives, v.13, n.6, p.36-39, 2020. https://doi.org/10.36560/13620201002
    » https://doi.org/10.36560/13620201002
  • MARCOS-FILHO, J. Fisiologia de sementes de plantas cultivadas. ABRATES, 2015, 660p.
  • MARKESTEIJN, L.; POORTER, L. Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought-and shade-tolerance. Journal of Ecology, v.97, n.2, p.311-325, 2009. https://doi.org/10.1111/j.1365-2745.2008.01466.x
    » https://doi.org/10.1111/j.1365-2745.2008.01466.x
  • MARTINS, C.C.; PINTO, M.A.D.S.C. Armazenamento de sementes de ipê-amarelo-do-brejo (Handroanthus umbellatus (Sond.) Mattos. Bignoniaceae). Ciência Florestal , v.24, n.3, p. 533-539, 2014. https://www.scielo.br/j/cflo/a/FbGxGzjjRqW9YJ8dzjF7GTJ/abstract/?lang=pt
    » https://www.scielo.br/j/cflo/a/FbGxGzjjRqW9YJ8dzjF7GTJ/abstract/?lang=pt
  • MARTINS, L.; LAGO, A.A.; SALES, W.R.M. Conservação de sementes de ipê-amarelo (Tabebuia chrysotricha (Mart. ex A. DC.) Standl.) em função do teor de água das sementes e da temperatura do armazenamento. Revista Brasileira de Sementes , v.31, n.2, p.86-95, 2009a. https://doi.org/10.1590/S0101-31222009000200010
    » https://doi.org/10.1590/S0101-31222009000200010
  • MARTINS, L.; LAGO, A.A.D.; ANDRADE, A.C.S.D.; SALES, W.R.M. Conservação de sementes de ipê-roxo (Tabebuia impetiginosa) (Mart. ex DC.) Standl. em nitrogênio líquido. Revista Brasileira de Sementes , v.31, n.2 p.71-76, 2009b. https://www.scielo.br/j/rbs/a/fcFzLtZhxd5Mz7pQF4kYVLk/?format=pdf⟨=pt
    » https://www.scielo.br/j/rbs/a/fcFzLtZhxd5Mz7pQF4kYVLk/?format=pdf⟨=pt
  • McDONALD, M. B.; SULLIVAN, J. L.; LAUER, M. J. The pathway of water uptake in maize seeds. Seed Science and Technology, v.22, n.1, p.79-90, 1994.
  • MUCHA, J.; SZYMAŃSKA, A.K.; ZADWORNY, M.; TYLKOWSKI, T.; MICHALAK, M.; SUSZKA, J. Effect of seed storage temperature on fine root development and mycorrhizal colonization of young Populus nigra L. seedlings. Annals of Forest Science, v.72, p.539-547, 2015. https://doi.org/10.1007/s13595-015-0470-0
    » https://doi.org/10.1007/s13595-015-0470-0
  • NAKAGAWA, J. Testes de vigor baseados em desempenho de plântulas. In: KRZYZANOWSKI, F.C.; VIEIRA, R.D.; FRANÇA-NETO, J.B.; MARCOS-FILHO, J. (Eds.) Vigor de sementes: conceitos e testes 2. ed. Londrina: ABRATES, p. 601, 2020. https://www.bdpa.cnptia.embrapa.br/consulta/busca?b=pc&biblioteca=vazio&busca=autoria:%22KRZYZANOWSKI,%20F.%20C.%22
    » https://www.bdpa.cnptia.embrapa.br/consulta/busca?b=pc&biblioteca=vazio&busca=autoria:%22KRZYZANOWSKI,%20F.%20C.%22
  • NEVES, G.; SERIGATTO, E.M.; DALCHIAVON, F.C.; SILVA, C.A. Viabilidade e longevidade de sementes de Tabebuia aurea benth. & hook. submetidas a diferentes métodos de armazenamento. Bioscience Journal, v.30, n.3. p.737-742, 2014. https://repositorio.unesp.br/bitstream/handle/11449/111579/WOS000333425100015.pdf?sequence=1&isAllowed=y
    » https://repositorio.unesp.br/bitstream/handle/11449/111579/WOS000333425100015.pdf?sequence=1&isAllowed=y
  • OLIVEIRA, D.E.C.; RESENDE, O.; CAMPOS, R.C.; DONADON, J.R. Obtenção e modelagem das isotermas de dessorção e do calor isostérico para sementes de arroz em casca. Científica, v.42, n.3, p.203-210, 2014. http://dx.doi.org/10.15361/1984-5529.2014v42n3p203-210
    » http://dx.doi.org/10.15361/1984-5529.2014v42n3p203-210
  • PANIS, B.; PIETTE, B.; SWENNEN, R. Droplet vitrification of apical meristems: a cryopreservation protocol applicable to all Musaceae. Plant Science, v.168, n.1, p.45-55, 2005. https://doi.org/10.1016/j.plantsci.2004.07.022
    » https://doi.org/10.1016/j.plantsci.2004.07.022
  • QI, Y.; WEI, W.; CHEN, C.; CHEN, L. Plant root-shoot biomass allocation over diverse biomes: A global synthesis. Global Ecology and Conservation, v.18, p.e00606, 2019. https://doi.org/10.1016/j.gecco.2019.e00606
    » https://doi.org/10.1016/j.gecco.2019.e00606
  • R CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2020. Disponível em: Disponível em: https://www.R-project.org/ Acesso em: 09 set. 2021.
    » https://www.R-project.org/
  • REIS, R.C.R.; PELACANI, C.R.; ANTUNES, C.G.C.; DANTAS, B.F.; CASTRO, R.D. Physiological quality of Gliricidia sepium (Jacq.) Steud. (Leguminosae - Papilionoideae) seeds subjected to different storage conditions. Revista Árvore, v.36, n.2, p.229-235, 2012. https://doi.org/10.1590/S0100-67622012000200004
    » https://doi.org/10.1590/S0100-67622012000200004
  • RIBEIRO, R.C.; GOMES, S.E. V.; DANTAS, B.F. Physiological quality of Erythrina velutina Willd. (FABACEAE) seeds under different storage conditions. Scientia Forestalis, v.46, n.120, p. 562-570, 2018. https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1104185/1/bARBARA.pdf
    » https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/1104185/1/bARBARA.pdf
  • SHAPIRO, S.S.; WILK, M.B. An Analysis of variance test for normality. Biometrika, v.52, n.3, p. 591-611, 1965. https://www.jstor.org/stable/2333709?seq=1#metadata_info_tab_contents
    » https://www.jstor.org/stable/2333709?seq=1#metadata_info_tab_contents
  • SHEN, S.K.; WU, F.Q.; YANG, G.S.; WANG, Y.H.; SUN, W.B. Seed germination and seedling emergence in the extremely endangered species Rhododendron protistum var. giganteum-the world’s largest Rhododendron Flora-Morphology, Distribution, Functional Ecology of Plants, v.216, p.65-70, 2015. https://doi.org/10.1016/j.flora.2015.08.006
    » https://doi.org/10.1016/j.flora.2015.08.006
  • SHIBATA, M.; COELHO, C.M.M.; OLIVEIRA, L.M.D.; GARCIA, C. Accelerated aging of ipê seeds under controlled conditions of storage. Revista Brasileira de Sementes , v.34, p.247-254, 2012. https://www.scielo.br/j/rbs/a/vg4KLkZW7gyJwT5RVQYvMCF/?format=pdf⟨=en
    » https://www.scielo.br/j/rbs/a/vg4KLkZW7gyJwT5RVQYvMCF/?format=pdf⟨=en
  • ŠIDÀK, Z. Rectangular confidence region for the means of multivariate normal distributions. Journal of the American Statistical Association , v.62, n.318, p.626-633, 1967. https://doi.org/10.1080/01621459.1967.10482935
    » https://doi.org/10.1080/01621459.1967.10482935
  • SILVA, D.G.; CARVALHO, M.L.M.; NERY, M.C.; OLIVEIRA, L.M.; CALDEIRA, C.M. Alterações fisiológicas e bioquímicas durante o armazenamento de sementes de Tabebuia serratifolia Cerne, v.17, n.1, p.1-7, 2011. https://doi.org/10.1590/S0104-77602011000100001
    » https://doi.org/10.1590/S0104-77602011000100001
  • SMANIOTTO, T.A.D.S.; RESENDE, O.; MARÇAL, K.A.; OLIVEIRA, D.E.; SIMON, G.A. Qualidade fisiológica das sementes de soja armazenadas em diferentes condições. Revista Brasileira de Engenharia Agrícola e Ambiental , v.18, n.4, p.446-453, 2014. https://doi.org/10.1590/S1415-43662014000400013
    » https://doi.org/10.1590/S1415-43662014000400013
  • THORUP-KRISTENSEN, K.; HALBERG, N.; NICOLAISEN, M.; OLESEN, J.E.; CREWS, T.E.; HINSINGER, P.; KIRKEGAARD, J.; PIERRET, A.; DRESBØLL, D.B. Digging deeper for agricultural resources, the value of deep rooting. Trends in Plant Science , v.25, n.4, p.406-417, 2020. https://doi.org/10.1016/j.tplants.2019.12.007
    » https://doi.org/10.1016/j.tplants.2019.12.007
  • TOMLINSON, K.W.; STERCK, F.J.; BONGERS, F.; SILVA, D.A.S.; BARBOSA, E.R.M.; WARD, D.; BAKKER, F.T.; KAAUWEN, M.V.; PRINS, H.H.T.; BIE, S.; LANGEVELDE, F.V. Biomass partitioning and root morphology of savanna trees across a water gradient. Journal of Ecology , v. 100, n.5, p.1113-1121, 2012. https://doi.org/10.1111/j.1365-2745.2012.01975.x
    » https://doi.org/10.1111/j.1365-2745.2012.01975.x
  • TONETTO, T.D.S.; ARAUJO, M.M.; MUNIZ, M.F.B.; WALKER, C.; BERGHETTI, A.L.P. Storage and germination of seeds of Handroanthus heptaphyllus (Mart.) Mattos. Journal of Seed Science , v.37, p.40-46, 2015. https://doi.org/10.1590/2317-1545v37n1141116
    » https://doi.org/10.1590/2317-1545v37n1141116
  • TORRES, M.F.O.; FERREIRA, R.A.; PRATA, L.C.D.; SILVA-MANN, R. Seed Longevity of Enterolobium contortisiliquum (Vell.) Morong. Journal of Seed Science , v.42, 2020. https://doi.org/10.1590/2317-1545v42239618
    » https://doi.org/10.1590/2317-1545v42239618
  • VEIGA-BARBOSA, L.; MIRA, S.; GONZÁLEZ-BENITO, M.E.; SOUZA, M.M.; MELETTI, L.M.M.; PÉREZ-GARCÍA, F. Seed germination, desiccation tolerance and cryopreservation of Passiflora species. Seed Science and Technology , v.41, n.1, p.89-97, 2013. https://doi.org/10.15258/sst.2013.41.1.08
    » https://doi.org/10.15258/sst.2013.41.1.08
  • VERTUCCI, C.W. Predicting the optimum storage conditions for seeds using thermodynamic principles. Journal of Seed Technology, v.17, n.2, p.41-53, 1993.
  • VITIS, M.; HAY, F.R.; DICKIE, J.B.; TRIVEDI, C.; CHOI, J.; FIEGENER, R. Seed storage: maintaining seed viability and vigor for restoration use. Restoration Ecology, v.28, n.3, p.249-255, 2020. https://doi.org/10.1111/rec.13174
    » https://doi.org/10.1111/rec.13174
  • VORONKOVA, N.M.; KHOLINA, A.B.; KOLDAEVA, M.N.; NAKONECHNAYA, O.; NECHAEV, V.A. Morphophysiological dormancy, germination, and cryopreservation in Aristolochia contorta seeds. Plant Ecology and Evolution, v.151, n.1, p.77-86, 2018. https://doi.org/10.5091/plecevo.2018.1351
    » https://doi.org/10.5091/plecevo.2018.1351
  • WALTERS, C. Orthodoxy, recalcitrance and in-between: describing variation in seed storage characteristics using threshold responses to water loss. Planta, v.242, n.2, p.397-406, 2015. https://doi.org/10.1007/s00425-015-2312-6
    » https://doi.org/10.1007/s00425-015-2312-6
  • WALTERS, C.; BERJAK, P.; PAMMENTER, N.; KENNEDY, K.; RAVEN, P. Preservation of recalcitrant seeds. Science, v.339, n.6122, p.915-916, 2013. https://www.science.org/doi/abs/10.1126/science.1230935
    » https://www.science.org/doi/abs/10.1126/science.1230935
  • WALTERS, C.; PENCE, V.C. The unique role of seed banking and cryobiotechnologies in plant conservation. Plants, People, Planet, v.3, n.1, p.83-91, 2021. https://doi.org/10.1002/ppp3.10121
    » https://doi.org/10.1002/ppp3.10121
  • YUAN, H.M.; BLACKWELL, M.; MCGRATH, S.; GEORGE, T.S.; GRANGER, S.H.; HAWKINS, J.M.B.; DUNHAM, S.; SHEN, J.B. Morphological responses of wheat (Triticum aestivum L.) roots to phosphorus supply in two contrasting soils. The Journal of Agricultural Science, v.154, n.1, p.98-108, 2016. https://doi.org/10.1017/S0021859615000702
    » https://doi.org/10.1017/S0021859615000702

Publication Dates

  • Publication in this collection
    15 Apr 2022
  • Date of issue
    2022

History

  • Received
    29 Oct 2021
  • Accepted
    23 Feb 2022
ABRATES - Associação Brasileira de Tecnologia de Sementes Avenida Maringá, nº 1219 , Jardim Vitória Londrina - Paraná Brasil, Tel./ Fax. 55 43 3025-5120 - Londrina - PR - Brazil
E-mail: contato@abrates.org.br