Physiological aspects of germination and thermoinhibition in biofortified lettuce seeds after priming and storageAbstract
Thermoinhibition of germination in lettuce seeds limits seedling production under high-temperature conditions, and there are still no commercial biofortified cultivars tolerant to this stress. Priming can mitigate this problem; however, the maintenance of its effects during storage is still poorly understood. The objective of this study was to evaluate tolerance to thermoinhibition in seeds of biofortified lettuce lines after priming and different storage periods. Twelve genotypes (10 lines and 2 cultivars) were analyzed, subjected to osmopriming and stored for 0, 30, and 60 days, with germination aspects evaluated at 20 °C and 35 °C. Priming promoted significant gains in physiological performance, highlighting the line UFU125#1#1#1, which showed 81% germination at 20 °C and 74% at 35 °C, maintaining 70% germination after 60 days of storage, superior to the other genotypes. Under high-temperature conditions, most materials showed a marked reduction, with values below 40% germination, evidencing sensitivity to thermoinhibition. Vigor was also favored, with the germination speed index reaching 16.3 at 35 °C for UFU125#1#1#1 before storage. In general, stored seeds showed reduced germination (from 74% to 53% at 20 °C and from 61% to 28% at 35 °C); however, specific genotypes maintained superior performance. Priming is effective in increasing tolerance to thermoinhibition, although its effects are genotype-dependent and reduced with storage, highlighting the UFU125#1#1#1 line as promising for high-temperature conditions.
Keywords:
Lactuca sativa L.; thermodormancy; osmopriming; storability
Resumo
A termoinibição da germinação em sementes de alface limita a produção de mudas em condições de alta temperatura, e ainda não há cultivares comerciais biofortificadas com tolerância a esse estresse. O condicionamento fisiológico pode mitigar esse problema, porém a manutenção de seus efeitos durante o armazenamento ainda é pouco compreendida. Objetivou-se avaliar a tolerância à termoinibição em sementes de linhagens de alface biofortificada após priming e diferentes períodos de armazenamento. Foram analisados 12 genótipos (10 linhagens e 2 cultivares) submetidos ao osmopriming e armazenados por 0, 30 e 60 dias, com os aspectos germinativos avaliados a 20 °C e 35 °C. O priming promoveu ganhos expressivos no desempenho fisiológico, destacando-se a linhagem UFU125#1#1#1, que apresentou germinação de 81% a 20 °C e 74% a 35 °C, mantendo 70% de germinação após 60 dias de armazenamento, superior aos demais genótipos. Em condições de alta temperatura, a maioria dos materiais apresentou redução acentuada, com valores inferiores a 40% de germinação, evidenciando a sensibilidade à termoinibição. O vigor também foi favorecido, com índice de velocidade de germinação atingindo 16,3 a 35 °C para UFU125#1#1#1 antes do armazenamento. De modo geral, as sementes armazenadas reduziram a germinação (de 74% para 53% a 20 °C e de 61% para 28% a 35 °C), porém genótipos específicos mantiveram desempenho superior. O priming é eficiente para aumentar a tolerância à termoinibição, embora seus efeitos sejam dependentes do genótipo e reduzidos com o armazenamento, destacando-se a linhagem UFU125#1#1#1 como promissora para condições de alta temperatura.
Palavras-chave:
Lactuca sativa L.; termodormência; osmopriming; armazenabilidade
1. Introduction
Climatic conditions, especially temperature at the time of germination, are factors that influence the quality of lettuce seeds (Lactuca sativa L.) (Wang et al., 2015; Catão et al., 2023a; Queiroz et al., 2023). Seeds do not germinate at temperatures above 30 °C, with temporary inhibition (thermoinhibition) or complete inhibition (thermodormancy) potentially occurring due to endosperm hardening, which restricts radicle protrusion (Catão et al., 2018; Michael et al., 2023, Zhu et al., 2025). Significant damage occurs to lettuce seed germination after production and storage at high temperatures (Catão et al., 2016, 2018).
There is genetic variability in Lactuca species regarding tolerance to thermoinhibition at high temperatures. Seeds from the cultivar Everglades (L. sativa) and Lactuca serriola US96UC23 show thermoinhibition tolerance at 35 °C (Catão et al., 2014; Yoong et al., 2016). Therefore, the development of new thermotolerant cultivars is of great importance and can benefit farmers in hot regions or during summer season. However, no thermotolerant commercial lettuce cultivars are currently registered in the RNC/MAPA (Brasil, 2023) and available to the Brazilian market. Moreover, there are no registered cultivars that are both biofortified and thermoinhibition-tolerant.
Biofortified lettuce can provide significant health benefits, ensuring healthy eating and consequently improving quality of life, contributing to the Sustainable Development Goals (United Nations, 2025). These lines are rich in bioactive compounds such as carotenoids, chlorophylls, and anthocyanins (Clemente et al., 2021, 2023; Sanches et al., 2025), which have antioxidant activity and may reduce the risk of cardiovascular diseases and cancer, also being involved in slowing cellular aging (Paur et al., 2017; Pem and Jeewon, 2015). A deficiency in carotenoids, in particular, can impair vision and increase the risk of severe diseases and common childhood infections (FAO, 2024).
Despite the relevance of biofortification, few studies have focused on thermoinhibition tolerance using pre-germination treatments and storage of lettuce seeds rich in bioactives. Pre-germination methods or priming vary according to species, size, the initial physiological quality of the lot, and especially factors such as seed contact with water, osmotic, or matrix solutions. This technique is intended to enhance seed quality or improve seedling performance. However, the storage of primed seeds remains a key aspect to resolve, especially for commercial-scale use (Marcos-Filho, 2015).
Priming allows controlled imbibition and can induce protective and repair mechanisms in seeds, potentially leading to acclimatization and enabling seeds to tolerate future stress (Kubala et al., 2015). Therefore, priming is an effective tool for enhancing the vigor of lettuce seeds; however, this benefit may be rapidly lost depending on storage duration. Previous studies have shown that different priming methods, such as hydropriming, osmopriming, and matripriming, can improve germination, uniformity, and vigor of lettuce seeds, particularly under moderate thermal stress conditions, in addition to promoting seedling emergence and early establishment (Nascimento, 2005; Eckhardt et al., 2024). However, most of these studies have evaluated immediate responses after conditioning, with less attention given to the maintenance of physiological effects during storage. Information regarding the storage of lettuce seeds after osmopriming and their tolerance to thermoinhibition is still limited, especially when considering biofortified genetic materials. A key point is determining how long primed seeds remain viable during storage while retaining the ability to germinate at high temperatures (Dantas et al., 2021). Thus, this study aimed to analyze the thermoinhibition tolerance of biofortified lettuce seed lines after physiological priming and different storage periods.
2. Materials and Methods
The experiment and evaluations were conducted at the Seed Laboratory of the Institute of Agricultural Sciences of the Federal University of Uberlândia (UFU). Seeds from ten lettuce lines (UFU125#1#1#1; UFU40#5#5#1; UFU189#2#2#1; UFU86#2#1#1; UFU107#1#2#1; UFU189#3#4#1; UFU120#1#1#1; UFU206#1#1#1; UFU7#1#2#1; UFU177#1#3#1) from the UFU Biofortified Lettuce Breeding Program were used. All genetic records are stored in the “BG α BIOFORT” software, registration number BR512019002403-6 at INPI (Maciel et al., 2019). In addition to these genotypes, seeds from the cultivars Everglades (thermoinhibition-tolerant) and Grand Rapids (thermoinhibition-sensitive) were also used (Catão et al., 2014). The seeds were produced at the UFU Vegetable Experimental Station, Monte Carmelo campus (18°42’43.19” S; 47°29’55.8” W; 873 m altitude).
Initially, the seeds were subjected to osmopriming in an aerated polyethylene glycol 6000 (PEG 6000) solution at -1.2 MPa (Nascimento and Cantliffe, 1999), with concentration defined according to Villela et al. (1991). For priming, 2.0 g of seeds were placed in 100 mL Erlenmeyer flasks containing 60 mL of osmotic solution. The flasks were sealed with cotton stoppers connected to a compressed air pump to aerate the solution. The system was kept in a BOD incubator at 15 °C for 48 hours with an 8-hour photoperiod.
After priming, seeds were washed under running water to remove the osmotic solution from the seed coat, and excess water was removed using paper towels. The seeds were then dried in a forced-air oven at 32 ± 2 °C, 45% RH, for 48 hours. After drying, the seeds were packed in paper bags and stored in a cold and dry chamber (15 °C and 55% relative humidity). Analyses were performed at 0, 30, and 60 days of storage. The following evaluations were conducted to assess seed quality and thermoinhibition tolerance:
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First count and germination: four replications of 50 seeds per genotype were sown on two layers of blotting paper moistened with distilled water (2.5 times the weight of dry substrate), placed in transparent plastic boxes (gerboxes), and incubated in BOD chambers at 20 °C and 35 °C under a 12-hour photoperiod. Normal seedlings were counted on the 4th and 7th days; results expressed as percentages (Brasil, 2025).
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Germination speed index (GSI): evaluated daily using the number of germinated seeds and calculated according to Maguire’s (1963) formula.
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Tetrazolium test: conducted on ungerminated seeds from the germination test to confirm thermoinhibition. The embryo was exposed by gently pressing and removing the seed coat. Seeds were stained with 1% 2,3,5-triphenyl tetrazolium chloride for 3 hours in the dark at 30 °C. Interpretation followed Brasil (2025), and results were expressed as the number of viable and dead seeds.
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Relative Germination Frequency (RF): the relative frequency was calculated to obtain the germination percentage over time (Labouriau, 1983), and was obtained using the following Formula 1:
where: Fr: relative frequency of emergence; n: frequency; ni: number of seeds germinated on day i; k: last day of observation.
The experimental design was completely randomized (CRD) with four replicates. The analysis of variance was conducted in a 12 × 3 × 2 factorial scheme (genotypes × storage periods × germination temperatures). Means were subjected to analysis of variance, and the results were analyzed using the Scott-Knott test at a 5% significance level. All statistical analyses were performed using R software (R Core Team, 2025).
3. Results
Regarding the first germination count at 20 °C and zero days of storage, genotypes UFU125#1#1#1, Grand Rapids, Everglades, UFU107#1#2#1, and UFU177#1#3#1 showed higher vigor (Table 1). However, it is possible to observe that the percentage of normal seedlings decreased with seed storage, especially after 60 days. When seeds were exposed to a temperature of 35 °C during germination, lower vigor was observed regardless of the storage period. The exceptions were genotypes UFU125#1#1#1, Everglades, and UFU177#1#3#1, which maintained a higher percentage of normal seedlings even after 60 days of storage.
First germination count (%) of seeds from biofortified lettuce lines and the cultivars Everglades and Grand Rapids after priming, as affected by temperatures of 20 and 35 °C and storage periods.
Analyzing the seeds of the UFU125#1#1#1 line at both 20 and 35 °C, no difference was observed in the first germination count between 0 and 30 days of storage. However, regarding temperature, at 60 days, a higher percentage of normal seedlings was recorded at 35 °C. A reduction in vigor (first count) was also observed at 60 days of storage at both temperatures for UFU125#1#1#1 seeds. For the Everglades cultivar, there was a decrease in the percentage of normal seedlings at 30 and 60 days of storage. The genotypes UFU 40#5#5#1 and UFU 86#2#1#1 were below the commercialization standard even before storage (Brasil, 2019).
There was significant interaction between the factors analyzed for the germination percentage, genotype × temperature, genotype × storage and temperature × storage (Table 2). In the analysis of genotype × temperature, it was observed that at 20 °C, only genotypes UFU125#1#1#1 and Everglades achieved germination rates above 80%, which is the minimum standard required for seed commercialization, according to legislation (Brasil, 2019). At 35 °C, none of the genotypes met the required standard. In some genotypes, a clear reduction in seed germination was observed with the increase in temperature (Table 2).
Germination (%) of seeds of biofortified lettuce lines and Everglades and Grand Rapids cultivars after priming as a function of temperatures of 20 and 35 °C and storage periods.
In the genotype × storage interaction, it was observed that germination performance varied among genotypes after priming (Table 2). At zero days of storage, genotypes UFU125#1#1#1 and Everglades showed higher germination rates, 84% and 94%, respectively. After 30 days of storage, genotypes UFU125#1#1#1, Grand Rapids, Everglades, and UFU177#1#3#1 showed higher percentages of normal seedlings, differing from the other genotypes. After 60 days of storage, genotype UFU125#1#1#1 showed a germination rate of 70%, which was statistically superior. The genotypes UFU 40#5#5#1, UFU 189#2#2#1, UFU 86#2#1#1, UFU 120#1#1#1, and UFU 7#1#2#1 showed low germination regardless of germination temperature and storage period.
With the progression of the storage period, seed germination decreased, except for UFU125#1#1#1. The germination of seeds from genotypes UFU40#5#5#1 and UFU86#2#1#1 did not decrease during storage; however, the initial germination (0 days of storage) was extremely low (46% and 40%, respectively).
In the interaction between the temperatures of 20 and 35 °C and the storage periods, it was observed that germination decreased at 35 °C in all storage periods, causing seed thermoinhibition or thermodormency. After priming, lettuce seed germination also declined at both temperatures.
There was a triple interaction among the analyzed factors (genotypes × temperature × storage) for the germination speed index (Table 3). At 20 °C, genotypes Grand Rapids and Everglades exhibited higher vigor at zero days of storage. However, in this same storage period at 35 °C, only the seeds of genotypes UFU125#1#1#1 and Everglades showed greater vigor (Table 3).
Germination speed index of seeds of biofortified lettuce lines and Everglades and Grand Rapids cultivars after priming as a function of temperatures of 20 and 35 °C and storage periods.
Seed vigor declined over the storage period at both 20 °C and 35 °C. After 30 days of storage, the most vigorous seeds were from genotypes UFU125#1#1#1, UFU40#5#5#1, Grand Rapids, and UFU177#1#3#1 at 35 °C. After 60 days of storage, the genotypes UFU125#1#1#1, Everglades, and UFU177#1#3#1 did not differ in seed vigor and were statistically superior to the others. When analyzing the genotypes UFU125#1#1#1, Everglades, UFU107#1#2#1, UFU189#3#4#1, UFU7#1#2#1, and UFU177#1#3#1 in isolation, higher vigor was observed at 35 °C compared to 20 °C, without storage.
An increase in the number of ungerminated seeds (non-germinated remnants) was observed due to germination temperature and storage periods (Figure 1). At 20 °C, there were fewer ungerminated seeds compared to 35 °C, regardless of the storage period. After 60 days of storage, the number of non-germinated seeds increased at both temperatures.
Number of remaining seeds* (viable and dead) of biofortified lettuce lines and the cultivars Everglades and Grand Rapids based on the tetrazolium test, as a function of germination temperatures and storage periods. *Non-germinated seeds from a total of 200 seeds used in the germination test.
According to the tetrazolium test, most of the non-germinated seeds were dead, especially at 35 °C. The tetrazolium test did not reveal a significant number of viable seeds, and therefore, they were not graphically represented. The genotypes UFU125#1#1#1 and Everglades exhibited fewer remaining and dead seeds across all temperatures and storage periods. The genotype UFU86#2#1#1 showed a higher number of remaining and dead seeds at 20 °C in all storage periods.
In the frequency distribution of germination at 20 °C, the highest peaks—approximately 80%—were observed in the genotypes UFU125#1#1#1, UFU40#5#5#1, UFU107#1#2#1, UFU189#3#4#1, and UFU206#1#1#1 at zero days of storage, indicating synchronized germination (Figures 2A and 2B).
(A) Relative frequency distribution of germination at 20 °C for seeds of biofortified lettuce lines (UFU 125#1#1#1; UFU 40#5#5#1; UFU 189#2#2#1; UFU 86#2#1#1) and the cultivars Grand Rapids and Everglades after physiological priming and storage; (B) Relative frequency distribution of germination at 20 °C for seeds of biofortified lettuce lines (UFU 107#1#2#1; UFU 189#3#4#1; UFU 120#1#1#1; UFU 206#1#1#1; UFU 7#1#2#1; UFU 177#1#3#1) after physiological priming and storage.
It is possible to observe, over time and through frequency distribution, that seeds tend to germinate until reaching a maximum value and subsequently decline. However, a shift in the germination time frequency curve was observed at zero days of storage for genotypes UFU86#2#1#1 and UFU7#1#2#1 (Figures 2A and 2B). This behavior indicates a delay in the germination process or a reduction in seed vigor, corroborating the physiological data presented in Tables 2 and 3.
At 30 and 60 days of storage, the relative frequency of germination at 20 °C did not exceed 60%, with shifts both to the left and to the right of the germination time. This indicates a lower synchrony in the germination process (Figures 2A and 2B). This pattern was evident in genotypes UFU125#1#1#1, Grand Rapids, Everglades, UFU107#1#1#1, UFU189#3#4#1, UFU120#1#1#1, UFU206#1#1#1, UFU7#1#2#1, and UFU107#1#3#1.
Seed germination patterns at 35 °C varied throughout the storage period. At zero days of storage, the frequency distribution did not exceed 60% (Figures 3A and 3B), with reduced relative frequency observed in genotypes UFU125#1#1#1, UFU40#5#5#1, Grand Rapids, UFU86#2#1#1, Everglades, UFU120#1#1#1, UFU206#1#1#1, and UFU107#1#3#1. Genotypes UFU189#2#2#1 and UFU7#1#2#1 reached maximum relative frequencies of only 40% and 20%, respectively, indicating susceptibility to thermoinhibition even after priming at 35 °C (Table 2). UFU189#2#2#1 also exhibited high seed mortality in the tetrazolium test (Figure 1), suggesting death caused by high germination temperature. At 30 days of storage, the highest frequency peaks were observed in UFU86#2#1#1, UFU107#1#2#1, and UFU7#1#2#1, reaching around 60% on the third day of germination at 35 °C (Figures 3A and 3B). After 60 days, the frequency curves shifted in both directions, indicating decreased synchrony and delayed germination. Throughout the storage period, seed vigor declined compared to the initial time point.
(A) Relative frequency distribution of germination at 35 °C for seeds of biofortified lettuce lines (UFU 125#1#1#1; UFU 40#5#5#1; UFU 189#2#2#1; UFU 86#2#1#1) and the cultivars Grand Rapids and Everglades after physiological priming and storage; (B) Relative frequency distribution of germination at 20 °C for seeds of biofortified lettuce lines (UFU 107#1#2#1; UFU 189#3#4#1; UFU 120#1#1#1; UFU 206#1#1#1; UFU 7#1#2#1; UFU 177#1#3#1) after physiological priming and storage.
4. Discussion
The critical period for the induction of thermoinhibition occurs within the first 8-12 hours of imbibition at high temperature. Endosperm weakening is associated with the activity of the enzyme endo-β-mannanase, whose expression is reduced at high temperatures (Catão et al., 2018; Michael et al., 2023). This enzyme plays a key role in endosperm degradation, and its inhibition contributes directly to the failure of radicle protrusion under thermal stress conditions. Such reduction in enzymatic efficiency is closely linked to seed deterioration, particularly under prolonged storage and elevated temperatures, which ultimately compromises germination performance (Catão et al., 2018).
Almeida et al. (2019) suggested evaluating seeds under high temperatures at 11 days after the beginning of the germination test. Thermoinhibition is not a condition that can be overcome over time, but rather by reducing the temperature to which the seeds are exposed during germination (Catão et al., 2023a). It is worth noting that thermosensitive genotypes have higher amounts of mannose and galactose in the cell wall, resulting in endosperm rigidity and preventing radicle protrusion (Michael et al., 2023; Wei et al., 2024). Abscisic acid content also remains stable in seeds germinated at 33 °C and is only reduced when the temperature drops to 23 °C (Kaya, 2022). Over the course of storage, lettuce seed germination also declined at both temperatures after priming. Catão et al. (2018) reported that high temperatures, as well as longer storage periods, compromise the quality of lettuce seeds by reducing their viability.
With increasing temperature, the metabolic processes in seeds are accelerated, increasing respiration and, consequently, the deterioration process (Marcos-Filho, 2015). The main changes related to seed deterioration involve enzyme degradation and inactivation. Evidence suggests that high temperatures cause oxidative stress, during which reactive oxygen species (ROS), such as superoxide radical (O2−), hydroxyl radical (OH), hydrogen peroxide (H2O2), and singlet oxygen (1O2), are produced (Wei et al., 2024).
Osmopriming has proven effective in increasing germination speed and enhancing seed tolerance to adverse conditions, highlighting the physiological benefits provided by this technique (Wei et al., 2024). However, it is important to emphasize that seeds subjected to osmopriming generally exhibit lower storage tolerance, since this treatment induces metabolic changes that, although beneficial for immediate germination, make seeds more susceptible to deterioration during storage (Farooq et al., 2019). The viability and vigor of primed seeds decrease significantly with prolonged storage, especially when conducted under high temperatures (Catão et al., 2018). Therefore, the use of primed seeds should be limited to situations in which sowing occurs shortly after treatment, in order to ensure the benefits of priming without compromising the physiological quality of the seed lot.
Queiroz et al. (2023) in similar evaluations, observed that lettuce seeds remaining after germination tests at 20 and 35 °C had a higher percentage of viability, indicating thermoinhibition. However, this was not observed in the present study, as seeds subjected to germination at both 20 and 35 °C showed high mortality after staining in the tetrazolium test. This test is an important tool for detecting thermoinhibition in lettuce seeds, as it assesses the activity of dehydrogenase enzymes, which are essential for seed respiration. Thus, the tetrazolium test can be used to confirm thermoinhibition in lettuce seeds under high temperature conditions (Catão et al., 2023b). Lettuce seeds exposed for prolonged periods at 35 °C show high mortality after experiencing thermodormancy and/or thermoinhibition (Wei et al., 2024).
The genotypes UFU125#1#1#1 and Everglades exhibited fewer remaining and dead seeds across all temperatures and storage periods. It has been reported that the UFU125#1#1#1 genotype shows germination behavior similar to the Everglades cultivar under high temperatures (Catão et al., 2023a). The genotype UFU86#2#1#1 showed a higher number of remaining and dead seeds at 20 °C in all storage periods (Figure 1), which may be explained by the accelerated deterioration of osmotically primed seeds during storage (Wei et al., 2024).
The relative frequency distribution of germination was used in the study of seed germination of chickpea (Aasim et al., 2024) and can be a useful tool for investigating thermoinhibition, allowing the analysis of germination behavior under high temperature conditions. Germination frequency is related to the mean germination time and germination speed index (Pontes et al., 2025). Thus, these shifts in frequency points reflect changes in the germination speed index, representing an estimate of the average duration required for seeds to germinate. A shift of the frequency curve to the right or left of the mean germination time reflects a delay in the germination process (Pontes et al., 2025).
In general, temperatures above 30 °C affect seed germination by reducing the germination speed or percentage, depending on the location and sowing season. Different strategies have been used to mitigate the problems of thermoinhibition and/or thermodormancy. Among these are the identification and development of thermotolerant genotypes, as well as the use of growth regulators or seed priming (Eckhardt et al., 2024).
Environmental effects on the expression of thermotolerance traits have also been observed. Thermoinhibition tolerance in lettuce seeds is a trait controlled by one or a few genes, with additive effects and high heritability, making it possible to use contrasting cultivars (with genetic dissimilarity) for the selection of genotypes tolerant to high temperature stress (Oliveira et al., 2021; Catão et al., 2022; Oh et al., 2025).
Overall, although priming promoted improvements in specific genotypes and storage periods, its effectiveness was limited under more stressful conditions, particularly at 35 °C. In several cases, germination percentages remained below commercial standards even after priming, indicating that the technique alone may not be sufficient to mitigate severe thermal stress. This variability among genotypes highlights the need for careful selection of responsive materials and suggests that priming should be integrated with genetic and physiological approaches to achieve consistent thermotolerance.
Although the development of thermotolerant lettuce cultivars for germination under high-temperature conditions is still a distant goal in breeding programs, priming remains a promising strategy to mitigate the negative effects of thermal stress. Seed priming can enhance germination performance and vigor, offering an accessible and effective alternative to support seedling establishment until more genetically adapted cultivars become available. However, in the present study, this improvement was not consistently evident across all evaluated materials, as some genotypes did not show clear gains in germination performance after priming, indicating that the effectiveness of this technique may be genotype-dependent and requires further investigation.
5. Conclusions
After priming, seeds of the biofortified lettuce line UFU125#1#1#1 exhibited tolerance to thermoinhibition at 35 °C, and physiological traits such as synchrony and germination speed were maintained during storage, standing out compared to the other evaluated genotypes.
Acknowledgements
The authors thank the Minas Gerais Research Foundation (FAPEMIG) for financial support (project APQ-03076-21) and for granting a scholarship to the first author.
Data Availability Statement
Data available upon request to authors.
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Editor:
Takako Matsumura Tundisi
