Recovery capacity and morphophysiological responses of Sapindus saponaria L. to water stressAbstract
Water stress is characterized by the lack or excess of water for a certain period, which can hinder the establishment and growth of different tree species. Thus, this study aims to evaluate growth and physiological changes in young Sapindus saponaria plants subjected to flooding, drought, rehydration and post-flooding recovery. For flooding, plants were kept in pots containing water 2 cm above the soil; for drought, plants were not irrigated for 25 days. At the end of the period, growth, height, dry and fresh mass of leaves, stem, and root measurements were assessed. Photosynthetic pigments and total soluble carbohydrate contents were also analyzed. Young S. saponaria plants showed reduced growth rates under drought conditions, and did not recover when rehydrated. In addition, drought caused a decrease in the chlorophyll a/b ratio and an increase in the total soluble carbohydrates content in the roots. Plants kept under flooding and post-flooding conditions did not show differences in growth and chlorophyll content, but a higher total soluble carbohydrates content was observed in the root of flooded plants. The study revealed young S. saponaria plants are intolerant to drought periods, showing low recovery capacity, but are tolerant to flooding and post-flooding periods.
Keywords:
hypertrophied lenticels; adventitious roots; Sapindaceae; flooding; drought
Resumo
O estresse hídrico se caracteriza pela falta ou excesso de água por determinado período, o que pode prejudicar o crescimento e o estabelecimento de diferentes espécies arbóreas. Assim, o objetivo desse trabalho foi avaliar o crescimento e as alterações fisiológicas em plantas jovens de Sapindus saponaria submetidas ao alagamento, seca, reidratação e recuperação após-alagamento. Para a condição de alagamento as plantas foram mantidas em vasos contendo água com 2 cm acima do solo, enquanto para a condição de seca, a irrigação das plantas foi suspensa por 25 dias. Ao final do período de estresse avaliaram-se as variáveis de crescimento, altura, massa seca e fresca das folhas, caule e raiz e analisaram-se o teor de pigmentos fotossintéticos e o teor de carboidratos solúveis totais. As plantas jovens de S. saponaria apresentaram redução no crescimento sob seca e não recuperaram o crescimento na reidratação. Além disso, a seca causou redução da razão clorofila a/b e aumento no teor de carboidratos solúveis totais nas raízes. As plantas mantidas sob alagamento e pós-alagamento não apresentaram diferença no crescimento e no teor de clorofila, no entanto, observou-se maior teor de carboidratos solúveis totais na raiz de plantas alagadas. O estudo revelou que as plantas jovens de S. saponaria são intolerantes a períodos de seca, apresentando baixa capacidade de recuperação, mas são tolerantes aos períodos de alagamento e pós-alagamento.
Palavras-chaves:
lenticelas hipertrofiadas; raízes adventícias; Sapindaceae; alagamento; seca
1. Introduction
Tropical forests have been affected by severe droughts (Hollunder et al., 2022), which can lead to the selection of species tolerant to water stress or cause the mortality of vulnerable species (Aguirre-Gutiérrez et al., 2020). Although the understanding of drought effects worldwide is growing, their impact on tropical forests is still poorly understood, limiting our ability to understand forests responses to future climate scenarios (Hollunder et al., 2022).
Plants subjected to drought show several physiological responses, including decreased growth rate and xylem ring formation, as well as reduced water transport and carbon availability, potentially affecting photosynthesis (DeSoto et al., 2020). Water transport in plants can be affected due to xylem cavitation, caused by the formation and propagation of tiny air bubbles inside xylem vessels under extreme negative pressure, which may lead to plant death (Griffin-Nolan et al., 2021). The endogenous increase in abscisic acid (ABA) causes plasma membrane depolarization and loss of turgidity in guard cells, reducing stomatal conductance (Osakabe et al., 2014), which interferes with the ability to acquire CO2 for photosynthesis.
Floods also cause abiotic stress, negatively affecting the development and growth of different plants (Bhatt et al., 2015). Water stress due to flooding causes decrease in shoot and root biomass, reduction in hydraulic conductivity, chlorosis, necrosis, abscission, and leaf senescence (Lukic et al., 2021). Under hypoxic and anoxic soil conditions, plants deprived of O2 rely on anaerobic metabolism to maintain adequate ATP production, which is one of many strategies to survive water stress (Shingaki-Wells et al., 2014). Among the responses against flooding is the upward elongation of the shoot, formation of aerenchyma, induction of barriers to radial O2 loss in the roots, development of adventitious roots, changes in leaf anatomy and gas flow through porous tissues (Sasidharan et al., 2017).
Sapindus saponaria L. belongs to the Sapindaceae family, commonly known as wingleaf soapberry or western soapberry. It is a light-demanding, deciduous, early secondary or climax tree species resistant to drought and floods and used to regenerate degraded areas (Carvalho, 2014). The Sapindus genus is used as raw material to produce biodiesel, biomedical and biochemical products, but with climate change, deforestation and economic development, germplasm diversity can face potential destruction (Liu et al., 2021, 2022). The species occurs in the Amazon, Cerrado, Atlantic Forest and Pantanal biomes, being typical of riparian forests, seasonal semideciduous forests and ombrophilous forests. It is native, but not endemic to Brazil (Carvalho, 2014). This species is suitable for restoring riparian environments (Guarim Neto, 1991), but it is considered drought-resistant in Argentina (Díaz Cillo, 2008).
This study aims to evaluate the growth and physiological changes of young S. saponaria plants subjected to flooding, drought and post-recovery from water stress.
2. Material and Methods
2.1. Obtaining plant material and testing in pots
Fruits of S. saponaria were collected from riparian areas of a seasonal semideciduous forest in Porto Rico, in the state of Paraná, and transferred to the Laboratory of Seed and Seedling Physiology of the State University of Maringá (UEM). Seeds were obtained manually from the fruits and scarified by soaking them in concentrated sulfuric acid for 30 minutes, followed by washing in running water (Neves et al., 2018). Subsequently, seeds were sown in polystyrene trays containing sand and Fertilizare® substrate, in a 2:1 ratio. After the seedlings emerged, they were transferred to black plastic bags, about 10 cm wide and 20 cm high, containing the same composition as substrate. Seedlings were kept in the greenhouse for 15 days at pot capacity and later subjected to water stress treatments.
2.2. Water stress
To simulate the water deficit, young S. saponaria plants were not irrigated for 25 days. Control plants received daily manual irrigation, maintaining pot capacity.
For flooding analysis, pots with substrate and containing young S. saponaria plants were placed in plastic buckets, keeping the water up to 2 cm above the substrate. Each bucket received a pot containing an S. saponaria plant. The plants kept under the control condition received daily manual irrigation, maintaining pot capacity. Flooding and control conditions were maintained for 25 days.
Afterwards, growth variables were analyzed, and photosynthetic pigments and total soluble carbohydrate contents of plants kept under water deficit, flooding and control conditions were quantified.
2.3. Recovery
The period to verify the recovery capacity of the plants kept under water stress was 25 days, in which plants under water deficit and not used in the morphophysiological analyses were rehydrated and irrigated daily (considering pot capacity). Flooded plants were removed from the buckets and kept in drained soil, with daily irrigation (considering pot capacity).
After the recovery period, the performance of the plants was verified regarding survival and appearance of new leaves, and analyses of growth variables and total soluble carbohydrate content were carried out.
2.4. Morphological and plant growth analyses
Morphological observations were carried out daily in plants kept under water stress (flooding and water deficit), as well as during the recovery period. For these analyses, the occurrence of hypertrophied lenticels and/or adventitious roots in flooded plants were verified, as well as yellowing and necrosis in plants under drought conditions.
To analyze growth variables, 10 plants from each treatment (control, flooding, water deficit, and recovery) were randomly chosen. The growth variables evaluated were shoot height (H), root length (RL), number of leaves (NL), leaf fresh mass (LFM), leaf dry mass (LDM), stem fresh mass (SFM), stem dry mass (SDM), root fresh mass (RFM), root dry mass (RDM), total fresh mass (TFM),total dry mass (TDM), seed fresh mass (SFM), seed dry mass (SDM), collar diameter (CD), water content (WC), and root dry mass/shoot dry mass ratio (RDM/SM). However, for the analysis of plant rehydration, the plant dry mass was not verified.
Root length and shoot height were determined in centimeters using a ruler. A digital caliper (± 0.01 mm accuracy) was used to measure CD (area between the stem and the root). After obtaining height and RL, plants were separated into root, stem and leaves, weighed to obtain fresh mass, and oven-dried at 60 °C for 48 hours to obtain dry mass. The fresh and dry masses of different organs were determined on a precision analytical scale (accuracy 0.0001), model MARK/M214 Ai. The number of leaves was obtained after directly counting the fully expanded leaves of each plant.
The TFM was obtained by summing the leaf, stem and root fresh mass.TDM was the sum of the stem and root dry mass.
The root dry mass/shoot dry mass ratio was obtained by dividing the root dry mass over the sum of the leaf and stem dry mass.
The water content of the plants was calculated using the Equation 1:
2.5. Analyses of physiological variables
For the analysis of physiological variables, the photosynthetic pigments content (chlorophyll a, b and total content) and carotenoids of the leaves kept under treatment (control, drought and flooding) were quantified, while non-structural carbohydrates (total soluble carbohydrates) were quantified in roots and leaves of the control, flooding, water deficit and post-recovery treatments (rehydration and post-flooding).
To quantify chlorophyll a, b contents and carotenoids, the fully expanded leaves of the second and/or third node were collected from five plants of each treatment. All collections were carried out at the same time of the day, following Carvalho et al. (2007). Extraction was performed with 80% acetone and quantification using a spectrophotometer (Spectrofotometer Shimadzu UV—1201) at 470, 645 and 663 nm (Lichtenthaler and Wellburn, 1983) and 647 nm (Lichtenthaler and Buschmann, 2001); results are expressed in mg g −1 FM. Chlorophyll contents were estimated according to the methodology by Arnon (1949). For total chlorophyll, the sum of chlorophyll a and b contents was used.
Four plants of each treatment were used to evaluate non-structural carbohydrates (total soluble sugars). Samples obtained from the root and leaf of each treatment were crushed and centrifuged to obtain alcoholic extract, which was evaporated before adding distilled water, obtaining aqueous extract, used to determine the soluble compounds. Total soluble sugar contents were determined using reactions with anthrone (Clegg, 1956), and the samples were read in a spectrophotometer at 620 nm. Results were expressed in μg g −1 FM.
2.6. Statistical analysis
The statistical analyses in this study followed a completely randomized design. Ten replicates (ten plants) of each treatment were used for the analysis of growth parameters (shoot height, root length, fresh and dry mass, and crown diameter). For the analysis of photosynthetic pigments and total soluble carbohydrates, four replicates of each treatment were used.
Growth and physiological data were subjected to analysis of variance (ANOVA) and analyzed using Tukey’s test (p<0.05) for growth variables and Dunnett’s test for physiological variables using the GraphPadPrism 8.0 software. Results that did not present normality were analyzed using a nonparametric test. Student's T-test was used (p<0.05) to analyze photosynthetic pigment and total soluble carbohydrates contents of the plants after the recovery period.
3. Results
3.1. Growth of young S. saponaria plants—water stress
Water deficit caused a decrease in most growth variables of young S. saponaria plants compared to control and flooding (Table 1). Plants kept under water deficit had lower H, NL, LFM, SFM, RFM, SFM, and total fresh mass TFM. There was also a smaller CD and lower water content WC than plants kept under irrigation (control) and flooding.
Growth of young Sapindus saponaria plants under field capacity (control), flooding and drought conditions.
Young S. saponaria plants under drought did not differ from the control plants regarding LFM and SDM. However, plants under drought had a higher RDM/SM ratio (Table 1).
Regarding RL, RDM and SDM, no significant difference was observed between plants kept under the control, drought and flooding treatments.
Flooding did not affect plant growth, with no significant difference for the variables analyzed compared to control plants.
3.2. Growth of young S. saponaria plants—recovery
After the flooding period, plants showed similar performance to control plants, with no significant differences between control and post-flooding plants (Table 2). Considering growth evolution between the flooding and post-flooding periods, no relevant increase was observed. However, there was a 2.7% increase in leaf fresh mass, 92% in root fresh mass, 23% in total fresh mass, and 12% in crown diameter.
Growth of young Sapindus saponaria plants under field capacity (control), post-flooding and rehydration conditions.
Rehydrated plants also showed lower growth values compared to the control and post-flooding plants, except for seed dry mass (Table 2). Yet, after rehydration, an increase in fresh mass was observed, with a 32% increase in leaf fresh mass, 158% in stem fresh mass, 54% in root fresh mass and 80% in the crown diameter. Control plants, after the two evaluation periods (Table 2), showed a 26.5% increase in leaf fresh mass, 34% in stem fresh mass, 55% in root fresh mass, 36.9% in the total fresh mass and a 18%increase in the crown diameter. These values are lower than those obtained for rehydrated plants, except for root fresh mass, for which the values were similar.
3.3. Analysis of the physiological variables of young S.saponaria plants
3.3.1. Content of photosynthetic pigments
Water stress (flooding and drought) did not interfere with photosynthetic chlorophyll pigments a (Figure 1A), b (Figure 1B), ratio a/b (Figure 1C), total chlorophyll (Figure 1D), total carotenoids (Figure 1E) and total chlorophyll/carotenoid ratio (Figure 1F).
Chlorophyll a (A), chlorophyll b (B), chlorophyll a/b (C), total chlorophyll (D), total carotenoids (E) and total chlorophyll/carotenoids (F) contents from young Sapindus saponaria plants under control, flooding and drought conditions. *Different letters represent a significant difference between treatment and control, according to Dunnett’s test at 5%.
For the recovery period, no significant difference was observed between plants under control and post-flooding treatments regarding photosynthetic pigment contents (Figure 2).
Chlorophyll a (A), chlorophyll b (B), chlorophyll a/b (C), total chlorophyll (D), total carotenoids (E), and total chlorophyll/carotenoids (F) contents from young Sapindus saponaria plants under control and post-flooding conditions. ns = not significant, according to the Student’s t-test.
3.3.2. Total soluble carbohydrate contents
The roots of young S. saponaria plants kept under water stress (drought) conditions had a higher total soluble carbohydrates content compared to control and flooding (Figure 3A). However, after the recovery period, the roots of plants under control, post-flooding and rehydration conditions did not show significant differences regarding total soluble carbohydrates content (Figure 3B).
Total soluble carbohydrate content of the roots of young Sapindus saponaria plants,comparing control, flooding and drought (A), control, post-flooding and rehydration (B), drought and rehydration (C) and flooding and post-flooding (D). *Different letters represent a significant difference between the treatment and the control, according to Dunnett’s test (A and B) and the Student’s t-test (C and D).
Comparing plants after drought and rehydration, the total soluble carbohydrates content decreased in the roots of rehydrated plants (Figure 3C), while soluble carbohydrates content in the roots of flooded plants did not differ from roots of post-flooded plants (Figure 3D).
Comparing the total soluble carbohydrates of the leaves of plants maintained under different treatments, the leaves of plants under drought had higher content when compared to the control and flooding (Figure 4A). Comparing the plants after the recovery period, the leaves of rehydrated plants maintained the highest soluble carbohydrates content; however, the leaves of the post-flooding plants had a higher content than the leaves of control plants (Figure 4B).
Total soluble carbohydrate content of leaves of young Sapindus saponaria plants,comparing control, flooding and drought (A), control, post-flooding and rehydration (B), drought and rehydration (C) and flooding and post-flooding (D). *Different letters represent a significant difference between the treatment and the control, according to Dunnett’s test (A and B) and theStudent’s t-test (C and D).
Analyzing the soluble carbohydrates of leaves of plants under water stress and after recovery, higher contents were found in leaves of rehydrated and post-flooded plants compared to leaves of plants kept under drought and flooding, respectively (Figures 4C and 4D).
3.4. Morphological changes of young S. saponaria plants kept under water stress and survival after recovery
Figures 5A-C depict control, flooded and water deficit plants, respectively.
Control (A), Flooding (B), Water suspension (C), Post-flooding (D), Rehydration (E), presence of hypertrophied lenticels and adventitious roots (F), adventitious roots at the end of flooding (G), beginning of leaf wilting (H), disappearance of hypertrophied lenticels after flooding (I-J).
Adventitious roots were found in flooded plants (Figures 5B and 5G) and leaves without turgidity and with reduction of the root system in plants under drought (Figures 5C and 5E).
Hypertrophied lenticels in flooded plants were observed from the seventh day of treatment (Figure. 5F), and, on the 12th day, adventitious roots were seen (Figure. 5F) in some plants. At the end of the flooding period, 100% of plants had hypertrophied lenticels and 75% of plants had adventitious roots.
Plants without daily irrigation began showing signs of wilting on the 12th day of treatment (Figure. 5H), 82.5% of plants without irrigation showed wilting and 17.5% of plants survived the drought treatment. Plants that were watered again started returning to normal on the eighth day of rehydration.
Post-flooding plants (Figure. 5D) show recovery of the root system, with maintenance of adventitious roots and disappearance of hypertrophied lenticels (Figure 5I-J).
4. Discussion
Water stress can cause changes in plant growth and physiological variables. S. saponaria plants kept under drought conditions showed reduced growth variables such as lower height, number of leaves, fresh mass and crown diameter (Table 1). The lowest growth observed in these plants remained after the rehydration period, in which there was no significant recovery of the plants. Water is essential for plants and water deficit affects different morphophysiological characteristics, restricting plant growth and productivity (Mukarram et al., 2021). Reduction of biomass, height, and basal diameter are mechanisms to avoid drought (Yi et al., 2020), providing greater survival capacity during stress periods.
Studies suggest increased root biomass as a response to drought, with greater investment in the underground system (Yi et al., 2020). However, we found that the fresh root biomass of plants under water deficit was about five times lower than irrigated plants. A similar outcome was found regarding leaf fresh mass, while the stem fresh mass was approximately four times lower in plants under stress. This can be associated with WC, which was significantly lower in plants kept under drought. We observed that the WC in dry treatment averaged 25.75%, while the control averaged 73.84% (WC), which may justify the lower leaf, stem and root fresh mass of the drought treatment. Leaf water content (WC %) is an indicator used to identify drought tolerance. Slower development due to water deficit can induce osmotic adjustment, resulting in the maintenance of adequate water content in leaves during drought (Masheva et al., 2022). However, no significant difference was observed in the dry mass of plants kept in irrigated and drought conditions.
Plants under drought usually show an increase in abscisic acid (ABA) content, altering growth and physiology characteristics. Greater allocation of biomass in the root to the detriment of the shoot is one of the expected responses in plants under drought conditions, an effect induced by ABA (Yu et al., 2019). Our study shows the RDM/SM ratio was significantly higher in plants under drought, reflecting greater plant investment in root biomass, which can minimize water loss through shoot stomata.
Fewer leaves in plants under drought is an expected response, since limiting leaf growth may be associated with an attempt to maintain water status, with a reduction in transpiration areas such as leaves. However, water stress did not affect photosynthetic pigments (Figure 1). In many crops, maintenance of chlorophyll content may be related to photosynthetic capacity and a drought tolerance mechanism (Chutteang et al., 2023).Drought stress decreases photosynthesis as it reduces carbon dioxide availability by increasing resistance to carbon dioxide flux from stomata, disrupts biochemical and/or photochemical activity and increases net peroxidation of the leaf membrane. Hence, chlorophyll content can increase or decrease under water stress (Moustakas et al., 2022; Yang et al., 2023).
Flooded plants adopt different physiological, morphological and biochemical strategies in the face of stress, such as the development of adventitious roots, improving the transport of O2 for submerged roots and nutrient and water absorption, as well as increasing plant survival and productivity (Aslam et al., 2023). However, the performance of young S. saponaria plants kept under flooding was similar to the control plants, with no significant differences in growth variables (Table 1), indicating greater flood tolerance.
Soluble sugars play an important role in plants under drought, such as antioxidant role as a scavenger of hydroxyl radicals (Rivas et al., 2017; Sperdouli and Moustakas, 2012) and the high leaf content of soluble sugars during the drought period can play an osmoprotective role by stabilizing membranes, proteins, and enzymes (Rivas et al., 2017). In plants subject to flooding, the accumulated soluble sugars, especially in leaves of woody species, can reduce the transport of assimilates in the phloem from the leaves to the roots. This strategy can protect flooded plants by altering osmotic potential, maintaining cell turgor pressure, and stabilizing cellular and enzymatic activity (Bispo and Vieira, 2022). However, comparing the soluble carbohydrate contents in leaves of flooded plants and in the post-flooding period, we observed a significant increase of soluble carbohydrates content in leaves of post-flooded plants (Figure 4D), but still lower than that found in rehydrated leaves (Figure 4B). Thus, although growth and physiological variables yielded similar figures to the control plants, an increase in the synthesis capacity was observed, with greater accumulation of soluble carbohydrates post-flooding.
Plants that endure severe drought periods use non-structural carbohydrates to facilitate the recovery process of the tissue above ground, with these resources allocated to the roots and later used for leaf regrowth (Baião et al., 2023; Lopes et al., 2022). This was not observed in young S. sapindus plants, which had an increase in total soluble carbohydrates from the root, but no leaf regrowth was observed after the recovery period. However, the higher total soluble carbohydrates content in the root of plants under drought conditions (Figure 3) may have assumed an osmoregulation role (Ozturk et al., 2020), contributing to the reduction in water potential of plants. A high soluble carbohydrates content was also obtained in leaves of S. saponaria under drought (Figure 4).
Mechanisms associated with the response of trees to drought recovery, considering physiological and biochemical adjustments, are still poorly understood, and studying these mechanisms can help quantify post-drought resilience and predict forest responses to climate change with greater precision (Duan et al., 2020). Results obtained for young S. saponaria plants after being kept in a water deficit enable the conclusion that this species is more susceptible to drought, which can compromise the establishment and survival of seedlings after drought events. However, comparing the growth evolution of rehydrated plants with control plants, there was a greater increase of LFM, RFM, TFM and WC variables in rehydrated plants, indicating rehydration enabled growth to resume in percentage terms. The same happened with the metabolic capacity for the synthesis of soluble carbohydrates, since no significant difference was observed in the carbohydrate content between the control, post-flooding, and rehydration plants.
Although no significant differences were observed between control plants and plants under flooding and in the post-flooding, there was a 92% increase in the fresh mass in roots of plants post-flooding, which is noticeable comparing Figures 5B, 5D, 5G and 5I, in which recovery and greater development of the root are observed. Flooding induces hypoxia, which can compromise root growth and nutrient uptake (Herrera, 2013). Considering there was no significant difference in the soluble carbohydrates content in the roots between the control and flooded plants (Figure 3A), carbohydrates may have been used as an energy source to form adventitious roots and hypertrophied lenticels, compromising root volume. Gama et al. (2020) observed survival of S. saponaria seedlings to flooding, indicating tolerance to water stress and the possibility of using the species in riparian forest recovery projects. This was noticeable in our study with the physiological and growth variables analyzed after the flooding period and recovery (post-flooding).
5. Conclusion
Young S. saponaria plants kept under flooding showed similarity with the control plants regarding growth variables, photosynthetic pigment and total soluble carbohydrate contents. However, water deficit negatively affected plant growth, with greater accumulation of total soluble carbohydrates in the root during drought. The results obtained allow us to conclude S. saponaria is a flood-tolerant species, but sensitive to drought in early growth stages. In view of this, S. saponaria can be used for forest recovery in areas subject to flooding.
Acknowledgements
The authors thank the Coordination for the Improvement of Higher Education Personnel (CAPES) for the financial aid and the scholarship granted to the first author.
Data Availability Statement
The entire data set that supports the results of this study was published in the article itself.
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