Doi: http://dx.doi.org/10.17584/rcch.2016v10i1.4456

¹ Department of Biology, University of Maringá, Maringá, PR (Brazil).
² Plant Ecophysiology Laboratory, Federal University of Pernambuco, Department of Botany, CCB, Recife, PE (Brazil). ]]> ³ Tropical Semiarid Agricultural Research Center, Embrapa Semiárido, Petrolina, PE (Brazil).
⁴ Brazilian Institute for Space Research, Remote Sensing Division, São José dos Campos, SP (Brazil).
⁵ Faculty of Agricultural Sciences, Agronomy Department, University of Córdoba, Montería (Colombia).
⁶ Corresponding author. mfpompelli@gmail.com

Received for publication: 13-01-2016 Accepted for publication: 14-05-2016

ABSTRACT

In this study, we investigated the different responses of Spondias tuberosa (umbu) trees, which grow in two different ecological life zones in northeast Brazil: tropical wet and tropical arid ecosystems. We evaluated the responses of plants grown under humid and dry conditions by measuring the photosynthesis, water status, fluorescence parameters, carbon isotopes and antioxidant system activity. The higher net photosynthesis values were recorded contemporaneously with the lower VPD values. The highest internal-to-ambient CO₂ concentration and the absence of typical changes in the fluorescence parameters suggested an onset of a nonstomatal limitation in the photosynthesis. Our results showed that umbu plants can adjust their antioxidant activity during the dry season as a defensive strategy against the deleterious effects of water stress. This evidence is supported by the observed modifications in the pigment concentrations, increased accumulation of hydrogen peroxide and malondialdehyde, high levels of electrolyte leakage, increased antioxidant activity, and decreased carbon isotope discrimination in the umbu trees during the dry season. Supported by multivariate analysis of variance, significantly effect of interaction between categorical “months of collect and location” predicts a strong “dry season effect” on our dataset. Taken together, our data show that umbu trees grown in a wet tropical environment are more susceptible to drought, as compared with their tropical arid counterparts.

Additional keywords: Caatinga, carbon isotope composition, global climate change, nonstomatal limitations, Umbuzeiro, water stress.

RESUMEN

En este trabajo se investigaron las respuestas de árboles de Spondias tuberosa (umbu), que crecen en dos zonas ecológicas del nordeste de Brasil: húmeda tropical y árida tropical. Se evaluaron las respuestas de las plantas con base en fotosíntesis, estado hídrico, parámetros de fluorescencia, isotopos de carbono y actividad del sistema antioxidante. Los altos valores de las tasas de fotosíntesis fueron correlacionados con bajos valores del DPV; los altos niveles de concentración interna de CO₂ y la ausencia de cambios típicos en los parámetros de fluorescencia, sugieren la aparición de una limitación no estomática de la fotosíntesis. Los resultados indicaron que las plantas de umbu pueden ajustar su actividad antioxidante durante la estación seca como una estrategia de defensa ante los efectos perjudiciales de un estrés por sequía. Esta afirmación está soportada por las modificaciones observadas en la concentración de pigmentos, incrementos en la acumulación de peróxido de hidrógeno y malondialdehido, altos niveles de electrolitos libres, incremento de la actividad antioxidante y decrecimientos en la discriminación isotópica del carbono en la localidad árida. El análisis de varianza multivariado mostró efectos significativos para la interacción “mes de colecta y localidad”, lo cual fue fuertemente predecible en la localidad. El análisis integral de los datos demostró que los árboles de umbu que crecieron en un ambiente húmedo tropical, son más susceptibles a la sequía, comparados con su contraparte de ambientes áridos tropicales.

INTRODUCTION

Water stress is an important factor that affects plant growth and yield, especially in the hot and seasonally wet-dry climates in the semiarid regions of the world (Ondrasek, 2014).

A combination of drought and excess light decreases the efficiency of photosynthesis and may also lead to leaf overheating, especially when the transpirational leaf cooling is reduced due to water deficits (Rizhsky et al., 2004; Rizhsky et al., 2002; Valladares and Pearcy, 1997).

Tropical plants growing under water stress exhibit modifications in photosynthetic processes, including disruptions in the stomatal control of the leaf gas exchange (Arcoverdeet al., 2011; Lawlor and Tezara, 2009; Lima Filho, 2007; Pompelli et al., 2010a; Santos et al., 2013), alterations in chlorophyll fluorescence kinetics (Faraloniet al., 2011; Maxwell and Johnson, 2000), damage to photosynthetic membranes (Krieger-Liszkay, 2005), changes in the carbohydrate status (Chimentiet al., 2002; Silva et al., 2010), and others. The water stress-induced limitation of net photosynthesis (P_N) may cause damage to the plant with exposure to excess irradiance; if this energy is not safely dissipated, it may cause an overreduction of the reaction centers and increased production of reactive oxygen species (ROS) in the chloroplasts, leading to photosystem PSII damage (Smirnoff, 1995).

Knowledge of species physiology in situ under arid/semiarid conditions may contribute significantly to our understanding of how to optimize productivity in trees under drought conditions in natural environments. Data regarding species physiology under arid conditions may also indicate how these species can be used in the regeneration of important regions undergoing desertification. In this context, we examined Spondias tuberosa Arruda (“umbuzeiro” or “umbu plant”), which is a small native tree that grows naturally among Caatinga vegetation throughout arid, semiarid and wet environments in northeastern Brazil, where it is adapted to survive under water stress conditions (Lins Netoet al., 2012). This tree is considered to be a species with great economic, social and ecological importance to the arid/semiarid northeast, Brazil (Lins Netoet al., 2010). At the end of the dry season, the umbuzeiro partially shed their leaves to avoid transpiration, reducing the plant’s growth rate, leaf initiation and leaf expansion during the drought, until the beginning of the first rains (Cavalcantiet al. 1996). During this period, the survival of the species is assured by a specialized root system bearing tubers (or xylopodia), whose function is to store water, soluble sugars, starch, minerals, and other solutes (Lins Netoet al., 2010). Old plants growing in their native fields can have more than 1,000 xylopodia, and their fresh weight can exceed 2,000 kg. These resources are used during the dry season to maintain normal plant metabolism (Cavalcanti and Resende, 2006; Lima Filho, 2001; Lima Filho, 2004).

There are few reports describing the physiological behavior of plants under arid conditions and their interactions with the environment (Campos et al., 2012; Cattivelli et al., 2008; Dombroski et al., 2011; Lima Filho, 2004). For example, Lima Filho (2004) observed that the environmental difference between the dry and rainy seasons is the primary factor that influences the course of gas exchange in umbu trees under semiarid conditions. Nevertheless, Lima Filho (2001) suggested that, under dry conditions, the diurnal water balance of the S. tuberosa would be maintained at the expense of water stored in the tubers and by restricted transpiration. In addition, Lima Filho (2007) also noted that the gas exchange of umbu plants with fewer tubers was more strongly affected than the gas exchange of plants with more tubers under water-stressed soil conditions. These investigators suggested that the root tubers may act as an important source of water under stress conditions. However, the aforementioned studies (Lima Filho, 2001; Lima Filho, 2004; Lima Filho, 2007) only describe the gas exchange of umbu trees under semiarid conditions and the importance of tubers in helping plants avoid stress.

In this study, we hypothesized that variations in the seasonal rainfall regime distinctly affect the ecophysiological plant performance in contrasting environments (wet and arid). It may affect the photoprotection and carbon gain and may also limit growth in S. tuberosa trees, mostly in plants grown in tropical wet regions, because the root mass fraction of well-watered trees is often reduced, as compared with that of waterstressed trees reducing the photosynthetic capacity (Poorter et al., 2012). Therefore, the main objective of this study was to evaluate the effects of the seasonal rainfall regime alterations on the plant physiological behavior for the gas exchange and photoprotection of S. tuberosa trees growing under wet and arid conditions in two regions of Bahia State, northeast, Brazil.

MATERIALS AND METHODS

Site description and experimental design

Water potential measurements

The leaf-water potential (Ψ_w) was measured using a Scholander-type pressure chamber (mod 3005F01; Soil Moisture Equipment Corp, Santa Barbara, CA). The measurements were taken in one leaf per plant at predawn (n=10).

Carbon isotope composition

From each experiment tree (n=5), one expanding leaf was collected in situ and it was oven-dried for 72 h at 70ºC. The isotope ratio, which was expressed as δ¹³C, was calculated as

where Rsample is the ¹³C/¹²C ratio in the sample and Rstandard is the ¹³C/¹²C ratio in the standard (PDB-Pee Dee Belemnite).

Leaf discs (1.4 cm in diameter) were collected in situ at 09:00-10:00 a.m. under clear-sky conditions, rapidly frozen in liquid nitrogen, and stored at -20ºC until analysis. Antioxidant enzymes, including superoxide dismutase (SOD; EC 1.15.1.1), catalase (CAT; EC 1.11.1.6) and ascorbate peroxidase (APX; EC 1.11.1.11), were assayed as described by Pompelli et al. (2010a). The H₂O₂ was analyzed according to Chen and Kao (1999). The Malondialdehyde (MDA) was determined following Cakmak and Horst (1991). The electrolyte leakage was assayed according to Campos et al. (2012).

The chlorophyll a+b and total carotenoids were extracted with 80% (v/v) aqueous acetone and quantified spectrophotometrically according to Pompelli et al. (2013). β-carotene, violaxanthin (V), antheraxanthin (A) and zeaxanthin (Z), were assayed by HPLC as reported by Ramalho et al. (1999).

Statistical analysis

The data were first analyzed by multivariate analysis of variance (MANOVA) with “month of collection and location” as categorical factors and using as dependent variables “photosynthetic” (P_N, E, g_s, C_i:C_a, WUE, T_leaf, VPD), “photochemical” (Φ_PSII, P, D, P_E) and “enzymatic” (SOD, CAT, APX, H₂O₂, MDA, electrolyte leakage) group in a GLM Bi-factorial MANOVA, for each variable. Since the interaction effect was highly significant according to the Wilks test in all of the performed analyses (P≤0.0001), the effective hypothesis decomposition was done with a one-way ANOVA, and the means were compared using Duncan’s or Student’s t test. All of the statistical tests were performed using the statistical software package Statistica version 10.0 (StatSoft, Tulsa, OK). The Lilliefors test was conducted to assess whether the experiment errors were normally distributed. As no transformation was needed, all of the statistical analyses were carried out on untransformed data. The results were considered to be significant when P≤0.05. Only the 8:00h data (when applicable) were used for the photosynthetic variable in MANOVA.

RESULTS

Gas exchange measurements

Annual fluctuations in the net photosynthesis (P_N), stomata conductance (g_s) and transpiration (E) were observed for the two populations. High variations throughout the day were observed, with a 7-fold difference between the extreme values (Fig. 2). The PN was always greater than 10 μmol CO₂ m-² s-¹ during the humid season, peaking at 17.4 μmol CO₂ m-² s-¹ for plants evaluated in April under wetter climate conditions. The P_N of the tropical arid plants was consistently lower than the P_N of the tropical wet plants. By means of all of the performed MANOVA, a strong interaction between the categorical variables “month of collect and location” notably pointed to a generalized “dry season effect” (November) and indicated that S. tuberosa plants have a differential behavior in wet and arid environments in this season. Consistent with this, the November measurements show that reductions in the P_N were stronger in the plants grown in the tropical humid environment than they for the tropical arid counterparts

(Fig. 2). From the humid to the dry season, the PN decreased by 84% and 34% in the tropical wet and tropical arid plants, respectively (figure 2), and the relationship between PN and gs was significantly positive (r = 0.753; P≤0.001). When only the dry season data were analyzed, the correlations were not significant (P=0.688), indicating circumstantially that gs could be a key factor in determining carbon uptake in a humid environment, but not in a dry one.

A negative relationship between the photosynthetic parameters and PAR (r = -0.421, -0.349, and -0.339 for P_N, E and gs, respectively; P≤0.05) was observed. During both seasons, the photosynthetic parameters differed significantly between the ecosystems, but these differences became stronger during the dry season (figure 2).

Figure 2

The P_N, E and g_s may have decreased because of a high vapor pressure deficit (VPD), as confirmed by their strong negative correlations (r = -0.809, -0.786, and -0.849 for PN, E and g_s, respectively; P≤0.0001).

In the tropical wet plants, the WUE was strongly reduced during the dry season but sharply recovered at the beginning of the rainy season (figure 3). A similar pattern was not observed for the WUE of the tropical arid plants, which remained constant throughout the year (figure 3). A 50% increase was verified in the C_i:C_a ratio during the dry season, as compared with the humid season in both populations (Fig. 3) circumstantially indicating a nonstomatal limitation of photosynthesis in this season. A high C_i:C_a was correlated with lower P_N and E values (r = -0.947 and -0.877, respectively; P≤0.0001) and a positive relationship (r = 0.828; P≤0.0001) between the C_i:C_a and δ¹³C was verified.

The predawn leaf water potential (Ψ_pd) was higher than -1.0 MPa during the entire study period, with the exception of November, when the lower values were observed in the plants grown in tropical wet. This result provides evidence that the trees experienced moderate to severe water stress (figure 3).

Chlorophyll fluorescence and quenching

The maximum efficiency of photosystem II (F_v:F_m ratio) showed significant differences (P≤0.05) between the dry and humid seasons (table 1). During the dry season, there was a small reduction in the Fv:Fm ratio at midday (table 1), with the lowest value found in the tropical wet environment at November. The F_v:F_m ratio (table 1), ΦPSII and P, followed similar trends (figure 4). All of these parameters in both ecosystems reached their minimum values during the dry season and the maximum values during the humid seas P = 0.015), but they were not correlated with the atmospheric temperature (P = 0.773). This finding indicates that plants that were exposed to a water shortage were capable of dissipating part of the excess energy as latent heat to minimize the water lost by transpiration (r = -0.946; P≤0.0001, between D and transpiration).

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Carbon isotope composition

Consistent with the dry season effect predicted by MANOVA’s performance, the plants grown in the tropical wet climate showed less enriched δ¹³C values, as compared with the tropical arid plants throughout the study period (figure 5), with exception of the data collected in November. During the rainy season, the δ¹³C ranged from -29.18 to -29.72‰ in the leaves of tropical wet plants and the value in the tropical arid leaves was approximately -28‰. During the dry season, the δ¹³C composition of the leaves from the tropical wet plants varied substantially (3.1‰); however, the composition of the leaves from the tropical dry plants did not vary substantially (0.6‰). The physiological responses to drought (figure 3) reflected the isotopic signature, or δ¹³C, of the leaves. A less negative isotopic signature was observed under the drought conditions (figure 5).

Biochemical analysis

The chlorophyll content of the tropical wet plants was similar to that of the tropical arid plants; however, the minimum chlorophyll content in both climates was observed at the end of the water deficit period (November), with the tropical arid plants showing a higher concentration than their tropical wet counterparts (table 2). Independent of the locations, the water shortages led to a reduction in the total chlorophyll (~17%).

The β -carotene, antheraxanthin and zeaxanthin concentrations showed similar fluctuations, with gradual increases from July to November and a decrease in April in the next year. Significant correlations between Z and D (r = 0.558; P≤0.0001) and between VAZ and D (r = 0.557; P≤0.0001) ratios were shown during the year. For example, the thermal energy dissipation and D were associated with increased levels of de-epoxidated forms of A and Z within the VAZ cycle (table 2) in November.

DISCUSSION

The current study provides a seasonal profile of the daily photosynthetic performance of S. tuberosa trees grown under wet and arid conditions in natural environments. In general, the umbu plants grown in the tropical wet environments showed a differential behavior mainly at drought when compared to the tropical arid environment with the same stress. The multivariate and physiological analysis points to higher susceptibility to drought for the tropical wet plants. In all of the plants, the diurnal course PN, g_s, and E values were maximal during the midmorning and decreased in the afternoon and those parameters did not respond toan elevated light stimulus, most likely because Tleaf and VPD were increased (figure 2). It is possible that these environmental factors may have somehow affected the stomatal functioning during the day although we cannot rule out the effect of endogenous factors related to the activity of the circadian rhythm in modulating stomatal functioning and PN (Mendes and Marenco, 2014). The effect of VPD on PN, g_s, and E showed that changes in intensity of light can alter the performance of the photosynthetic apparatus over the course of a day irrespective of the seasonal rainfall regime. In this study, we showed that, during the period when the water stress was most severe, i.e., November, the photosynthetic rates of the tropical arid plants were significantly higher than the rates in the tropical wet plants, an effect that was strongly shifted at the beginning of the rainy season, which is the opposite to what should be expected for trees growing in a wet environment. Some investigators previously reported that S. tuberosa can maintain its Ψ_pd at a relatively constant level during the beginning of the dry season (Lima Filho, 2001; Lima Filho, 2004; Lima Filho, 2007; Lins Netoet al., 2012). A possible explanation for this result is that the umbu tree reduces its stomatal conductance in response to drought early in the morning, resulting in a dramatic decline in plant water loss and assuring significant water storage in the tubers (Lima Filho and Silva, 1988). However, as the water in the soil decreases, which leads to reduced water storage in the tubers, both E and gs substantially decrease as a function of Ψ_pd (Lima Filho, 2004; Silva et al., 2008). S. tuberosa root tubers can serve as water storage vessels, and a higher root mass fraction, lower leaf masses and lower total leaf areas are observed in arid environments (Araújo et al., 2009; Lima Filho, 2004; Poorter et al., 2012), which may help the plants to perform better in droughts. These factors may play a substantial role in the amount of water supplied via tubers and the level of water conservation in leaves to maintain a higher PN under an extreme drought. Despite greater volume of rains in October and November in the arid environment, all of the analyses were done after the rains in both locations throughout the year, excluding small variations of monthly accumulated rainfall as shown in figure 1 A and allowing us to explore physiological patterns for seasonal fluctuation. Additionally, it is plausible to speculate that plants growing in areas with a lower water content throughout the year may have xylem vessels with lower diameters, as this represents an important mechanism for avoiding cavitation under extreme droughts (Nardini et al., 2014; Silva et al., 2013), while also restricting water flow when water is plentiful. The annual profile of leaf transpiration (figure 2E), which was focused on the morning period when the stomata are wide open, corroborates this proposition.

In the present study, the E was strongly affected by the VPD associated with a high temperature and high solar radiation, especially during the dry season (figure 2). The increased VPD led to an increase in transpiration, leading to evaporative leaf cooling due to latent heat loss if water was available. This is in agreement with results reported by others (Passos et al., 2009; Santos et al., 2013). If water was not available, a high irradiance (figure 2A), particularly during drought, may have been related to the extremely high leaf temperatures (figure 2B).

An increase in C_i due to stress could occur in response to low photosynthetic activity (Singh and Reddy, 2011); however, this is not a universal response. Stomatal closure typically leads to a decrease in C_i, thereby leading to a decrease in the C_i:C_a ratio. The decreased _Ci indicates that stomatal limitations are dominant under moderate but not in severe drought, as observed in tropical wet plants evaluated in November (Fig. 3B). At this time, the umbu leaves showed high C_i:C_a ratios with a low P_N, which indicates that there is a limitation of carbon uptake imposed by nonstomatal factors. The dry season had a detrimental effect on the Rubisco activity or ATP synthesis; moreover, under progressive droughts, the mesophyll conductance (gm) may decline (Flexas and Medrano, 2002; Lawlor and Tezara, 2009). This allows us to conclude that the nonstomatal limitation likely occurred along with the potential limitation of conductance of the mesophyll, which together must have accounted for the PN decreases during the driest months (Ni and Pallardy, 1992; Silva et al., 2010).

When the photochemical quenching was reduced, the non-photochemical energy quenching (D and P_E) was increased (figure 4). The deconvolution of fluorescence signals clearly indicates decreases in the photochemical quenching parameters and damage to PSII. The lower extent to which PSII uses the energy absorbed by chlorophyll in photochemical reactions and the increase in non-photochemical signals suggests that trees grown in wet, tropical environments are damaged by excess light under droughts. The lower F_v:F_m (md) values (table 1) and the larger D and smaller ΦPSII values (figure 4) observed throughout the year in trees grown in wet environments and subsequently exposed to drought conditions (i.e., in November) supports this conclusion.

The decreased P values were not entirely offset by the increased D during the dry season, leading instead to a higher P_E. The increased P_E suggests that the down-regulation of PSII to prevent the over-reduction of QA was not sufficient to compensate for the decreased demand for electrons through NADP⁺ consumption (Chaves et al., 2008; Pompelli et al., 2010b; Ramalho et al., 1999). This outcome may in turn result in singlet oxygen formation and damage to membrane components, similar to that which occurs during light stress (Takahashi and Badger, 2011).

As the drought progressed and soil water content declined, the δ¹³C increased and became less negative, with values lower than -27.2‰, suggesting a carbon limitation induced by water limitation (Schifman et al., 2012), as reported in this study (figure 5). The less negative values of δ¹³C in the tropical arid plants indicated that the water status was generally lower, with a consequent increase in the stomatal closure and some degree of CO₂ restriction in photosynthesis during the humid months. The opposite situation during the driest month (November) indicates that the tropical wet plants experienced greater restriction of CO₂ influx than the tropical arid plants

The high carotenoid-to-Chl ratios during the dry season (table 2), particularly in leaves from the wet environments, may help the leaves to avoid photooxidative processes because, in addition to their role as secondary light-absorbing pigments, the carotenoids prevent the photooxidation of the photosynthetic apparatus by reducing the Chl triplet quencher, preventing the formation of singlet oxygen (¹O₂), or by acting directly on ¹O₂ scavengers (Krieger-Liszkay 2005). These mechanisms may help to protect the plants, but they are not always sufficient to prevent photodamage in dry leaves.

Plants subjected to water stress tend to overproduce ROS in different tissues (Carvalho, 2008), and antioxidant enzymes constitute an important line of cellular defense, detoxifying ROS compounds. However, we showed that the increases in the CAT and APX activities during the dry season were not enough to dissipate the excess, reducing the power accumulated in the H₂O₂ that was generated from the water-water cycle or in the SOD activity. In November, the driest month, the H₂O₂ and MDA levels were as high as they were in September, despite the increased activity of the enzymes in the antioxidative system. Although there were increases in the H₂O₂, MDA and antioxidant enzymes levels, our results showed that S. tuberosa plants have the ability to increase their antioxidant activity during the dry season (figure 6) as a defense strategy against the deleterious effects, indicating that APX plays a positive role in the response to water stress. However, this mechanism is not robust enough to prevent damage. We attribute the improved drought tolerance of S. tuberosa plants that were grown in the arid environment to the combination of high leaf Ψ_w, higher g_s and E, and evaporative leaf cooling that allow for the maintenance of a constant leaf temperature. The likely outcome is an increased net CO₂ influx and elevated P and Φ_PSII with an efficient sink for electrons from photosynthesis, thus preventing ROS production and reducing cellular oxidative damages. Our data do not indicate that modestly increased carotenoid pools can serve as an effective antioxidant system.

Conclusions

P_N and g_s in S. tuberosatrees appear to be highly sensitive to diurnal variations, and even when the photosynthetic parameters are affected by environmental factors (e.g., light and VPD), the stomatal response to a water deficit suggests that stomatal closure is the first line of defense against desiccation in umbu trees. Furthermore, the over-excitation of the reaction centers of PSII during the dry season may increase ROS production in various subcellular organelles, such as chloroplasts and peroxisomes. Although the physiological profile of S. tuberosa characterizes it as a drought tolerant species the P_N, g_s and E in the plants of the tropical wet population are likely to be limited by the water deficit during the dry season, unlike the umbu plants of the arid population. Such species, when growing under low water conditions, can acclimate to this abiotic stress and are able to survive subsequent drought periods with less damage, as compared with plants from tropical wet regions.

Finally, our results suggest that this species has great potential to acclimate to the altered environment predicted for arid/semiarid regions as a result of climate changes. However, further studies are needed to determine the effects of a prolonged dry season on S. tuberosa plants and to develop strategies to mitigate these effects.

Acknowledgements

The authors would like to thank the National Council for Scientific and Technological Development, CNPq (Grants 473202/2008-5) and the Foundation for Science and Technology of Pernambuco (Grants APQ-0150-2.03/08) for their financial support of this research.

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