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Proline and antioxidant enzymes protect Tabebuia aurea (Bignoniaceae) from transitory water deficiency

Abstract

Water deficiency is a major abiotic stress that limits biomass production and drives plant species distributions. We evaluate the effects of water deficiency on ecophysiological and biochemical parameters of seedlings of Tabebuia aurea. Plants were subjected to daily watering (control) and to stress by soil water deficiency for 29 days. Leaf area, plant biomass, gas exchange, SPAD index, maximum quantum yield (Fv / Fm ), quantum yield of PSII (ΦPSII), superoxide dismutase (SOD) and L-ascorbate peroxidase (APX) activity, lipid peroxidation, and proline content were recorded. Plants responded to water deficit by reducing leaf area and accumulating proline. Stomatal conductance was reduced to limit the water loss by transpiration. However, limiting CO2 uptake caused reduction in photosynthesis and biomass. The excess of energy unutilized by photosynthesis reduced SPAD index and ΦPSII. As a result, we observed an increase in SOD and APX activity, protecting chloroplast membranes from further damages caused by lipid peroxidation. Our results indicate that T. aurea have capacity to survive under water deficiency reducing stomatal aperture, but affecting the rate of CO2 assimilation. Nevertheless, plants showed mechanisms to preventing damages to the photosynthetic apparatus. Such plasticity is an important adaptation for plants growing in dry environmental.

Key words
antioxidant system; gas exchange; tree species; water deficit; proline

Resumo

A deficiência hídrica é um importante estresse abiótico que limita a produção de biomassa e dirige a distribuição de espécies vegetais. Nós avaliamos os efeitos da deficiência hídrica sobre parâmetros ecofisiológicos e bioquímicos de plantas jovens de Tabebuia aurea, uma espécie arbórea nativa da “Caatinga”, um bioma semiárido. Plantas foram submetidas à irrigação diária (controle) e ao estresse promovido por deficiência de água no solo por 29 dias. A área foliar, biomassa da planta, trocas gasosas, índice SPAD, rendimento quântico máximo (Fv / Fm ) efetivo do PSII (ΦPSII), atividade da superóxido dismutase (SOD) e L-ascorbato peroxidase (APX), peroxidação lipídica e teores de prolina foram determinados. As plantas responderam ao estresse hídrico reduzindo a área foliar e acumulando prolina. A condutância estomática também foi reduzida limitando a perda de água por transpiração. Contudo, a limitação da absorção de CO2 causou reduções nas taxas fotossintéticas e na biomassa. O excesso de energia não utilizada pela fotossíntese provocou uma redução no índice SPAD e em ΦPSII. Como resultado, nós observamos um aumento nas atividades de SOD e APX, protegendo as membranas dos cloroplastos de danos causados pela peroxidação de lipídeos. Nossos resultados indicam que T. aurea tem capacidade de sobreviver sob deficiência hídrica reduzindo a abertura estomática, mas afetando a taxa de assimilação de CO2. Apesar disso, as plantas mostraram mecanismos de prevenção de danos ao aparato fotossintético. Tal plasticidade é uma importante adaptação para plantas crescendo em ambientes semiáridos como a Caatinga.

Palavras-chave
sistema antioxidante; trocas gasosas; espécies arbóreas; deficiência hídrica; prolina

Introduction

Adaptations to water deficiency is crucial for plants growing in semi-arid environments such as the Caatinga biome of Northeastern Brazil, a seasonally dry tropical forest that has been severely degraded by human activities (Da Silva et al. 2017Da Silva JMC, Leal IR & Tabarelli M (2017) Caatinga: the largest tropical dry forest region in South America. Springer International Publishing, Cham. Pp. 281-333.). Like many semi-arid regions, climate change is exacerbating droughts in the Caatinga (Torres et al. 2017Torres RR, Lapola DM & Gamarra NLR (2017) Future climate change in the Caatinga. In: Da Silva JMC, Leal IR & Tabarelli M (eds.) Caatinga: the largest tropical dry forest region in South America. Ed. Springer International Publishing, Cham. Pp. 359-368.), leading to increasingly harsh conditions for the native vegetation (Acosta-Salvatierra et al. 2017Acosta-Salvatierra LH, Ladle RJ, Barbosa H, Correia RA & Malhado AC (2017) Protected areas buffer the Brazilian semi-arid biome from climate change. Biotropica 49: 753-760.). Increased knowledge about plant responses to water deficiency is crucial for understanding the impacts of climate change and for the restoration of the Caatinga.

Trees growing in the semi-arid face a difficult trade-off between reducing water loss and growth under drought conditions. Specifically, if they close stomata to reduce transpiration, then less CO2 will be available for photosynthesis and biomass accumulation will be reduced (Barros et al. 2020Barros V, Melo A, Santos M, Nogueira L, Frosi G & Santos MG (2020) Different resource-use strategies of invasive and native woody species from a seasonally dry tropical forest under drought stress and recovery. Plant Physiology and Biochemistry 147: 181-190.). The capacity to survive and grow under conditions of limited water availability is therefore critical for semi-arid vegetation and is a major driver of plant species distributions (Bykova et al. 2019Bykova O, Chuine I & Morin X (2019) Highlighting the importance of water availability in reproductive processes to understand climate change impacts on plant biodiversity. Perspectives in Plant Ecology, Evolution and Systematics 37: 20-25.).

In addition to stomatal closure, plants show a plethora of physiological mechanisms to tolerate periods of water deficit, resulting in alterations in gas exchange, chlorophyll index and chlorophyll a fluorescence (Silva-Pinheiro et al. 2016Silva-Pinheiro J, Lins LKS, Souza FC, Silva CEM, Moura FBP, Endres L & Justino GC (2016) Drought-stress tolerance in tree semi-arid species used to recover logged area. Brazilian Journal of Botany 39: 1031-1038.). Morphological adjustments are also an important strategy to adapt to water scarcity, which can last up to nine months of the year, in “Caatinga” (Da Silva et al. 2017Da Silva JMC, Leal IR & Tabarelli M (2017) Caatinga: the largest tropical dry forest region in South America. Springer International Publishing, Cham. Pp. 281-333.). Moreover, drought episodes occur in parallel with high temperatures and light intensities further contributing to the physiological challenges of life in semi-arid ecosystems (Souza et al. 2010Souza BD, Meiado MV, Rodrigues BM & Santos MG (2010) Water relations and chlorophyll fluorescence response of two leguminous trees from the “Caatinga” to different watering regimes. Acta Physiologiae Plantarum 32: 235-244.). During the dry season increasing vapor pressure deficit (VPD) increases soil water deficit, negatively affecting plant development (Queiroz et al. 2019Queiroz MG, Silva TGF, Zolnier S, Souza CAA, Souza LSB, Steidle AJN, Araújo GGL & Ferreira WPM (2019) Seasonal patterns of deposition litterfall in a seasonal dry tropical forest. Agricultural and Forest Meteorology 279: 107712.). This is because both soil and atmosphere moisture are involved in stomatal responses to water deficiency (Tominaga et al. 2014Tominaga J, Inafuku S, Coetzee T & Kawamitsu Y (2014) Diurnal regulation of photosynthesis in Jatropha curcas under drought during summer in a semi-arid region. Biomass & Bioenergy 67: 279-287.; Barros et al. 2020Barros V, Melo A, Santos M, Nogueira L, Frosi G & Santos MG (2020) Different resource-use strategies of invasive and native woody species from a seasonally dry tropical forest under drought stress and recovery. Plant Physiology and Biochemistry 147: 181-190.). Plants may also reduce their leaf area in response to water deficit, probably as an additional strategy to prevent excessive loss of water (Silva-Pinheiro et al. 2016Silva-Pinheiro J, Lins LKS, Souza FC, Silva CEM, Moura FBP, Endres L & Justino GC (2016) Drought-stress tolerance in tree semi-arid species used to recover logged area. Brazilian Journal of Botany 39: 1031-1038.).

As mentioned above, high radiation levels and water deficiency occur simultaneously, and may cause damage to the thylakoid membranes, impairing the electron transfer in photosystem II (Deng et al. 2018Deng Y, Jia X, Sun X, Liang L & Su J (2018) Comparison of jasmine antioxidant system responses to different degrees and durations of shade. Acta Physiologiae Plantarum 40: 41.). Some plants respond to these conditions by dissipating excess of absorbed light energy as heat. However, this mechanism may fail if plants are submitted to low water availability (Santos et al. 2013Santos CM, Verissimo V, Wanderley Filho HCL, Ferreira VM, Cavalcante PGS, Rolim EV & Endres L (2013) Seasonal variations of photosynthesis, gas exchange, quantum efficiency of photosystem II and biochemical responses of Jatropha curcas L. grown in semi-humid and semi-arid areas subject to water stress. Industrial Crops and Products 41: 203-213.).

Plants may also respond to water deficiency by accumulating compatible solutes and by activating their antioxidant system. These mechanisms contribute to maintaining plant cell turgor and protecting the integrity of the membranes (Nounjan et al. 2018Nounjan N, Chansongkrow P, Charoensawan V, Siangliw JL, Toojinda T, Chadchawan S & Theerakulpisut P (2018) High performance of photosynthesis and osmotic adjustment are associated with salt tolerance ability in rice carrying drought tolerance QTL: physiological and co-expression network analysis. Frontiers in Plant Science 9: 1135.). The antioxidant system also protects against the toxic effects of reactive oxygen species (ROS) as O2− and H2O2 (Martins et al. 2018Martins K, Brito POB, Arruda JF, Nunes FHJ, Pontes RAF & Gondim FA (2018) Plant growth, antioxidative enzymes, lipid peroxidation and organic solute contents in mulungu seedlings (Erythrina velutina) under different field capacities. Journal of Agricultural Science 10: 443-454.) and includes enzymes such as superoxide dismutase (SOD) and L-ascorbate peroxidase (APX) functionally scavenging ROS (Sharma et al. 2012Sharma P, Jha AB, Dubey RS & Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012: 217037.).

Studies of plant physiological responses to short (transitory) episodes of water deficiency are important to understand how drought-adapted plants deal with carbon assimilation and biomass distribution among shoots and roots during conditions of low soil water availability. This information is crucial for Caatinga conservation, since effective restoration of this highly degraded biome will depend upon detailed knowledge of the physiological tolerances and ecology of native plant species. Tree species are particularly important in this respect because they act as ‘nurse plants’ for many other species, facilitating the growth and reproduction of other native species (Moura et al. 2013Moura FBP, Malhado ACM & Ladle RJ (2013) Nursing the Caatinga back to health. Journal of Arid Environments 90: 67-68.).

Tree seedlings are usually used to recover degraded areas subject to water deficiency. The ability to tolerate water scarcity in the early stages of development is the key characteristic for choosing plant species for the recovery of degraded lands (Vieira et al. 2017Vieira AV, Silva MG, Moro CF & Laura VA (2017) Physiological and biochemical changes attenuate the effects of drought on the Cerrado species Vatairea macrocarpa (Benth.) Ducke. Plant Physiology and Biochemistry 115: 472-483.). One of the most promising tree species for restoration projects is the drought tolerant Tabebuia aurea (Silva Manso) Benth. & Hook.f. ex S.Moore (Bignoniaceae), which is widely distributed in tropical and subtropical regions of the Americas (Lorenzi 1992Lorenzi H (1992) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brazil. Instituto Plantarum, Nova Odessa. 46p. ). Previous studies have indicated that leaf water potential of T. aurea rapidly recovers after a short-term stress provoked by water deficiency. Specifically, Silva-Pinheiro et al. (2016)Silva-Pinheiro J, Lins LKS, Souza FC, Silva CEM, Moura FBP, Endres L & Justino GC (2016) Drought-stress tolerance in tree semi-arid species used to recover logged area. Brazilian Journal of Botany 39: 1031-1038. subjected plants to water deficit by suppressing irrigation until photosynthesis reached zero, and then plants were re-watered until carbon assimilation rates reached those values of irrigated plants. They recorded that plants supported an average of about -4.0 MPa of leaf water potential, indicating considerable capacity to adapt to water scarcity conditions.

Here, we investigate the physiological response of T. aurea to short-term water deficiency (29 days) under greenhouse conditions. Specifically, we focus on the effects of water deficiency on gas exchange, dissipation of energy, proline accumulation and the antioxidant system. We aimed to assess the responses of plants after a controlled period of water deficit, not submitting individuals to total drought. Our results have direct for the effective use of T. aurea for the restoration of degraded areas of the semi-arid Caatinga biome.

Material and Methods

Experimental site and plant material

We collected seeds of Tabebuia aurea from a seasonally dry tropical forest region known as “Caatinga” (09°21’49’’S, 37º14’54’’W). Seeds were initially germinated in soil in plastic trays. We selected 18 apparently healthy seedlings and transferred them into 25 L plastic pots (one plant per pot) containing 20 kg of soil. The soil was collected from an area located at the Agricultural Science Center (Federal University of Alagoas). The soil was characterized as sand = 674 g Kg-1, (26% thin sand and 74% thick sand), clay = 296 g Kg-1 and silte = 30 g Kg-1, as medium texture soil. The main chemical elements were P = 207 mg dm-3, K = 3.6 mg dm-3, Ca2+ = 41 cmolc dm-3, Mg2+ = 13 cmolc dm-3, MO = 25 dag Kg-1.

The experiment was performed under greenhouse conditions at the Federal University of Alagoas, Brazil (09°28’02”S, 35°49’43”W). Microclimatic data was recorded by an automatic weather station (WS - GP1, Delta-T Devices, Cambridge, England) installed inside the greenhouse (data shown in Fig. 1a-b). The mean temperature during the experiment was 30.29 ºC, the mean relative humidity and radiation was 68.92% and 569 μmol m2 s-1 respectively, and the mean VPD was 1.61 KPa.

Figure 1
a-b. Greenhouse microclimatic data during the experiment – a. temperature (ºC) and relative humidity (%); b. radiation (photosynthetically active radiation - PAR) (µmol m-2 s-1) and vapour pressure deficit - VPD (KPa). Each point (day) represents a mean of 24 measurements (hour-hour).

Six month-old plants were subjected to two treatments, with nine replicates each: (1) control: plants daily irrigated to field capacity; (2) stress: plants subjected to controlled water deficit maintained at soil water potential (Ψwsoil) below -1.5 MPa (Fig. 2) for 29 days. The analysis started when the water potential of the soil reached values equal to or below 1.5 MPa. The maintenance of the water potential was performed with the replacement of the water lost daily. For this purpose, pots were weighed daily with the use of a semi-analytical balance in order to replace the water lost by evapotranspiration. The Ψwsoil was measured daily using a WP4C - Dew Point Potential Meter (Decagon Devices, Pullman, USA) with soil samples collected through a PVC tube inserted in each pot at a depth of 10 cm, based on previous studies of Silva-Pinheiro et al. (2016)Silva-Pinheiro J, Lins LKS, Souza FC, Silva CEM, Moura FBP, Endres L & Justino GC (2016) Drought-stress tolerance in tree semi-arid species used to recover logged area. Brazilian Journal of Botany 39: 1031-1038..

Figure 2
Soil water potential (Ψwsoil) of Tabebuia aurea soil under water deficit during the experiment. The arrow indicates the day when plants reached Ψwsoil below -1.5 MPa (first day of the experiment). * means significance at P < 0.05 between treatments using the t test. n = 9.

Dry mass, number of leaves, leaf area, leaf water status, gas exchange, relative chlorophyll content, and photochemical efficiency of photosystem II (PSII) were measured 29 days after the imposition and maintenance of treatments. We also collected leaf material to quantify the levels of soluble proteins, proline, the activity of the antioxidant enzymes SOD and APX and malondialdehyde-equivalents (MDA).

Dry mass accumulation and leaf area

Dry mass was measured with a semi-analytical balance AD3300 (Marte Científica, Santa Rita do Sapucaí, Brazil) after sectioning and drying stems, leaves and roots for three days at 65 ºC in a forced air oven . Leaf area was determined using a Leaf Area Meter LI-3100C (LI-COR, Richmond, New Zealand).

Gas exchange measurements

Leaf gas exchange was evaluated between 08:00 and 10:00 a.m. using an infrared CO2 gas analyzer model Li-6400XT (LI-COR, Lincoln, USA). Photosynthetic rate (A), transpiration rate (E) and stomatal conductance (gs) were determined for healthy, fully expanded leaves from the middle of the plant using the following settings: 1000 µmol m-2 s-1 photosynthetic photon flux density (determined through a light curve), we used a buffer volume to dampen fluctuations in concentration of atmospheric CO2, block temperature 27 ºC. Water use efficiency (instantaneous - iWUE and intrinsic - IWUE) was calculated as A/E (iWUE) and A/gs (IWUE).

Photochemical efficiency of photosystem II (PSII), relative chlorophyll content (SPAD index) and leaf water status

Quantum yield of PSII (ΦPSII) was evaluated at midday with a fluorometer PAM-2500 (Walz Heinz GmbH, Effeltrich, Germany). The maximum quantum yield of PSII (Fv / Fm ) was also determined at midday using a saturation pulse of actinic light (8000 µmol m-2 s-1) during one second to promote PSII reaction center closing, following Maxwell & Johnson (2000)Maxwell K & Johnson GN (2000) Chlorophyll fluorescence: a pratical guide. Journal of Experimental Botany 51: 659-668.. The readings of Fv / Fm began 20 min after leaf adaptation to darkness, using special clips. We determined relative chlorophyll content (SPAD index) using a portable chlorophyll meter SPAD-502 (Minolta, Plainfield, USA). Leaf water potential (Ψwleaf) was used to verify plant water status and was measured using a pressure chamber (SoilMoisture Equipment, Santa Bárbara, USA) (Scholander et al. 1965Scholander PF, Hammel HT, Hemingsen EA & Bradstreet ED (1965) Hydrostatic pressure and osmotic potentials in leaves of mangroves and some other plants. Proceedings of the National Academy of Sciences of the United States of America 51: 119-125.) at predawn and midday. All measurements were made on the same leaves that were used to evaluate gas exchange.

Biochemical analyses

We collected leaf samples and immediately stored them at -80 °C until analysis. Proline was extracted from lyophilized leaves and determined according to Bates et al. (1973)Bates LS, Waldren RP & Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207.. Acid ninhydrin solution was prepared by heating 1.25 g of ninhydrin in 20 mL of 6 M phosphoric acid and 30 mL of glacial acetic acid with continuous stirring until mixture was completely homogenized. We mixed 0.1 g of triturated leaf with 118 mM sulfosalicylic acid. Homogenized samples were centrifuged at 3000 g for 10 min at a temperature of 25 ºC, and the supernatant was used for subsequent analysis. Absorbance was read at wavelength of λ = 520 nm by using toluene blank and standards of known concentration of proline.

SOD activity was measured following the method described by Giannopolitis & Ries (1977)Giannopolitis CN & Ries SK (1977) Superoxide dismutases: occurrence in higher plants. Plant Physiology 59: 309-314.. 300 mg of fresh weight leaves were homogenized in a mortar by using liquid N2 with polyvinylpyrrolidone (PVP) and extracted with pH 7.8 phosphate buffer. The assay was carried out using the following reaction mixture: 50 mM potassium phosphate buffer (pH 7.8), 100 nM ethylenediaminetetracetic acid (EDTA), 75 mM nitro blue tetrazolium (NBT), 13 mM methionine and 2 mM riboflavin and 50 µL of plant extract. Subsequently, the homogenate was centrifuged at 14.000 g for 15 min at 4 °C. After this step, the reaction mixture was exposed to white light for 10 minutes and absorbance was measured at 560 nm. SOD activity of the extract was expressed as SOD mg-1 protein.

The activity of APX was determined following Nakano & Asada (1981)Nakano Y & Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-especific peroxidase in spinach choloroplasts. Plant and Cell Physiology 22: 867-880. with some modifications. The extract was obtained from 100 mg of fresh leaf material homogenized in 2 mL of the extraction mixture, composed by deionized water, 50 mM monobasic potassium phosphate (pH 7.5) buffer, 20 mM ascorbate, 0.1% Triton-x 100, 0.2 mM EDTA, and 300 mg of PVP, with liquid N2. Subsequently, the homogenate was centrifuged at 14.000 g for 15 min at 4 °C and the supernatant was used for determination of APX activity. Then, 75 µL of homogenate was added to a reaction mixture containing deionized water, 50 mM monobasic potassium phosphate (pH 7.5) buffer, 0.5 mM ascorbate and 0.05 mM hydrogen peroxide. Absorbances were measured for one minute at 290 nm and the extinction coefficient used for ascorbate was 2.8 mM-1cm-1 at 290 nm. Results were expressed as APX min-1 mg-1 protein. Total protein concentration was determined by the method of Bradford (1976)Bradford MM (1976) A rapid and sensitive method for the qualification of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72: 248-254. using bovine serum albumin (Sigma Chemical Company) as a standard.

Lipid peroxidation in leaf tissues was measured according to method described by Cakmak & Horst (1991)Cakmak I & Horst J (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum 83: 463-468.. Grounded leaves (100 mg of fresh leaf) were homogenized using a pestle and mortar with liquid N2 and 4 mL of trichloroacetic acid (TCA) 0.1% w/v. Subsequently, the homogenate was centrifuged at 15.000 g for 15 minutes at 4 °C. Malondialdehyde-equivalents (MDA) quantification was as follows: 1.5 mL of the thiobarbituric acid solution (0.5% TBA made in 20% TCA) was added to homogenate that was heated for 5 minutes at 95 °C. The concentration of MDA was calculated from the absorbance of 530 nm by using the extinction coefficient of 155 Mm-1 cm-1 and was expressed as nmol g-1 FW.

Statistical analysis

Data from different treatments were compared using T test (P < 0.05). Was used 9 (nine) replicates in the analysis of gas exchange, biomass, leaf area, number of leaves, Ψwleaf, SPAD Index, Fv / Fm and ΦPSII. Was used 8 (eight) replicates for proline content analysis and 5 (five) replicates in MDA, APX and CAT analysis. We used Pearson’s correlation analysis to investigate possible correlations between Ψwleaf, proline content, Ψwsoil, SPAD Index, ΦPSII, Fv / Fm , SOD, APX, MDA, A, gs and E in each treatment, using software R (R Development Core Team 2020R Development Core Team (2020) R: a language and environment for statistical computing, reference index version 3.6.3. R Foundation for Statistical Computing, Vienna. Available at <https://www.r-project.org/>. Access on 29 February 2020.
https://www.r-project.org/...
) 3.4.3. Photochemical, biochemical and gas exchange parameters were subjected to a principal component analysis (PCA) using Past3 software. Pearson’s correlation and PCA analysis were made with 5 (five) replicates from each variable. We used SigmaPlot (free trial) to plot graphics.

Results

Plant morphology and Gas exchange

On the 29th day after the suspension of irrigation, significant effects of water regimes on T. aurea biomass were detected. The leaf dry mass of plants under water deficit was 38% lower than the control (P = 0.004) and stem (P = 0.0002) and root (P = 0.003) dry mass was 29% lower than the control (Fig. 3a). No significant differences were observed for the root: shoot ratio between treatments (P = 0.3) (Fig. 3b). Leaf area and number of leaves were 31% lower in plants under water deficit than in the control (P = 0.03) (Fig. 3c,d). The rate of stomatal conductance (gs ) was reduced by 91% in plants under water deficit (P = 0.000005), affecting transpiration by 90% reduction (P = 0.000004) and photosynthesis by 85% reduction (P = 0.000001) (Tab. 1). We observed a positive correlation between gs and A (r = 0.90 *) (Tab. 2). The iWUE had an increase of 52% (P = 0.002) and IWUE increased 76% (P = 0.002) in plants under water deficit (Tab. 1).

Figure 3
a-d. Tabebuia aurea seedlings under two water regimes: control and water deficit – a. biomass; b. root : shoot ratio; c. leaf area; d. number of leaves. * means significance at P < 0.05 between treatments by T test; ** mean significance at P < 0.01, ns = not significant. n = 9.
Table 1
Stomatal conductance (g s), transpiration (E), photosynthesis (A), instantaneous water-use efficiency (iWUE) and intrinsic water-use efficiency (IWUE) of Tabebuia aurea seedlings under two water regimes: control and water deficit.
Table 2
Pearson’s correlation coefficients between physiological and biochemical variables of Tabebuia aurea submitted to two water regime (control and water deficit): Ψwleaf, proline (Pro), Ψwsoil, SPAD Index (SPAD), F v / F m, SOD, APX, MDA, A, g s and E. Up-right diagonal refers to the control treatment and down-left diagonal refers to the water deficit treatment. n = 5.

Photochemical efficiency of photosystem II & relative chlorophyll content

On the 29th day, the SPAD index was 8% lower in plants under water deficit (P = 0.03), though Fv / Fm did not differ significantly between this treatment and the control (P = 0.41). ΦPSII was impaired by water deficit, with reductions of around 48% (P = 0.001) (Fig. 4). Furthermore, we found positive correlation between Fv / Fm and the SPAD index (r = 0.90 *) (Tab. 2).

Figure 4
a-c. Tabebuia aurea seedlings under two water regimes: control and plants under water deficit – a. SPAD index; b. Fv / Fm ; c. ΦPSII. * means significance at P < 0.05 between treatments by T test and ** means significance at P < 0.01, ns = not significant. n = 9.

Leaf water potential & proline content

Ψwleaf values decreased significantly after the reduction in soil water potential. Predawn Ψwleaf levels were around -0.7 MPa in control plants and -1.7 MPa in plants under water deficit (Fig. 5a). At midday, Ψwleaf declined to -2.9 MPa in plants under water deficit and to -0.9 MPa in control plants. Leaf proline content did not differ between treatments at the predawn. By midday the leaf of the plants under water deficit showed significant increase of proline of 69% when compared to the control, both lyophilized before analysis (Fig. 5b). We observed an inverse correlation between proline and Ψwleaf (r = -0.89 *) and APX (r = -0,88 *) in plants under water deficit (Tab. 2).

Figure 5
a-b. Tabebuia aurea seedlings under two water regimes: control and plants under water deficit, at predawn (5–6 a.m. before sunrise) and at midday (12 p.m.) – a. leaf water potential (Ψwleaf); b. leaf proline content. * means significance at P < 0.05 between treatments by T test and ** means significance at P < 0.001, ns = not significant. n = 9 for Ψwleaf, n = 8 for proline content.

Concentration of antioxidant enzymes

The indicative values ​​of the concentration of SOD did not differ between control and water deficit treatments at predawn, but had increased significantly (61%) at midday in plants under water deficit. In contrast, the results obtained from APX was higher at predawn (28% higher) than at midday (24% higher) in plants under water deficit. MDA content in leaves was not affected by water deficiency (Fig. 6). However, MDA showed an inverse correlation with A (r = -0.93 *) (Tab. 2).

Figure 6
a-c. Leaves of Tabebuia aurea seedlings under two water regimes: control and plants under water deficit, at predawn (5-6 a.m. before sunrise) and midday – a. SOD activity; b. APX activity; c. malondialdehyde-equivalents content (MDA). * means significance at P < 0.05 between treatments by T test; ** mean significance at P < 0.01, ns = not significant. n = 5.

Plants under the two treatments were clearly separated on the PCA analysis. The first two main components of the PCA explained 92.4% of the total variation. Gas exchange (A, gs and E) and Ψwleaf made the higher contributions to PC1, which explained 75.6% of the variation and managed to separate the groups of control and water deficit plants. PC2, that explained 16.8% of the variation, accounted primarily for antioxidant enzymes (SOD and APX), MDA, proline content, and Fv / Fm , indicating a gradient of separation between plants, independent from watering regime (Fig. 7).

Figure 7
Principal component analysis (PC1 and PC2) applied to the variables of gas exchange (A, gs , E, iWUE, IWUE), photochemical (ΦPSII, Fv / Fm , SPAD index), Ψwleaf, Ψwsoil, proline content in leaves, antioxidant enzimes (APX, SOD) and MDA of Tabebuia aurea seedlings under two water regimes: control and plants under water deficit.

Discussion

The results of this experiment with Tabebuia aurea demonstrated that plants had tolerance to soil water deficiency. The induced water deficit significantly affected growth, gas exchange and biochemical parameters. As anticipated, the plants adaptively responded with a drought avoidance strategy by reducing leaf area and closing stomata. Although the chlorophyll index and effective quantum efficiency of photosystem II reduced under water restriction, values of Fv / Fm indicated that the photochemical apparatus continued to be active. Possibly, the activity of SOD and APX prevented damage to the chloroplast membranes. Such drought tolerance mechanisms are among the strategies adopted by semi-arid plants to tolerate long periods of water shortage, as also the individual characteristics related to their own physiological plasticity of each species (Souza et al. 2010Souza BD, Meiado MV, Rodrigues BM & Santos MG (2010) Water relations and chlorophyll fluorescence response of two leguminous trees from the “Caatinga” to different watering regimes. Acta Physiologiae Plantarum 32: 235-244.).

This is a strategy to prevent excessive loss of water, thereby increasing the ability of young plants to survive water scarcity (Nascimento et al. 2011Nascimento SP, Bastos EA, Araújo ECE, Filho FRF & Silva EM (2011) Tolerância ao déficit hídrico em genótipos de feijão-caupi. Revista Brasileira de Engenharia Agrícola e Ambiental 15: 853-860.; Silva-Pinheiro et al. 2016Silva-Pinheiro J, Lins LKS, Souza FC, Silva CEM, Moura FBP, Endres L & Justino GC (2016) Drought-stress tolerance in tree semi-arid species used to recover logged area. Brazilian Journal of Botany 39: 1031-1038.). Silva-Pinheiro et al. (2016)Silva-Pinheiro J, Lins LKS, Souza FC, Silva CEM, Moura FBP, Endres L & Justino GC (2016) Drought-stress tolerance in tree semi-arid species used to recover logged area. Brazilian Journal of Botany 39: 1031-1038. also observed that water deficiency reduced the leaf area of Bauhinia monandra Kurz and T. aurea. Several plant species native to the Caatinga lose their leaves just before flowering, which typically coincides with a period of drought, producing new leaves at the beginning of the rainy season (Mendes et al. 2013Mendes MMS, Lacerda CF, Fernandes FÉP, Cavalcante ACR & Oliveira TS (2013) Ecophysiology of deciduous plants grown at different densities in the semiarid region of Brazil. Theoretical and Experimental Plant Physiology 25: 94-105.). We observed that reductions in leaf area occurred concomitantly with reductions in root biomass, suggesting that T. aurea did not invest in root growth as an adaptive strategy to access more water.

Under water deficiency, T. aurea reduced stomatal conductance, which consequently affected transpiration rate and photosynthesis. However, lower rates of transpiration and stomatal conductance can play a beneficial role by increasing leaf iWUE (that is most responsive for environmental changes such as VPD) and IWUE (that is regulated by plants physiology state or genotype) respectively (Mujawamariya et al. 2018Mujawamariya M, Manishimwe A, Ntirugulirwa B, Bahati EN, Nyirambangutse B, Nsabimana D, Wallin G & Uddling J (2018) Climate sensitivity of tropical trees along an elevation gradient in Rwanda. Forests 647: 1-19.). Both parameters are commonly analyzed together with carbon isotope discrimination to select more productive or tolerant plant genotypes (Centritto et al. 2009Centritto M, Lauteri M, Monteverdi MC & Serraj R (2009) Leaf gas exchange, carbon isotope discrimination, and grain yield in contrasting rice genotypes subjected to water deficits during the reproductive stage. Journal of Experimental Botany 60: 2325-2339.; Broeckx et al. 2014Broeckx LS, Fichot R, Verlinden MS & Ceulemans R (2014) Seasonal variations in photosynthesis, intrinsic water-use efficiency and stable isotope composition of poplar leaves in a short-rotation plantation. Tree Physiology 34: 1-14.; Medrano et al. 2015Medrano H, Tomás M, Martorell S, Flexas J, Hernández E, Rosselló J, Pou A, Escalona JM & Bota J (2015) From leaf to whole-plant water use efficiency (WUE) in complex canopies: limitations of leaf WUE as a selection target. The Crop Journal 3: 220-228.; Wang et al. 2020Wang B, Zhang J, Pei D & Yu L (2020) Combined effects of water stress and salinity on growth, physiological and biochemical traits in two walnut genotypes. Physiologia Plantarum 172: 176-187.). Increasing water-use efficiency during periods of water deficit as seen on this study is an important characteristic that can increase plant tolerance to drought (Wang et al. 2020Wang B, Zhang J, Pei D & Yu L (2020) Combined effects of water stress and salinity on growth, physiological and biochemical traits in two walnut genotypes. Physiologia Plantarum 172: 176-187.). It is important to highlight that the water-use efficiency measured at leaf level such as by gas exchange has its limitations due be always measured over short periods and so, can reflect only short-term variations in environmental conditions and the current physiological state of the leaves (Landsberg 1999Landsberg J (1999) Relationship between water use efficiency and tree production. In: Landsberg J (ed.) The ways tree use water. Water and salinity issues in agroforestry. Nº 5. Rural Industries Research and Development Corporation, Canberra. Pp. 45-54.).

Stomatal opening is proportional to the amount of CO2 demanded by photosynthesis and the amount of water loss by transpiration. Stomatal closing is thus a mechanism to reduce transpiration and decrease gas exchange, with negative consequences for carbon fixation and biomass accumulation (Barros et al. 2020Barros V, Melo A, Santos M, Nogueira L, Frosi G & Santos MG (2020) Different resource-use strategies of invasive and native woody species from a seasonally dry tropical forest under drought stress and recovery. Plant Physiology and Biochemistry 147: 181-190.). Stomatal effects seem to be the main limiting factor for photosynthesis, since other parameters were not severely affected. It is noteworthy that the plants were able to remain photosynthetically active even under dry conditions throughout the experiment. Nevertheless, the decrease in stomatal conductance under water deficit suggests that the gs response is a key mechanism of drought tolerance. The positive correlation observed in these variables shows that stomatal closure was linked to reductions in Ci and photosynthetic rates in stressed plants.

Stomatal closure is a strategy to minimize the negative effects of water deficiency and is an important characteristic of drought tolerant species (Lawlor & Tezara 2009Lawlor DW & Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Annals of Botany 103: 561-579.; Berry et al. 2010Berry JA, Beerling DJ & Franks PJ (2010) Stomata: key players in the earth system, past and present. Current Opinion in Plant Biology 13: 232-239.), as observed in Carapa guianensis Aubl. (Carvalho et al. 2009Carvalho JFG, Silva CEM & Guimarães DG (2009) Fotossíntese e potencial hídrico foliar de plantas jovens de andiroba submetidas à deficiência hídrica e à reidratação. Pesquisa Agropecuária Brasileira 44: 8-14.). Various studies (e.g., Pinheiro et al. 2005Pinheiro HA, Da Matta FM, Chaves ARM, Loureiro ME & Ducatti C (2005) Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora. Annals of Botany 96: 101-108.; Deuner et al. 2008Deuner S, Alves JD, Fries DD, Zanandrea I, Lima AA, Henrique PC & Goulart PFP (2008) Hydrogen peroxide and ascorbic acid effects on antioxidant enzyme activity in coffee seedlings. Revista Ceres 55: 134-140.; Nascimento et al. 2008Nascimento MN, Alves JD, Soares AM, Castro EM, Magalhães MM, Alvarenga A & Silva GH (2008) Biochemical alterations of plants and bud morphology of coffee tree associated to events on flowering in response to meteorological elements. Ciência Rural 38: 1300-1307.; Broeckx et al. 2014Broeckx LS, Fichot R, Verlinden MS & Ceulemans R (2014) Seasonal variations in photosynthesis, intrinsic water-use efficiency and stable isotope composition of poplar leaves in a short-rotation plantation. Tree Physiology 34: 1-14.) suggest that stomatal closure is the primordial strategy to minimize water loss during the day period. Galmés et al. (2007)Galmés J, Medrano H & Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytologist 175: 81-93. working with eight Mediterranean species submitted to water deficiency also verified decreases in stomatal conductance. Certainly, decreases in stomatal conductance are important to minimize water loss, but with the consequence that the rubisco catalytic site may be deprived of CO2 leading to a decrease in carbon assimilation. Thus, acclimation of T. aurea during drought stress is primarily dependent on stomatal control, since CO2 availability is crucial to ensure photosynthesis. Under regular watering, open stomata permit high levels of gas exchange enabling vegetative growth, as observed in our study. Generally, gs of species from semiarid environments have more sensitive drought responses before a change in leaf water content is detectable (Souza et al. 2010Souza BD, Meiado MV, Rodrigues BM & Santos MG (2010) Water relations and chlorophyll fluorescence response of two leguminous trees from the “Caatinga” to different watering regimes. Acta Physiologiae Plantarum 32: 235-244.).

The multivariate analysis (PCA) corroborates the results found by Pearson’s correlation, that shows a correlation between the gas exchange variables and supports the role of the control of the stomatal opening and its reflexes on the A and E as an important drought tolerance strategy adopted by the plants of T. aurea under water deficit in this experiment. In a review of 20 water stress indicator parameters, Füzy et al. (2019)Füzy A, Kovács R, Cseresnyés I, Parádi I, Szili-Kovács T, Kelemen B, Rajkai K & Takács T (2019) Selection of plant physiological parameters to detect stress effects in pot experiments using principal component analysis. Acta Physiologiae Plantarum 41: 56. concluded that gas exchange is one of the parameters set that are the most useful indicators of stress, preferably when the plant biomass is constant between treatments (not observed in this experiment), which reinforces the data obtained from the PCA.

High levels of radiation can cause reductions in gas exchange due to photoinhibition, when excess excitation energy absorbed by plant leaves exceeds the photosystem II repair cycle (Nixon et al. 2010Nixon PJ, Michoux F, Yu J, Boehm M & Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Annals of Botany 106: 1-16.). However, we observed a similar Fv / Fm ratio in plants submitted to water deficiency and well-watered plants. Although T. aurea did not exhibit significant differences of Fv / Fm between treatments, there was a reduction in ΦPSII in plants under water deficit, which may have contributed to the decrease in photosynthesis. Reductions in ΦPSII probably impair efficiency of photosystem II, reducing the proportion of energy absorbed by plants (Maxwell & Johnson 2000Maxwell K & Johnson GN (2000) Chlorophyll fluorescence: a pratical guide. Journal of Experimental Botany 51: 659-668.).

The increase in SOD and APX activity observed after 29 days of water deficiency probably reflects an adaptation to avoid chronic photooxidative damage. SOD is the first barrier against the toxic effect of ROS (Mittler 2002Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7: 405-410.). Oxidative stress induced by an excess of energy in photosystems may limit photosynthesis and lead to an over-excitation of the reaction centers of photosystem II leading to a production ROS (Carvalho 2008Carvalho MHC (2008) Drought stress and reactive oxygen species. Plant Signaling & Behavior 3: 156-165.; Santos et al. 2013Santos CM, Verissimo V, Wanderley Filho HCL, Ferreira VM, Cavalcante PGS, Rolim EV & Endres L (2013) Seasonal variations of photosynthesis, gas exchange, quantum efficiency of photosystem II and biochemical responses of Jatropha curcas L. grown in semi-humid and semi-arid areas subject to water stress. Industrial Crops and Products 41: 203-213.). An increase in SOD and APX activity was verified in plants stressed by water deficit. These enzymes are involved in antioxidant defense system, scavenging ROS and reducing damage to chloroplasts membranes and photosystem (Rena & Maestri 2000Rena AB & Maestri M (2000) Water relations in coffee. Item 48: 34-41.; Grisi et al. 2008Grisi FA, Alves JD, Castro EM, Oliveira C, Biagiotti G & Melo L (2008) Leaf anatomical evaluations in ‘Catuaí’ and ‘Siriema’ coffee seedlings submitted to water stress. Ciência e Agrotecnologia 32: 1730-1736.; Deng et al. 2018Deng Y, Jia X, Sun X, Liang L & Su J (2018) Comparison of jasmine antioxidant system responses to different degrees and durations of shade. Acta Physiologiae Plantarum 40: 41.). When considered with the similarity in MDA content in both treatments, these results indicate that antioxidant system of T. aurea is able to regulate oxygen metabolism avoiding chronic damages to the chloroplast membrane system and protecting proteins complexes that catalyzes the light reactions (Queiroz et al. 2002Queiroz CGS, Garcia QS & Lemos Filho JP (2002) Atividade fotossintética e peroxidação de lipídios de membrana em plantas de aroeira-do sertão sob estresse hídrico e após reidratação. Brazilian Journal of Plant Physiology 14: 59-63.; Oliveira et al. 2014Oliveira MT, Matzek V, Dias CM, Rivas R, Falcão HM & Santos MG (2014) Stress tolerance and ecophysiological ability of an invader and a native species in a seasonally dry tropical forest. PLoS ONE 9: e105514.).

Besides the ROS detoxification system, plants can develop other strategies to tolerate water deficit, such as reduction of chlorophyll synthesis or of chloroplast pigment content (Silva-Pinheiro et al. 2016Silva-Pinheiro J, Lins LKS, Souza FC, Silva CEM, Moura FBP, Endres L & Justino GC (2016) Drought-stress tolerance in tree semi-arid species used to recover logged area. Brazilian Journal of Botany 39: 1031-1038.). The observed reduction in SPAD index in drought stressed plants suggests that chlorophyll content was affected by the water deficit. A decrease in chlorophyll content under drought stress has been considered as a typical symptom of oxidative stress and may result from photooxidation of the photosynthetic pigments (Anjum et al. 2011Anjum SA, Xie X, Wang L, Saleem MF, Man C & Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. African Journal of Agricultural Research 6: 2026-2032.; Abdoli & Saeidi 2013Abdoli M & Saeidi M (2013) Evaluation of water deficiency at the post anthesis and source limitation during grain filling on grain yield, yield formation, some morphological and phonological traits and gas exchange of bread wheat cultivar. Albanian Journal of Agricultural Sciences 12: 255-265.). Although, the positive correlation between Fv / Fm and SPAD index implies that water deficiency reduces chloroplast pigment content and may damage PSII activity, there is evidence that water stressed plants can prevent photoinhibitory damage by reducing chlorophyll content (Kyparissis et al. 1995Kyparissis A, Petropoulou Y & Manetas Y (1995) Summer survival of leaves in a soft-leaved shrub (Phlomis fruticosa L., Labiatae) under mediterranean field conditions: avoidance of photoinhibitory damage through decreased chlorophyll contents. Journal of Experimental Botany 46: 1825-1831.). Similar results have been reported in other studies with tree species under water deficiency (Alves 2007Alves JJ (2007) Geoecologia da “Caatinga” no semiárido do nordeste brasileiro. Climatologia e Estudos da Paisagem 2: 58-71.; Huseynova et al. 2016Huseynova IM, Rustamova SM, Suleymanov SY, Aliyeva DR, Mammadov AC & Aliyev JA (2016) Drought-induced changes in photosynthetic apparatus and antioxidant components of wheat (Triticum durum Desf.) Photosynthesis Research 130: 215-223.).

Proline content increased in the leaves of plants under water deficit, and we can suggest that that T. aurea has an osmotic adjustment mechanism based on proline accumulation; there was a positive correlation between proline and Ψwleaf. These changes are consistent with other studies that show that increased proline can benefit plant metabolism, like maintaining cell turgor by osmoregulation and protecting membranes and macromolecules from damage caused by desiccation (Hayat et al. 2012Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J & Ahmad A (2012) Role of proline under changing environments. Plant Signaling & Behavior 7: 1456-1466.; Hassan et al. 2021Hassan MAE, Santhoshkumar AV, Hrideek TK, Jijeesh CM & Joseph J (2021) Variability in drought response among the plus tree accessions of Tectona grandis (Linn f.) from the provenances of Kerala, South India. Acta Physiologiae Plantarum 43:47.). Our results do not support the strategy of maintaining the turgor since there was a reduction in plant growth and closure of stomata, but it indicates that proline may have acted in protecting membranes and as a reserve of carbon and nitrogen for subsequent synthesis of organic compounds after rehydration (Aranjuelo et al. 2011Aranjuelo I, Molero G, Erice G, Avice JC & Nogués S (2011) Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.). Journal of Experimental Botany 62: 111-123.; Hemaprabha et al. 2012Hemaprabha G, Swapna S, Lavanya DL, Sajitha B & Venkataramana S (2012) Evaluation of drought tolerance potential of elite genotypes and progenies of sugarcane (Saccharum sp. hybrids). Sugar Tech 15: 9-16.).

Our results suggest that the analyzed physiological and biochemical variables were adjusted to attenuate the effects of water deficiency. Stomatal conductance was reduced, but it probably was essential for plants to remain photosynthetically active during the 29 days of water deficit. Despite a reduction in biomass accumulation due decreases in photosynthesis and leaf area, antioxidant activity avoided significant damage to the thylakoid membranes.

Tabebuia aurea responded to experimental water deficiency via stomatal regulation, resulting in a decrease in biomass accumulation. Nevertheless, plants were able to maintain low rates of photosynthesis supported by the protective effects of an antioxidant mechanism and synthesis of proline. These physiological adaptations make this species a good candidate for restoration initiatives in degraded areas of the semi-arid Caatinga biome of northeast Brazil.

Acknowledgements

L.E was supported by the Research Productivity Scholarship Program in Brazilian Council for Scientific and Technological Development (CNPq) (No. 310300/2017-7). The authors thank Richard James Ladle, for proofreading the manuscript.

This work was supported by the National Council for Scientific and Technological Development (CNPq, Brazil) [449264/2014].

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Edited by

Area Editor: Dr. Marcelo Mielke

Publication Dates

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

History

  • Received
    13 Nov 2020
  • Accepted
    20 Apr 2021
Instituto de Pesquisas Jardim Botânico do Rio de Janeiro Rua Pacheco Leão, 915 - Jardim Botânico, 22460-030 Rio de Janeiro, RJ, Brasil, Tel.: (55 21)3204-2148, Fax: (55 21) 3204-2071 - Rio de Janeiro - RJ - Brazil
E-mail: rodriguesia@jbrj.gov.br