Does Oxidative Stress Determine the Thermal Limits of the Regeneration Niche of Vriesea Friburgensis and Alcantarea Imperialis (Bromeliaceae) Seedlings? T
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Journal of Thermal Biology 80 (2019) 150–157 Contents lists available at ScienceDirect Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio Does oxidative stress determine the thermal limits of the regeneration niche of Vriesea friburgensis and Alcantarea imperialis (Bromeliaceae) seedlings? T Alexandre Aparecido Duartea,1, Cristiane Jovelina da-Silvaa,1, Andréa Rodrigues Marquesb, ⁎ Luzia Valentina Modoloa, José Pires Lemos Filhoa, a Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil b Departamento de Ciências da Natureza, CEFET/MG, Belo Horizonte, MG, Brazil ARTICLE INFO ABSTRACT Keywords: The predicted environmental changes may be detrimental to initial seedling growth, particularly the expected Thermal limits increase in air temperature. We therefore investigated the thermal limits for growth and development of Vriesea Oxidative stress friburgensis and Alcantarea imperialis seedlings in the context of oxidative stress. The optimal temperatures for the Nitric oxide growth of V. friburgensis and A. imperialis were 25 and 25–30 °C, respectively. Extreme temperatures (15, 30, or Hydrogen peroxide 35 °C) induced oxidative stress in both species with significant accumulation of hydrogen peroxide (H O ) and Seedling growth 2 2 nitric oxide (NO). Under oxidative stress, the amount of chlorophyll decreased in both species, more prominently Abiotic stress in V. friburgensis, while carotenoid levels dramatically increased in A. imperialis. Notably, the activities of su- peroxide dismutase, catalase (CAT), and ascorbate peroxidase increased in A. imperialis at extreme temperatures. Similar results were observed for V. friburgensis; however, the activity of CAT remained unaffected regardless of temperature. Seedlings of A. imperialis survived at a wider range of temperatures than V. friburgensis, which had greater than 40% mortality when growing at 30 °C. Overall, precise control of cellular H2O2 and NO levels takes place during the establishment of A. imperialis seedlings, allowing the species to cope with relatively high temperatures. The thermal limits of the fundamental niches of the species investigated, determined based on the ability of seedlings to cope with oxidative stress, were distinct from the realized niches of these species. The results suggest that recruitment success is dependent on the ability of seedlings to handle extreme temperature- triggered oxidative stress, which limits the regeneration niche. 1. Introduction spanning the native ranges of species, and that the geographic dis- tributions of species represent the realized, rather than the funda- The predicted scenarios based on expected global climatic changes mental, tolerance limits of said species (Drake et al., 2017). The fun- may impose severe limits on the viability of plant populations. Seed damental niche (NF) of a species comprises the set of environmental germination and post-germination stages are recognized as crucial conditions that allows it to survive and reproduce not considering its phases of the plant life cycle, and changes in the environmental con- interaction with other living organisms (Soberón and Arroyo-Peña, ditions to the regeneration niche may severely compromise plant sur- 2017). However, species can occupy only a portion of the potential area vival (Donohue et al., 2010; Donohue, 2014; Marques et al., 2014; defined by the NF, which results in a small geographic area known as Arana et al., 2015; Fernández-Pascual et al., 2017). Hence, the re- the realized niche (NR)(Soberón and Nakamura, 2009). generation niche breadth and the upper and lower thermal limits for Most studies on the thermal tolerance of plants focus on seeds, while germination (Cochrane et al., 2014; Müller et al., 2017; Daibes and little is known about seedling performance as a function of temperature Cardoso, 2018; Duarte et al., 2018) and seedling establishment variation. Seed germination can be empirically defined as a tempera- (Klanderud et al., 2017) modulate the initial success of recruitment and ture-dependent process (Porceddu et al., 2013; Batlla and Benech- thus influence the composition of communities (Walck et al., 2011; Arnold, 2015; Arana et al., 2015; Duarte et al., 2018), in which the Jiménez-Alfaro et al., 2016). Climate change has revealed that func- relationship between temperature and enzyme activity is quite complex tional traits respond to warming along a gradient of local temperatures (Rasheed et al., 2016). Signaling processes and variation in the activity ⁎ Corresponding author. E-mail address: [email protected] (J.P. Lemos Filho). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.jtherbio.2019.02.003 Received 15 June 2018; Received in revised form 3 January 2019; Accepted 1 February 2019 Available online 02 February 2019 0306-4565/ © 2019 Elsevier Ltd. All rights reserved. A.A. Duarte et al. Journal of Thermal Biology 80 (2019) 150–157 of antioxidant enzymes are biochemical events that may be reliable (Paula et al., 2016). The species also occurs in Campos Rupestres tools in estimating the thermal limits of the NF of seedlings. Imbalance throughout the EMR (Versieux and Wanderley, 2007). Within the in the production of reactive oxygen species (ROS) because of thermal geographic limits of its occurrence, the average minimum temperature stress (for review see Szymańska et al., 2017) has been demonstrated to registered during the dry season is slightly above 15 °C, while the negatively affect cell membrane stability and activity of antioxidant average maximum temperature during the wet season is below 30 °C enzymes (Mittler et al., 2012). Uncontrolled overproduction of ROS (Fig. 1). - - (i.e., O2 ,H2O2, and OH ) also decreases chlorophyll content and da- Seeds of at least 10 V. friburgensis plants (~2500 seeds) grown in mages the thylakoid membranes, which in turn compromises plant Campo Rupestre of Serra da Piedade (Minas Gerais State) and 10 A. growth (Nievola et al., 2005; Mollo et al., 2011; Mathur et al., 2014). imperialis plants (~ 2500 seeds) grown in a garden in São Paulo (São Notably, plants may benefit from relatively low amounts of ROS be- Paulo State) were collected in June (the dry season) and October (onset cause of the ability of ROS to function as signaling molecules (Mittler of the wet season), respectively, during their dispersal periods. Freshly et al., 2011; Choudhury et al., 2017; Da Silva et al., 2017). It has been harvested seeds from mature fruits of each species were mixed to avoid reported that increases in the levels of nitric oxide (NO), a reactive maternal effects and were set to germinate in 9 mm Petri dishes con- nitrogen species recognized as signaling molecule, boost the anti- taining a sufficient amount of water for imbibition. Afterwards, plates oxidant system and enhance the membrane stability in plant species were maintained in a germination chamber (FANEN, model 347 CDG, upon thermal or salt stress (Fan et al., 2015; Da Silva et al., 2017). The São Paulo, Brazil) at 25 °C, with a photosynthetic photon flux density − plant antioxidant system includes enzymes such as superoxide dis- (PPFD) of 30 μmol m2 s 1 and a 12 h photoperiod. The temperature of mutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and pig- 25 °C was chosen because both species exhibited the highest germina- ments including carotenoids (Del Río, 2015). tion percentage and rate at this temperature. Fives samples, each The limits of tolerance are species-specific(Davis et al., 2005) and composed of 100 seeds, were dried out at 60 °C for 72 h in order to vary according to the plant's capacity to metabolically adjust to tem- determine seed biomass. peratures outside of the optimal range. Relatively little is known about the potential effects of rising temperatures on bromeliads (Chaves et al., 2.2. Seedling growth and quantification of photosynthetic pigments 2015, 2018; Duarte et al., 2018; Müller et al., 2017), as only three re- ports have so far focused on plant cultivation under low temperatures Three hundred seeds with protruding roots were selected and (Pedroso et al., 2010; Mollo et al., 2011; Carvalho et al., 2013, 2014). maintained on moisturized paper inside Plexiglass boxes (15 per box) at − Thus, the lack of knowledge on the effect of temperature on bromeliad a PPFD of 30 µmol m2 s 1 (12 h photoperiod) and different air tem- seedling growth makes the prediction of recruitment success of this peratures (15, 25, 30, or 35 °C) with five replicates per treatment. family following climate change difficult. Recent studies of thermal Seedling mortality and number of leaves were determined for all in- tolerance have suggested that the capacity for evolutionary adaptation dividuals on the last day of experimentation (day 30). The effect of is greater for minimum rather than maximum thermal tolerances, with temperature on biomass accumulation in seedlings of Vriesea fri- maximum temperature tolerance remaining relatively unchanged burgensis (n = 12 per replicate) and Alcantarea imperialis (n = 12 per (Araújo et al., 2013). In addition, species with narrow NR are restricted replicate) was determined as later described in Section 2.1. Photo- to a narrow NF, whereas NR can either be broad or narrow when the NF synthetic pigments were extracted from three seedlings from each re- is broad (Bush et al., 2017). In this context, we evaluated the perfor- plicate using dimethyl sulfoxide and quantified as described by mance of Vriesea friburgensis (a widely distributed species) and Alcan- Wellburn (1994). The results were expressed as µg of pigment per g of tarea imperialis (a species with a narrow geographic range) based on the fresh weight (FW). activation of the antioxidant system in seedlings to determine the thermal niche breadths of both bromeliads. The seedlings’ growth and 2.3. Quantification of endogenous H2O2, NO and activity of antioxidant survival were investigated at optimal and extreme temperatures to enzymes correlate their performance with metabolic changes associated with oxidative stress. Five samples of both plant species, each constituting 20 fresh seedlings, were grown at 15, 25, 30, or 35 °C and harvested 30 days 2.