UV-B effects on growth, photosynthesis, total antioxidant potential and cell wall components of shade-tolerant and sun-tolerant ecotypes of Paubrasilia echinata

Highlights

• The shade-tolerant ecotype of P. echinata is negatively responsive to UV-B while the sun-tolerant ecotype is positively responsive.

• Antioxidant potential in UV-B is more efficient in sun-tolerant than shade-tolerant ecotype.

• UV-B increased lignin to the detriment of hemicelluloses in the sun-tolerant ecotype, but did not influence these polymers in the shade-tolerant ecotype.

Abstract

The incidence of UV-B radiance on the surface of the earth has been intensifying in the tropics of the southern hemisphere. However, little is known about its effect on tropical trees, especially on sun-tolerant versus shade-tolerant plants. For this study we used two ecotypes of the tropical tree Paubrasilia echinata. These ecotypes diverge among themselves in relation to leaf morphology and ecological habitats as with respect to light availability. The small-leaf ecotype is shade-tolerant and the medium-leaf ecotype is sun-tolerant. The plants were submitted to UV-B for 45 days. The shade-tolerant ecotype proved to be negatively responsive to UV-B indicated by inhibition of stem growth, total biomass, CO₂ assimilation (A) and photochemical efficiency (F_V'/F_M'), whereas the sun-tolerant ecotype showed to be positively responsive. This divergence of responses between the two ecotypes seems to be related to the capacity to produce phenolic compounds, total antioxidant capacity (TAC) and cell respiration (Rd). UV-B increased flavonoids, lignin, TAC and reduced Rd in the sun-tolerant ecotype. In the shade-tolerant ecotype, these responses were opposite, with increased leaf loss. As for cell wall polymers (CWP), the ultraviolet radiance increased the lignin content to the detriment of hemicelluloses in the sun-tolerant ecotype. However, it did not influence the cellulose content. In the shade-tolerant ecotype, in general, the proportions of the three CWP remained invariable in relation to the control. The results indicate that the ecotypes of P. echinata function as a good model to investigate the UV-B effects on sun-tolerant and shade-tolerant tropical trees. We presume that the increase in UV-B may be a compromise for populations of juvenile plants of the shade-tolerant ecotype and increase populations of the sun-tolerant ecotype.

Introduction

Depletion of the ozone layer (O₃) of the stratosphere by atmospheric pollution has elevated the incidence of ultraviolet radiance UV-B (280–315 nm) on the surface of the Earth (Ballaré et al., 2011; Ball et al., 2018). This is happening in a more pronounced way in the tropics of the southern hemisphere (Ballaré et al., 2011; Ball et al., 2018) with a prediction of great impact on the production of plants of agronomic interest and on the functioning of natural ecosystems (Piri et al., 2011).

Reviews on the UV-B effects on plants denote the manifestation of a range of deleterious effects on plant morphology, physiology and biochemistry differing in the intensity of the responses at the interspecific level, and dependent on UV-B doses, ontogenetic phase, and environmental conditions (controlled or not) for conducting the experiments (Piri et al., 2011; Zlatev et al., 2012; Barnes et al., 2017). In general, the increase in UV-B reduces biomass, stem growth, number of leaves, specific leaf area, photosynthesis and induces changes in flowering in the negatively responsive species (Piri et al., 2011; Kataria et al., 2014; Robson et al., 2015; Huché-Théliera et al., 2016; Barnes et al., 2017). In the indifferent species, no effect was observed on growth and photosynthesis (Krause et al., 2003; Piri et al., 2011). In a few cases, promotional effect may occur in the species that are positively responsive to UV-B (Zlatev et al., 2012).

The sensitivity level of plants to UV-B has been associated with the balance of oxidant activity and antioxidant potential (Kataria et al., 2014). Under high UV-B, plants produce more reactive oxygen species (ROS) such as H₂O₂ (Kataria et al., 2014), a potent agent of lipid peroxidation diagnosed by increased malondialdehyde–MDA (Asada, 1999). In excess, ROS cause oxidation of biomolecules such as lipids, proteins and DNA (Hideg et al., 2013). Antioxidant reactions to UV-B comprise enzymatic and non-enzymatic mechanisms (Baroniya et al., 2014; Zlatev et al., 2012; Martínez-Lüscher et al., 2015). Non-enzymatic reactions consist of the accumulation of phenolic substances such as flavonoids (Ruuhola et al., 2018), anthocyanins, carotenoids and other compounds (Zhu and Yang, 2015; Sankari et al., 2017) in the upper epidermis of the leaves, where they act as ultraviolet absorbers. This UV-B block prevents the formation of ROS at levels toxic for the cell (Shen et al., 2010; Hideg et al., 2013).

Even knowing that the cell wall represents the largest reservoir of carbon in plants and of the biosphere, and that it has a key role in the carbon cycle (Schädel et al., 2010), little attention has been given to the UV-B radiance effects on this cellular structure. The cell wall is composed of structural polysaccharides (cellulose and hemicelluloses), pectin, lignin, proteins and other compounds. In herbaceous species of the Arctic region, the ultraviolet radiance increased the levels of phenolic compounds associated with the cell wall structure (Semerdjieva et al., 2003; Ruhland et al., 2005). Another effect was the CH₄ release of pectin, resulting in cell wall loosening (Messenger et al., 2009). In addition, nothing else is known about the results of increased ultraviolet radiance in cell wall composition, especially in tropical forest trees with strong commercial appeal.

One of the tropical trees of the southern hemisphere with high economic value is the Brazilwood (Paubrasilia echinata), native from Brazil’s Atlantic Forest biome. The core of its wood is used to make high quality string for musical instruments internationally recognized. This species has three morphotypes (small, medium and large leaf) that differ from one another in the morphology and leaflet area of their recomposed leaves. The small and medium morphotypes are bipened, and have smaller and intermediate leaflet area, respectively, while the large morphotype is pened with superior leaflet area, and can occur sympatrically or allopatrically (Juchum et al., 2008). These morphotypes also diverge to the ecological habitats with respect to light availability. The small morphotype is shade-tolerant while the medium and large morphotypes are sun-tolerant (Gama, 2017). Considering that P. echinata variants also differ in ecological habit, in this study we adopted the word ecotype (Lowry, 2012) in place of morphotype.

This intraspecific ecophysiological distinction of the ecotypes of P. echinata is singular in humid rainforests. Therefore, it is very interesting to investigate the UV-B effects on sun-tolerant and shade-tolerant tropical trees, by excluding the interspecific taxonomic divergence. Thus, the shade-tolerant and sun-tolerant ecotypes of P. echinata could function as a good model for the investigation of UV-B reactions at morphological, physiological and biochemical levels, including the cell wall composition, which is so poorly explored in this field of research.

Considering that the shade-tolerant tropical tree ecotype has its growth and photosynthesis inhibited by higher solar radiance due to its low total antioxidant capacity–TAC (Favaretto et al., 2011) and considering the indication of cell wall loosening by UV-B (Messenger et al., 2009), we hypothesize that: i) the shade-tolerant ecotype is negatively responsive to UV-B due to its deleterious effect on growth and photosynthesis, while the sun-tolerant ecotype is indifferent to UV-B; ii) the sensitivity difference of the two ecotypes to UV-B is associated with the antioxidant phenolic compounds (flavonoids and lignin), TAC (total antioxidant potential) and cell wall composition, being affected in shade-tolerant, but indifferent in sun-tolerant. This study was carried out to describe the UV-B effects on growth, photosynthesis, antioxidant potential, levels of UV-B absorbing phenolic compounds and on the cell wall composition of the shade-tolerant and sun-tolerant ecotypes of P. echinata in the initial growth phase.