Elsevier

Journal of Hazardous Materials

Volume 352, 15 June 2018, Pages 130-138
Journal of Hazardous Materials

Sex-related responses of European aspen (Populus tremula L.) to combined stress: TiO2 nanoparticles, elevated temperature and CO2 concentration

https://doi.org/10.1016/j.jhazmat.2018.03.031Get rights and content

Highlights

  • Ti uptake in roots in high nTiO2 treated soils increased at elevated temperature.

  • Both elevated temperature and CO2 affected plant growth but nTiO2 did not.

  • Leaf phenolics were reduced at elevated temperature but increased at elevated CO2.

  • Nano-TiO2 increased leaf phenolics in females under all climate treatments.

  • Females had better chemical protection and defense against nTiO2 than males.

Abstract

The combined effects of climate change and chemical contaminants on plant performance are still not well understood. Especially, whether different sexes of dioecious plants respond differently to combined stresses is unknown. In order to study the sex-related responses of European aspen to soil nTiO2 contamination (0, 50, 300 mg kg–1) under elevated temperature (+1.6 °C) and CO2 (730 ppm), we conducted a study in greenhouses. Ti accumulated in roots exposed to nTiO2 (1.1–3.3 and 2.7–21.1 mg kg–1 in 50 and 300 mg kg–1 treatments, respectively). Elevated CO2 had no effects on Ti uptake, while elevated temperature increased it in the 300 mg kg–1 treatment. Males grew taller than females under ambient conditions, but females had greater height and biomass increment under elevated temperature. In all climate treatments, nTiO2 increased leaf phenolics in females by 12–19% and 15–26% at 50 and 300 mg kg–1, respectively. Leaf phenolics decreased under elevated temperature, but increased under elevated CO2 in both sexes. Results suggest that females have better chemical defense against nTiO2 than males under future climate conditions. In the longer run, this may cause changes in the competitive abilities of both sexes, which again may affect sex ratios and genetic variation in nature.

Introduction

Since industrialization, the increased human activities caused by rapid population growth and economic development have resulted in several environmental changes including elevated air temperature and CO2 concentrations. According to most climate scenarios, global average temperature will increase by 1.5–4.8 °C and CO2 concentrations are predicted to rise to 430–1000 ppm by the year 2100 compared to pre-industrial levels [1]. Elevated temperature and CO2 affect the growth, productivity, physiology, and biochemistry of plants. In addition, the pH of the soil rhizosphere and the diversity and activity of rhizosphere microorganisms may be altered, which would concomitantly affect plant growth [[2], [3], [4], [5]]. Plant secondary metabolites, such as phenolics, are not all necessary for growth, but may play a vital role in plant adaptability and defense [6]. Previous studies have shown that the concentrations of phenolic compounds in plants decreased under elevated temperature, and increased under elevated CO2 concentration. One has also revealed significant interactions between elevated temperature and elevated CO2, as elevated temperature diminished the positive effects of elevated CO2 on plant phenolics [[7], [8], [9]]. However, the effects of elevated temperature and CO2 can vary, depending on the exposure duration, compound, and plant species tested [8,10].

TiO2 nanoparticles (nTiO2) are extensively used in industrial and commercial products (e.g., cements, asphalts, paints, sunscreens, cosmetics, and coating) because of their photocatalytic properties [11,12]. Inevitably, the widespread use of nTiO2 will lead to its continuous release into the environment, which makes it a potential environmental contaminant. Nano-TiO2 is insoluble in soil and the nanoparticulate form is also the main chemical form that can be accumulated in plant tissues, especially in roots [13]. According to previous studies, nTiO2 reduced or did not affect plant biomass, modified antioxidative enzyme activities and biochemical compositions in plants, and altered soil enzyme activities and bacterial communities [[14], [15], [16], [17]]. One could expect that nTiO2 could possibly interact with climate change factors, but this has seldom been tested. Du et al. [12] found that under elevated CO2 concentration, nTiO2 significantly reduced rice biomass and grain yield, and also changed the functional composition of soil microbial communities. Apart from this, little is known about the effects of nTiO2 on plant performance under elevated temperature and CO2 concentration.

European aspen (Populus tremula L.), a dioecious tree species, has great economic (e.g., a source for paper and construction industry) and ecological (e.g., host for herbivores and epiphytes) significance. It is widely distributed throughout Eurasian boreal and temperate ecosystems, and the populations of P. tremula are male dominated in most of the distribution areas [18]. In general, females invest more resources in reproduction and accumulation of secondary metabolites for defense than growth, while males invest more in growth and have higher herbivore abundance and damage [[19], [20], [21], [22], [23]]. Effects of elevated temperature and CO2 on sex differences in plant growth may vary with plant species. For example, the positive effects of elevated temperature on growth were greater in males of Salix myrsinifolia Salisb. [22], while females had higher height and diameter growth than males of Populus cathayana Rehd. under elevated temperature [24]. Likewise, males of P. cathayana possessed greater increases in biomass under elevated CO2 [25], but no sex differences in S. myrsinifolia were affected by CO2 [26]. In addition, sex differences in defensive phenolics response to enhanced temperature and CO2 are also variable, depending on different plant tissues, growing stage, and compound in question [22,26]. As there are different trade-offs between growth and defense between the sexes, plants may also have varying sex-related responses in growth and phenolics to soil nTiO2 contamination under climate change. However, no studies have investigated the different responses of plant growth and phenolics to nTiO2 in combination with elevated temperature and CO2 between the sexes.

In order to investigate the sex-related effects of nTiO2 in combination with elevated temperature and CO2 on P. tremula seedlings, we conducted a study in climate-regulated greenhouses. We analyzed the changes in plant height and diameter growth, biomass, leaf area, Ti uptake and leaf phenolics in females and males of P. tremula seedlings under single and combined effects of soil nTiO2 contamination and enhanced temperature and CO2 concentration. Our aims of this study were to answer the following questions. (1) As a relatively stable contaminant in soil, will nTiO2 affect plant growth and leaf defensive phenolics, and will there be interactions between nTiO2 and climate factors? (2) Whether plant tissues will accumulate Ti from nTiO2 treatments, and how will elevated temperature and CO2 affect the Ti uptake in plants? (3) How will these responses differ between female and male seedlings of P. tremula?

Section snippets

Experimental setup

The study was conducted at Mekrijärvi Research Station (62°47′N, 30°58′E, University of Eastern Finland), for 11 weeks, from May 20 to August 5, 2015. Twelve greenhouses (16 m2) were randomly assigned to four combinations of two-level temperature and CO2 concentration treatments (n = 3): ambient temperature + ambient CO2 (C), elevated temperature + ambient CO2 (T), ambient temperature + elevated CO2 (CO2), and elevated temperature + elevated CO2 (T+CO2). Ambient temperature (15.7 °C on average)

Growth

Nano-TiO2 alone showed no main effects or interactions with other factors on height growth, diameter growth or biomass of P. tremula seedlings (Fig. 1, Fig. 2, Table S3). Height growth, diameter growth and biomass significantly increased under elevated temperature, while only the height increment was reduced under elevated CO2 compared to ambient treatments (Fig. 1, Fig. 2, Table S3) (based on Sobuj et al. [28], we had 3 more genotypes of those control individuals for height, diameter and

Growth

All the measured growth parameters were unaffected by nTiO2, which is in accordance with earlier studies on vegetables (Lycopersicon esculentum Mill.), crops (Triticum aestivum L. and Phaseolus vulgaris L.), and some aquatic plants (Rumex crispus L. and Elodea Canadensis Michx.) [15,32]. Nano-TiO2 has been reported to be less toxic than other metal-based nanoparticles (e.g., Ag and ZnO nanoparticles) because of its insolubility in soils [13,33]. However, the effects of nTiO2 on plant growth

Conclusions

The changes in plant growth and in the quantity and quality of defensive phenolics under changed climate conditions and soil nTiO2 contamination will affect the environmental adaptability of different sexes of P. tremula. We assume that in the long run, the competitive abilities of different sexes of P. tremula based on nTiO2 induced defense will be changed. Females will have better chemical protection and defense against nTiO2, while males may be more susceptible to herbivores, and the sex

Acknowledgements

We gratefully acknowledge the staff at Mekrijärvi Research Station for providing facilities and daily care of the plants. We thank Sinikka Sorsa, Katri Nissinen, Unni Krishnan, Leo Vainio, Toivo Ylinampa, Nazmul Hasan, Shahed Saifullah, and Apu Sarwar for their assistance during the measurements. This work was supported by the Academy of Finland (267360), University of Eastern Finland by Spearhead Project, National Natural Science Foundation of China (21177058), the Program for New Century

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