Selenium toxicity in upland field-grown rice: Seed physiology responses and nutrient distribution using the μ-XRF technique

https://doi.org/10.1016/j.ecoenv.2019.110147Get rights and content

Highlights

  • Foliar Se application above 250 g ha-1decrease rice yield and physiological seed quality.

  • The highest Kα counts of Se were detected mainly in the endosperm and aleurone/pericarp.

  • Sulfur accumulation occurred in the same tissues and in the embryo region.

  • The μ-XRF was a great technique to map the distribution of Se in rice seeds.

Abstract

Selenium (Se) is an essential element for human and animal, although considered beneficial to higher plants. Selenium application at high concentration to plants can cause toxicity decreasing the physiological quality of seeds. This study aimed to characterize the Se toxicity on upland rice yield, seed physiology and the localization of Se in seeds using X-ray fluorescence microanalysis (μ-XRF). In the flowering stage, foliar application of Se (0, 250, 500, 1000, 1500, 2000 g ha−1) as sodium selenate was performed. A decrease in rice yield and an increase in seed Se concentrations were observed from 250 g Se ha−1. The storage proteins in the seeds showed different responses with Se application (decrease in albumin, increase in prolamin and glutelin). There was a reduction in the concentrations of total sugars and sucrose with the application of 250 and 500 g Se ha−1. The highest intensities Kα counts of Se were detected mainly in the endosperm and aleurone/pericarp. μ-XRF revealed the spatial distribution of sulfur, calcium, and potassium in the seed embryos. The seed germination decreased, and the electrical conductivity increased in response to high Se application rates showing clearly an abrupt decrease of physiological quality of rice seeds. This study provides information for a better understanding of the effects of Se toxicity on rice, revealing that in addition to the negative effects on yield, there are changes in the physiological and biochemical quality of seeds.

Introduction

Selenium (Se) is an essential element for the maintenance of human and animal health because it plays a fundamental role in numerous metabolic and immunological processes (White, 2018). Selenium deficiency is a fairly common problem in human nutrition worldwide, but ingestion of Se at high concentrations can cause hair loss and nail decay (Fairweather-Tait et al., 2011). Selenium concentration in plants and their edible parts is directly related to the Se concentration in soils (Andrade et al., 2018; Lidon et al., 2019). A large part of ingested Se in the human diet is directly or indirectly attributed to edible plant parts (Joy et al., 2015). Thus, deficiency or toxicity of this element in the human population is usually attributed to foods produced in regions where soils naturally have low or high Se concentrations (Chilimba et al., 2014; Reis et al., 2017).

Inorganic fertilizers containing Se have been found to be efficient for increasing the Se concentration in crops, raising its dietary levels and decreasing deficiency in animals and humans (Fairweather-Tait et al., 2011; Mangueze et al., 2018; Silva et al., 2019). Rice is a staple food in dozens of countries and is responsible for providing approximately 80% of the daily caloric intake to approximately 3 billion people worldwide (Lucca et al., 2006; Reis et al., 2018).

At low concentrations, Se acts as an antioxidant, scavenging reactive oxygen species (ROS) and reducing oxidative stress, and positive effects are observed on the yield of various plant species (Chilimba et al., 2014; Reis et al., 2018; Lidon et al., 2019). In contrast, application of high concentration of Se induces inverse physiological effects in nontolerant plants, which is related to the replacement of cysteine and methionine in proteins by selenomethionine (SeMet) and selenomethylcysteine (SeMeSeCys) (Gupta and Gupta, 2017). The effects of Se toxicity include increased production of ROS and reactive nitrogen species (RNS), causing changes in proteins, lipids and carbohydrates, organelle degradation, and reduced plant growth (Mostofa et al., 2017; Silva et al., 2018; Kolbert et al., 2019). However, information in the literature on the effects of Se toxicity on the physiological quality of seeds is still very scarce.

Most studies that evaluated Se toxicity in rice have used plants in early developmental stages under greenhouse conditions or in laboratory tests (Nothstein et al., 2016; Mostofa et al., 2017; Du et al., 2019). In these studies, mainly the effects of excess of Se on leaves and roots were evaluated. Regardless, the physiological and biochemical responses to Se toxicity are still poorly understood, especially in plants grown under field conditions and in evaluations of seed quality. In addition, there is little detailed information on the spatial location of Se and nutrients in seeds as well as its effects on the physiologic potential of seeds form field-grown rice under Se toxicity.

In this sense, studies are needed to elucidate the metabolic, physiological plant adjustments, and Se seed storage relationships in rice seeds under toxicity conditions, given that rice seeds are among the main food sources in the world. Thus, the present study aimed to I) gain insight into plant physiological and metabolic modulation as regard to higher Se supply and II) to characterize the effect of Se toxicity on the yield, and on the spatial Se localization in the seed components using the X-ray fluorescence microanalysis (μ-XRF) in upland field-grown rice fertilized with sodium selenate.

Section snippets

Experimental site

The experiment was conducted at the Teaching, Research and Extension Farm of São Paulo State University (Universidade Estadual Paulista – UNESP), located in the municipality of Selvíria, State of Mato Grosso do Sul, Brazil (20°20′43″ S, 51°24′7″ W; 355 m altitude). According to the Köppen classification, the climate in the region is Aw, humid tropical, with rainy summers and dry winters (Silva et al., 2018). The mean annual rainfall is 1232 mm, and the mean temperature is 24.5 °C.

The soil is

Yield, Se concentration, and sugars

The Se treatments caused significant effects on the Se concentration (Fig. 1a) and seed yield (Fig. 1b). Foliar application of Se up to 2000 g ha−1 led to an increase in Se concentration in the seeds. Conversely, seed yield decreased as function of applied Se. The highest concentrations of Se were recorded in plants that received 2000 g Se ha−1, which yield was 41% lower than the control treatment.

Foliar application of Se affected the concentration of total soluble sugars (Fig. 1c) and sucrose (

Rice yield, Se concentration, and sugars

The increasing Se concentration in rice seeds according to the increase in sodium selenate applied (Fig. 1a) revealed the high Se transport capacity from leaves to seeds, as observed in former studies utilizing Se application (Andrade et al., 2018; Reis et al., 2018; Silva et al., 2018). Foliar concentration of Se above 5 mg kg−1 in non-hyperaccumulator plants is considered toxic for most crops (Rielly, 1996; Silva et al., 2018; Kolbert et al., 2019).

The reduced seed yield observed at all Se

Conclusion

Foliar application of Se concentration above 250 g ha−1 caused negative effects on upland rice, decreasing the yield and lowering the physiological seed quality.

Biochemical analyses of seeds did not indicate changes in total amino acids. However, there were diverse effects on protein fractions, with decreased content of albumin and increased prolamin and glutelin. The concentrations of total sugars and sucrose varied with the Se application.

The embryo and aleurone/pericarp were the main tissues

CRediT authorship contribution statement

André Rodrigues dos Reis: Conceptualization, Funding acquisition, Writing - review & editing. Eduardo Henrique Marcandalli Boleta: Formal analysis. Charline Zaratin Alves: Formal analysis. Mayara Fávero Cotrim: Formal analysis. Julierme Zimmer Barbosa: Writing - original draft. Vinícius Martins Silva: Formal analysis, Writing - review & editing. Rafael Lawandovski Porto: Formal analysis, Writing - review & editing. Maria Gabriela Dantas Bereta Lanza: Formal analysis. José Lavres: Writing -

Acknowledgments

We acknowledge FAPESP (São Paulo Research Foundation) for supporting this research, with financial resources provided by process numbers 16/19937-0, 15/05942-0 (Young Researchers Awards), and 15/19121-8 (Multiuser Equipment Facility). ARR also thanks the National Council for Scientific and Technological Development (CNPq) for the research fellowship (grant 309380/2017-0).

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