Elsevier

Food Chemistry

Volume 275, 1 March 2019, Pages 610-617
Food Chemistry

Isolated and combined effects of elevated CO2 and high temperature on the whole-plant biomass and the chemical composition of soybean seeds

https://doi.org/10.1016/j.foodchem.2018.09.052Get rights and content

Highlights

  • Elev/Temp reduce linolenic acid of oil and do not affect the protein content.

  • The effect of Amb/Temp on the accumulation of seed metabolites is reversed by Elev.

Abstract

Soybean plants of the variety ‘MG/BR Conquista’ were grown in open top chambers, simulating elevated CO2 concentration ([CO2]) and high temperature under the following treatments: 1) ambient [CO2] and ambient temperature (Amb); 2) elevated [CO2] (eCO2) and ambient temperature (Elev); 3) ambient [CO2] and high temperature (Amb/Temp); 4) elevated CO2 and high temperature (Elev/Temp). The aim was to evaluate responses to elevated [CO2] and high temperature, with focus on plant development and seed yield, and composition. Elev stimulated grain yield and Amb/Temp had opposite effect. Several biochemical parameters were affected by Amb/Temp, most of them reversed by simultaneous application of Elev. The oil obtained with Elev/Temp had lower degree of unsaturation. A network of relationships among biochemical parameters of grains at three developmental stages revealed that Amb/Temp and Elev/Temp affect significantly both carbohydrate and lipid metabolisms. No significant difference was obtained comparing networks corresponding to Amb and Elev/Temp.

Introduction

Over the past few decades, anthropogenic actions have caused a continuous rise in atmospheric CO2 concentration [CO2]. Recent estimates of [CO2] increment amounts to 1.5 ppm each year. The global average temperature is expected to rise 2.6–4.8 °C by the end of the century (IPCC, 2014). The effects on agriculture are unpredictable and the performance of crops in a new climate scenario is one of the relevant matters deserving concern (Korres et al., 2016).

Evidence has been accumulated that eCO2 and high temperature influence food composition (DaMatta et al., 2010, De Souza et al., 2015). In the short run, these changes may have implications regarding food security (Challinor et al., 2014).

High contents of protein and unsaturated oil make soybean a major food source in most countries. Estimates have shown that 20% of protein and 25% of lipids of the diet of humans and domestic animals are soybeans-derived (Vara Prasad, Allen Jr, & Boote, 2005).

It has been hypothesized that the expected increase of [CO2] and temperature in upcoming years might affect the yield, nutritional quality and contents of carbohydrates, protein and lipids of several crops, including soybean (Thomas et al., 2003, Uprety et al., 2010). Responses of soybean to climate changes have already been detected in recent years. In India, the rainfall peak has shifted from July to August (Ramkete, Gupta & Singh, 2015). Likewise, in the United States, there has been a shift of temperatures from July to August, as well as a shift from average to intense rainfalls (McFadden & Miranowski, 2016).

Crops respond differently to eCO2, depending on whether they are C3 or C4 photosynthetic systems. Responses of C3 plants to eCO2, including soybean, have been intensely studied over the last decades (McFadden & Miranowski, 2016). Using free-air carbon dioxide enrichment (FACE) and open-top chambers (OTC), Bunce (2016) obtained higher soybean yields with eCO2. Results from SoyFACE studies reveals that eCO2 increases the rate of photosynthesis, growth rate, grain yield and C/N rate (Bishop, Leakey, & Ainsworth, 2014). On the other hand, high temperature reduces crop plant biomass due to inhibition of carbon assimilation and increases photorespiration rates (Walker, VanLoocke, Bernacchi, & Ort, 2016). Temperatures above 35 °C reduce soybean yield and quality. Data are available also about soybean responses to either eCO2 or high temperature (Ren et al., 2009, Khan et al., 2011).

Literature containing evidence of combined effects of both eCO2 and high temperature on the yield and composition of grains over the development and grain filling is scarce. Baker, Allen, Boote, Jones and Jones (1989) analyzed the development, growth, total nonstructural carbohydrate, and seed yield of soybean (cv. Bragg) under eCO2 and high temperature. Using data obtained only at the end of the harvest, the authors concluded that the responses to eCO2 are highly dependent on temperature. Although Thomas et al. (2003) observed an effect of eCO2 on the total nonstructural carbohydrates, oil, and fatty acid concentrations, they did not address the combined effects of eCO2 and high temperature over the development of soybean grains.

It has been shown that responses of soybean plants to different climate conditions depend on the cultivar being studied. For example, the concentration of oleic acid of soybean grains of cultivars ‘Essex’, ‘Holladay’ and ‘NK6955’ grown under ozone stress is dependent on [CO2], with highly significant effects depending on the cultivar considered (Uprety et al., 2010). ‘MG/BR-46 Conquista’ is a variety of soybean introduced by the Brazilian state enterprise Embrapa Soybean Division in 1998 and now widely cultivated in Brazil. This variety is very versatile, covering areas ranging from the southeast to the north and northeast of the country. The objectives of the present study were to evaluate the effects of eCO2 (∼800 µmol mol−1) and high temperature (4 °C above ambient), separately and in combination, during growth and filling of the grain of soybean and chemical characteristics at three developmental stages and controlled conditions of temperature and CO2. Besides being the first report on the responses of this widely used soybean variety to the climate change, our study brings the first systemic evaluation of the physiological and biochemical responses of soybean to combined and separate effects of eCO2 and high temperature.

Section snippets

Plant material and growth conditions

The treatments to evaluate the effects of elevated [CO2] and high temperature were carried out in open-top chambers (OTCs) of the laboratory LAFIECO (www.lafieco.com.br), Botany Department, University of São Paulo, Brazil (23° 34′ 1″ S, 46° 43′ 49″ W, 783 m above mean sea level) according to Arenque, Grandis, Pocius, de Souza and Buckeridge (2014) with some modifications.

Soybean seeds of the variety ‘MG/BR-46 Conquista’ were provided by Embrapa Soybean Division (Brasília, DF – Brazil). This

Dry biomass of soybean plants

Leaf and stem biomasses increased until 60 DAE with all treatments. Instead, root biomass continued to increase until 105 DAE. The dry biomasses of leaves, stem, and root were affected by treatments and developmental stages (Fig. 1). Up to 60 DAE, Elev stimulated increments of leaf biomass. Foliar dry biomass was also influenced by senescence, a process that started around 90 DAE. Senescence speed was increased by Elev, Amb/Temp, and Elev/Temp in such a way that green leaves were completely or

Conclusions

The responses of soybean to climate changes, mainly eCO2 and elevated temperature, depend on the crop variety considered. Previous studies have shown changes regarding yield, plant development, and biochemical features. Several changes were observed in the present work, chiefly if eCO2 and high temperature (+4 °C) are analyzed independently. However, when both variables are merged into a combined treatment, most changes are neutralized (a phenomenon named buffering effect), and data regarding

Acknowledgements

The authors would like to thank; CAPES for the fellowships granted; the researcher of the Embrapa Soybean Division Dr. Vanoli Fronza (Londrina-PR) for sending the seeds of the cultivars used; Prof. Dr. Plínio Barbosa de Camargo (CENA-USP) for the contribution in the analysis of carbon and nitrogen. This work has been partly financed by the National Institute of Science and Technology of Bioethanol (INCT-Bioethanol – FAPESP 2008/57908-6 and CNPq 574002/2008-1). AS and MSB are fellow researchers

References (37)

  • A.J. Challinor et al.

    A meta-analysis of crop yield under climate change and adaptation

    Nature Climate Change

    (2014)
  • W.W. Christie

    Preparation of ester derivatives of fatty acids for chromatographic analysis

    Advances in Lipid Methodology

    (1993)
  • G. Csardi et al.

    The igraph software package for complex network research

    InterJournal, Complex Systems

    (2006)
  • S. De Siqueira Santos et al.

    CoGA: An R package to identify differentially co-expressed gene sets by analyzing the graph spectra

    PloS One

    (2015)
  • A.P. De Souza et al.

    Changes in whole-plant metabolism during the grain-filling stage in sorghum grown under elevated CO2 and drought

    Plant Physiology

    (2015)
  • E. Epstein

    Mineral Nutrition of Plants: Principles and perspectives

    (1972)
  • IPCC, (2014). Climate Change 2014: The physical science basis. Contribution of working group I to the fifth assessment...
  • M.A. Islam et al.

    Microalgal species selection for biodiesel production based on fuel properties derived from fatty acid profiles

    Energies

    (2013)
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