Elsevier

Plant Physiology and Biochemistry

Volume 86, January 2015, Pages 109-120
Plant Physiology and Biochemistry

Research article
Understanding abiotic stress tolerance mechanisms in soybean: A comparative evaluation of soybean response to drought and flooding stress

https://doi.org/10.1016/j.plaphy.2014.11.010Get rights and content

Highlights

  • Under drought stress photosynthesis was mainly affected by an increase in ABA.

  • Starch accumulation in leaves affected photosynthesis under flooding stress.

  • Drought stress increased the number and size of plastoglobules in leaf chloroplast.

  • Fibrillin proteins are involved in soybean response to drought and flooding.

Abstract

Many sources of drought and flooding tolerance have been identified in soybean, however underlying molecular and physiological mechanisms are poorly understood. Therefore, it is important to illuminate different plant responses to these abiotic stresses and understand the mechanisms that confer tolerance. Towards this goal we used four contrasting soybean (Glycine max) genotypes (PI 567690 – drought tolerant, Pana – drought susceptible, PI 408105A – flooding tolerant, S99-2281 – flooding susceptible) grown under greenhouse conditions and compared genotypic responses to drought and flooding at the physiological, biochemical, and cellular level. We also quantified these variations and tried to infer their role in drought and flooding tolerance in soybean. Our results revealed that different mechanisms contribute to reduction in net photosynthesis under drought and flooding stress. Under drought stress, ABA and stomatal conductance are responsible for reduced photosynthetic rate; while under flooding stress, accumulation of starch granules played a major role. Drought tolerant genotypes PI 567690 and PI 408105A had higher plastoglobule numbers than the susceptible Pana and S99-2281. Drought stress increased the number and size of plastoglobules in most of the genotypes pointing to a possible role in stress tolerance. Interestingly, there were seven fibrillin proteins localized within the plastoglobules that were up-regulated in the drought and flooding tolerant genotypes PI 567690 and PI 408105A, respectively, but down-regulated in the drought susceptible genotype Pana. These results suggest a potential role of Fibrillin proteins, FBN1a, 1b and 7a in soybean response to drought and flooding stress.

Introduction

Drought, flooding, high temperature, cold, salinity, and nutrient availability are abiotic factors that have a huge impact on world agriculture and account for more than 50% reduction in average potential yields for most major crops (Wang et al., 2003). As climate prediction models show increased occurrences of drought, flooding, and high temperature spells during the crop growing periods (IPCC, 2008, Mittler and Blumwald, 2010), global food production will continue to be challenged. The demand for food and oil crops will continue to rise with the increase in global population; therefore improving productivity to ensure sustainable yields under changing environmental conditions is essential. To achieve global food security there is a need to increase our understanding of plant responses to abiotic stress with an aim of breeding crops that can maintain higher photosynthetic rates, better growth, and improved yield under stress conditions (Condon et al., 2004, Morison et al., 2008). Some level of success has been achieved in crop breeding for tolerance to abiotic stresses through genetic manipulation of transcription factors (TFs), late embryogenesis abundant (LEA) proteins, and antioxidant proteins (Umezawa et al., 2006, Bhatnagar-Mathur et al., 2008). However, research programs aimed at developing tolerance to a particular stress do not necessarily test susceptibility to other abiotic stresses and this can have unforeseen consequences.

Although irrigation can be used as a strategy to overcome the effects of drought stress on crop yields, the available water resources continue to decline. Therefore, adapting crops to water-limited environments and improving their water use efficiency will be crucial for developing climate-resilient cultivars that are capable of producing more food per unit of water used. Drought stress causes tissue dehydration which is characterized by fundamental changes in water relations, physiological and biochemical processes, membrane structure, as well as ultrastructure of subcellular organelles (Sarafis, 1998, Yordanov et al., 2003). At the whole-plant level, drought stress leads to a progressive suppression of photosynthesis caused by stomatal and non-stomatal limitations (Wise et al., 1992, Yordanov et al., 2003). Tolerant genotypes should not only be able to retain sufficient water under drought, but also have a highly active system for protection against oxidative stress injury.

Flooding affects about 10% of the global land area (Setter and Waters, 2003). In the USA alone 16% of soils are affected by waterlogging and the economic losses for crop production are estimated to be the second largest after drought (Zhou, 2010). Yield losses resulting from flooding depend on the plant species and age, soil type, and duration of flooding. Despite knowledge of adaptive mechanisms and regulation at the molecular level, understanding of the mechanisms behind plant response to flooding is very limited. Studies with Arabidopsis (Arabidopsis thaliana) (Gonzali et al., 2005) and rice (Oryza sativa) (Hattori et al., 2009, Xu et al., 2006, Singh et al., 2010) have shown that there are many genes associated with flooding responses suggesting that the regulation of flooding tolerance in plants is complex. Many studies have looked into the mechanisms underlying the responses to flooding stress using model plants (Vashisht et al., 2011) as well as crop species (Setter and Waters, 2003, Zaidi et al., 2004, Rhine et al., 2010) however very few studies have looked at this at the whole plant and cellular level.

Plastoglobules are lipoprotein bodies attached to the thylakoids (Austin et al., 2006) that store lipids and antioxidants such as tocopherols, carotenes, and plastoquinones (Steinmuller and Tevini, 1985) and also contain tocopherol cyclase, which is involved in α-tocopherol synthesis (Austin et al., 2006, Vidi et al., 2006). Plastoglobules contain fibrillins, which are ubiquitous proteins that maintain plastoglobule structural integrity (Langenkamper et al., 2001, Vidi et al., 2006, Brehelin et al., 2007) and stabilize the photosynthetic apparatus during photo-oxidative stress (Yang et al., 2006, Youssef et al., 2010), osmotic stress (Gillet et al., 1998), drought (Rey et al., 2000), and low temperature (Rorat et al., 2001). Even though some studies have been conducted to dissect the role of plastoglobules in model (Ytterberg et al., 2006, Giacomelli et al., 2006) and some horticultural plants (Chen et al., 1998, Gillet et al., 1998), no information on major crops such as soybean is available for drought and flooding conditions.

Soybean is the world's most widely grown seed legume, providing an inexpensive source of protein and vegetable oil for human consumption. This important legume crop is adapted to grow in a wide range of climatic conditions; however, soybean growth, development, and yield are greatly affected by several abiotic stressors, such as; flooding (Komatsu et al., 2012, Khatoon et al., 2012), drought (Mohammadi et al., 2012), and salinity (Sobhanian et al., 2010). As in other major crops, breeding for drought tolerance in soybean has been a challenge because of the inherent complexity of breeding for drought tolerance combined with a lack of physiological perspective in the dissection of traits (Sadok and Sinclair, 2011) and limited drought tolerant germplasm resources (Carter et al., 1999, Carter et al., 2004). Traits that have been targeted for drought tolerance in soybean include deeper rooting system, sustained nitrogen fixation (Sinclair et al., 2007), slow canopy wilting (Sloane et al., 1990; Hufstetler et al., 2007; King et al., 2009) and water use efficiency. The slow wilting trait in soybean suggests a conservative water use strategy by some genotypes and has been used in breeding for drought tolerance. Even though there has been some success in breeding for abiotic stress tolerance in soybean, the underlying molecular and physiological mechanisms involved in drought and flooding tolerance are still poorly understood. Previous studies explored some morphological (Benjamin and Nielsen, 2006, Wang et al., 2012), physiological and biochemical (Sloane et al., 1990, Agarwal et al., 2005, Manavalan et al., 2009) and molecular (Ahuja et al., 2010, Stolf-Moreira et al., 2010, Manavalan et al., 2009) aspects in an effort to understand drought tolerance mechanisms in soybean; however, there is still limited information at the cellular and biochemical levels. Photosynthetic efficiency which is crucial for maximum yields is negatively affected by abiotic stress. In this study we looked at the role of some of the processes that will affect photosynthesis under drought and flooding stress. Using contrasting genotypes we compared soybean responses to drought and flooding stress at the physiological, biochemical, and cellular level, quantified these responses and tried to infer their role in soybean drought and flooding tolerance.

Section snippets

Growing conditions

Four contrasting soybean (Glycine max) genotypes were used in this experiment: PI 567690 – drought tolerant (DT), Pana (PI 597387) – drought susceptible (DS) (Pathan et al., 2014), PI 408105A – flooding tolerant (FT) and S99-2281 (PI 654356) – flooding susceptible (FS). The plants were grown under a 14 h photoperiod and optimum temperature 28/18 °C day/night at the Division of Plant Sciences greenhouses, University of Missouri, Columbia. A mixture of soil and sand (2:1) was used in 26.5-L pots

Results

Relative water content varied significantly among genotypes, with treatment as well as the interaction between genotype and treatment at P = 0.0005, <0.0001 and 0.0051 respectively (Table 1). At severe drought stress leaf relative water content ranged from 50.6 to 58.1% (Fig. 1A). Net photosynthesis, stomatal conductance, and internal carbon dioxide concentration (Ci) varied significantly among the genotypes studied (P < 0.0001, 0.0001 and 0.0165, respectively) and in response to stress (P

Discussion

Changes in water status (drought or flooding) have an impact on the plant growth and development. Although these abiotic stresses result in a decrease in photosynthetic rate, our study revealed that different mechanisms are responsible for this reduction.

Conclusion

Drought and flooding stress reduces photosynthetic rate in soybean. Under drought stress, reduction in photosynthetic rate is mainly due to a reduction in stomatal conductance caused by increased ABA concentration in the leaves. Different studies have shown that there are several factors that may cause the reduction in photosynthetic rate under flooding conditions, however our results indicate that starch accumulation in leaves play a key role in this reduction. Under stress conditions,

Authors' contribution

1. Raymond N. Mutava, Silvas Jebakumar Prince K., Naeem Hasan Syed: Contributed equally in objectives formulation, experimental design and set up, data collection, analysis and interpretation.

2. Li Song and Wei Chen: Did all tissue collection, DNA extraction and qRT-PCR analysis.

3. Babu Valliyodan: Coordinated biochemical analysis.

4. Henry T. Nguyen: Provided guidance and all other support that was needed to complete this research.

Acknowledgments

We would like to thank Dr. J. Grover Shannon (University of Missouri) for providing information on drought and flooding tolerance scores, Juliana P. Arndt (The Electron Microscopy Core Facility, University of Missouri) for the TEM samples preparation, Haiying Shi (Molecular Genetics & Soybean Genomics Laboratory, University of Missouri) for sugar analyses and Theresa Musket for manuscript language editing.

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