Comprehensive analysis of response and tolerant mechanisms in early-stage soybean at initial-flooding stress

doi:10.1016/j.jprot.2017.01.014

Journal of Proteomics

Volume 169, 3 October 2017, Pages 225-232

https://doi.org/10.1016/j.jprot.2017.01.014 Get rights and content

Highlights

•
Cellular proteins responsive to initial flooding stress in soybean were summarized.
•
The initial flooding responsive nuclear proteins in soybean were presented.
•
The initial flooding responsive cellular and nuclear phosphoproteins were reviewed.
•
The initial flooding tolerance related proteins and genes in soybean were discussed.
•
The location of initial flooding response and tolerance related genes were analyzed.

Abstract

Soybean is one of the most cultivated crops in the world; however, it is very sensitive to flooding stress, which markedly reduces its growth and yield. Morphological and biochemical changes such as an increase of fresh weight and a decrease of ATP content happen in early-stage soybean at initial-flooding stress, indicating that soybean responses to flooding stress are keys for its survival and seedling growth. Phosphoproteomics and nuclear proteomics are useful tools to detect protein-phosphorylation status and to identify transcriptional factors. In the review, the effect of flooding on soybean response to initial flooding stress is discussed based on recent results of proteomic, phosphoproteomic, nuclear proteomic, and nuclear phosphoproteomic studies. In addition, soybean survival under flooding stress, which is defined as tolerance mechanism, is discussed with the results of comprehensive analysis in flooding-tolerant mutant line and abscisic acid-treated soybean.

Biological Significance

Soybean is one of the most cultivated crops in the world; however, it is very sensitive to flooding stress, especially soybean responses to initial flooding stress is key for its survival and seedling growth. Recently, proteomic techniques are applied to investigate the response and tolerant mechanisms of soybean at initial flooding condition. In this review, the progress in proteomic, phosphoproteomic, nuclear proteomic, and nuclear phosphoproteomic studies about the initial-flooding response mechanism in early-stage soybean is presented. In addition, the tolerant mechanism in soybean is discussed with the results of comprehensive analysis in flooding-tolerant mutant line and abscisic acid-treated soybean. Through this review, the key proteins and genes involved in initial flooding response and tolerance at early stage soybean are summarized and they contribute greatly to uncover response and tolerance mechanism at early stage under stressful environmental conditions in soybean.

Graphical abstract

Introduction

Flooding is a complex stress that imposes many constraints to plant growth [1]. The severe constraint is starvation of oxygen and carbon dioxide, which is caused by extremely slow rates of diffusion in water compared to those in air [2]. The exchange of gas such as oxygen between the atmosphere and the plant tissue is reduced by flooding [3]. The limitation of oxygen availability in flooded soil causes hypoxic and anoxia conditions in root [4]. Respiration of root system, which provides substantial reduction in energy status, is inhibited by hypoxic and anoxia conditions [5]. The capacity for ATP production and energy transformation through mitochondrial oxidative phosphorylation was restricted by lower oxygen concentration in flooded plants [6]. Furthermore, flooding leads to change in soil chemical characteristics including soil acidification and redox potential [7], which limits the availability of soil nutrients and causes the accumulation of phytotoxins [8]. These results indicate that plant growth is suppressed under flooding stress through decreasing energy/nutrients supply and accumulating toxic metabolites.

Soybean, which is one of the major agricultural crops, is particularly sensitive to flooding stress [9]. The plant growth and grain yield are markedly reduced in flooded soil [9]. When soybean was treated with flooding at the vegetative growth stage or the reproductive stage, grain yield and quality were reduced compared to untreated soybean [10]. In addition, secondary aerenchyma is formed and worked as an oxygen pathway under flooded conditions [11]. In soybean, flooding stress impaired plant growth by inhibiting root elongation and reducing hypocotyl pigmentation [12]. In root tip of soybean, ubiquitin-mediated proteolysis was activated [13], and cell death was detected under flooding stress [14]. These findings suggest that flooding causes damage to soybean at early stage of growth.

Root tip is comprised of actively dividing cells that develop into primary and lateral roots [15], which plays great roles during water and nutrient uptake [16]. In soybean, root tip is characterized by an open meristem and quiescent center, which is located below the meristem and is mainly composed of a pool of stem cells that are important for root development [17]. Proteomic analysis indicated that root tip is the most sensitive organ to flooding stress compared to root, hypocotyl, and cotyledon [18]. The root tip plays key roles in the development of root structure and responses to environmental stresses, particularly flooding [19]. Based on the above reasons, the study of soybean-root tip is necessary to provide insight into plant responses to flooding stress.

Post-translational modifications such as phosphorylation, acetylation, and glycosylation contribute to plant responses to biotic and abiotic stresses [20]. Phosphorylation is one of the most studied post-translational modifications and a common signaling event occurred upon plant exposure to stresses [21]. Approximately one-third of all eukaryotic proteins are modified by phosphorylation [22]. Phosphorylation leads to changes of protein structure, which directly regulates protein activity and induces interacting partners or subcellular localization [23]. In the present review, the initial (3 h)-response mechanism in early-stage (2- or 3-day-old) soybean under flooding stress is explored based on recent proteomic, phosphoproteomic, and nuclear proteomic studies. In addition, the initial-flooding tolerant mechanism in early-stage soybean is discussed using the results from proteomic and transcriptomic studies.

Section snippets

Characterization of initial-response mechanism in early-stage soybean under flooding stress

Proteomic techniques have been applied up to now to understand the underlying mechanisms of soybean responses to flooding stress [19], [24], [25], [26], [27], [28]. Reactive oxygen species [ROS] scavengers such as ascorbate peroxidase, were decreased in soybean under flooding stress [28], indicating that the ability to remove ROS in soybean was reduced by flooding stress. Proteins involved in glycolysis/fermentation such as enolase and alcohol dehydrogenase were increased under flooding stress

Characterization of initial-response mechanism in early-stage soybean nucleus under flooding stress

The nucleus is the most important cellular organelle because it contains nearly all of the cellular genetic information, which is organized as chromosomes that provide sites for DNA replication and transcription [50]. Nucleus is composed of the inner/outer nuclear membranes, nuclear pore complexes, and nuclear lamina [51]. In nucleus, phospholipid-rich membrane contains sensitive ion channels and pores for the shuttling of various biomolecules across the nuclear membrane through conformational

Comparison between flooding and drought stresses in early-stage soybean

For soybean, another limiting abiotic stress is drought and progressive inhibition of root elongation occurred at long distances from the root tip [75]. Exploration of mechanism of soybean responses to drought might be useful to cultivate tolerant soybean. Recently, the comparative studies between flooding and drought stresses were performed [18], [76]. The common events in root tip of soybean under flooding and drought stresses contained those following aspects. Firstly, protein synthesis was

Characterization of tolerant mechanism in early-stage soybean at initial flooding stress

In soybean, although the mechanism of initial flooding response has been explored using different proteomic techniques [30], [39], [54], [65], the flooding tolerance related proteins and genes have not yet been uncovered. Identification of tolerance related genes is helpful for breeding flooding tolerant plants. For this purpose, proteomics and transcriptomics are useful techniques to screen tolerant genes from flooding tolerant soybean. A flooding-tolerant soybean mutant line was developed

Conclusion and future prospects

In soybean, initial flooding stress was perceived and transmitted into nucleus and led to the decrease of exon-junction complex/Box C/D snoRNPs and histone variants related proteins (Fig. 2). The decrease of these nuclear proteins causes suppression of mRNA export/pre-ribosomal biogenesis and change of chromatin structure (Fig. 2). These changes happened in nucleus continuously regulate cytoplasmic events including inhibition of protein synthesis, alteration of energy metabolism, suppression of

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgements

X. Yin was supported by a scholarship from the Chinese Scholarship Council (201304910204). This work was supported by JSPS KAKENHI Grant Number 15H04445.

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ReviewComprehensive analysis of response and tolerant mechanisms in early-stage soybean at initial-flooding stress

Highlights

Abstract

Biological Significance

Graphical abstract

Introduction

Section snippets

Characterization of initial-response mechanism in early-stage soybean under flooding stress

Characterization of initial-response mechanism in early-stage soybean nucleus under flooding stress

Comparison between flooding and drought stresses in early-stage soybean

Characterization of tolerant mechanism in early-stage soybean at initial flooding stress

Conclusion and future prospects

Conflict of interest

Acknowledgements

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BBA-Gene Struct. Expr.

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Trends Plant Sci.

Phytochemistry

Phytochemistry

Bioorg. Med. Chem.

Plant Sci.

How plants cope with complete submergence

New Phytol.

Response and adaptation by plants to flooding stress

Ann. Bot.

Aeration in higher plants

Flooding stress: acclimations and genetic diversity

Annu. Rev. Plant Biol.

Review: mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism

Funct. Plant Biol.

Soil oxidation-reduction in wetlands and its impact on plant functioning

Biology

QTL analysis of flooding tolerance in soybean at an early vegetative growth stage

Plant Breed.

Formation and function of secondary aerenchyma in hypocotyl, roots and nodules of soybean [Glycine max] under flooded conditions

Plant Soil

Proteome analysis of early-stage soybean seedlings under flooding stress

J. Proteome Res.

Identification of indicator proteins associated with flooding injury in soybean seedlings using label-free quantitative proteomics

J. Proteome Res.

Comparative proteomic profiles of the soybean [Glycine max] root apex and differentiated root zone

Proteomics

The evolution of root hairs and rhizoids

Ann. Bot.

Zonation and organization of root apical meristem of Glycine max

Bull. Torrey Bot. Club

Gel-free/label-free proteomic analysis of endoplasmic reticulum proteins in soybean root tips under flooding and drought stresses

J. Proteome Res.

Proteomics techniques for the development of flood tolerant crops

J. Proteome Res.

Post-translational modification of host proteins in pathogen-triggered deference signalling in plants

Mol. Plant Pathol.

Phosphorylation of proteins in plants: regulatory effects and potential involvement in stimulus/response coupling

Annu. Rev. Plant Physiol.

Directional and quantitative phosphorylation networks

Brief Funct. Genomic. Proteomic.

Organ-specific proteome analysis for identification of abiotic stress response mechanism in crop

Front. Plant Sci.

Proteomic techniques and management of flooding tolerance in soybean

J. Proteome Res.

‘Omics’ techniques and their use to identify how soybean responds to flooding

J. Anal. Sci. Technol.

Review
Comprehensive analysis of response and tolerant mechanisms in early-stage soybean at initial-flooding stress