Research articleIonomic, metabolomic and proteomic analyses reveal molecular mechanisms of root adaption to salt stress in Tibetan wild barley
Introduction
At present, over 6% of world's total land area is adversely affected by salinity, including approximately 20% of cultivated land and nearly half of irrigated land (Chinnusamy et al., 2005, FAO, 2015). Moreover, soil salinization is still expanding and becoming more serious in the world, mainly due to excessive irrigation and industrial pollution, posing a great threat to agricultural sustainability. Although a few plants, called halophytes, can adapt to high salinity, most cereal crops, including rice (Oryza sativa), wheat (Triticum aestivum), maize (Zea mays) and barley (Hordeum vulgare) are glycophytes, which show reduced growth and yield when exposed to salt stress (Glenn et al., 1999, Horie et al., 2012). Therefore, development of crop cultivars with high salt tolerance is extremely important for increasing crop productivity in saline soils.
Among cereals, barley is considered as the most salt tolerant crop, which can grow normally under 200 mM and even higher salt concentration (Munns and Tester, 2008). Consequently, barley is frequently used as a model crop for physiological and molecular studies on salt tolerance. However, narrower genetic diversity in the cultivated barley has become a limitation for identifying alleles which can be used in breeding program for salt tolerant improvement. On the other hand, wild barley, has a much wider genetic diversity, enriched in elite alleles that allow these accessions to perform better especially under abiotic stress (Nevo et al., 1979, Pakniyat et al., 1997, Dai et al., 2012, Dai et al., 2014). In our previous studies, we confirmed the wider genetic variation of Tibetan wild barley in salt tolerance and identified some accessions, including XZ26, XZ16 and XZ113 which showed even higher salt tolerance than CM72, a well-known salt tolerant cultivar (Qiu et al., 2011, Wu et al., 2011). Physiological and molecular changes in different tissues in responses to stress have been compared between wild and cultivated barley (Wu et al., 2013a, Shen et al., 2016, Shen et al., 2017), but the mechanisms of tissue tolerance to salt stress underlying these wild barley are still little known.
Plant roots are directly exposed to various environmental conditions, and will make the response to abiotic stress firstly. Thus, nutrition and water uptakes by roots are apparently inhibited when plants are subjected to salt stress, resulting in a significant reduction in cell elongation, especially at the root tips (Munns and Tester, 2008). After a long-term salt stress, ion toxicity and metabolic disorders occur in roots (Munns and Tester, 2008, Deinlein et al., 2014). On the other hand, adaptive or tolerant responses occur under salt stress, which maintain nutritional status and turgor pressure (Tester and Davenport, 2003, Shelden et al., 2016). Therefore, many strategies are developed in roots for adaptation to salt stress. For instance, Na sequestration in vacuoles, Na excretion, and elevated K uptake (i.e. Na/K homeostasis) are frequently found in the tolerant genotypes, which alleviate ion toxicity in roots (Tester and Davenport, 2003, Shabala and Cuin, 2008). However, little research has been done to understand comprehensively the whole root adaption to salt stress.
At present, ‘omic’ methodologies are widely used to investigate the abiotic stress tolerance in plants (Nawrot et al., 2016, Meena et al., 2017). Multi-omic methods may give insights into different levels for a better understanding of complex molecular networks underlying the mechanism of abiotic tolerance in plants (Nawrot et al., 2016, Wang et al., 2016). For instance, mass spectrometer (MS)-based proteomic and metabolomic profiling analysis could reflect protein and metabolite changes in different tissues of plants in response to environmental stimulus. Zhang et al. (2012) summarized 2171 salt-regulated proteins among 34 plant species, providing a framework of molecular networks for salt responsible proteins. In barley, proteomic comparison was performed between salt tolerant and sensitive cultivars (Witzel et al., 2014, Rasoulnia et al., 2011), and successfully identified some proteins involved in salt tolerance. Previously we compared proteomic and metabolomic differences in shoots of wild and cultivated barleys in response to salt stress (Wu et al., 2013a, Wu et al., 2013b, Shen et al., 2016). However, no research has been done to clarify the genotypic difference of both the proteomic and metabolomic profiles in the roots responding to salt stress.
In this study, two Tibetan wild barley accessions contrasting in salt tolerance (XZ26, tolerant; XZ169, sensitive) (Shen et al., 2016), were used to compare root ionome, metabolome and proteome profiles in response to 200 mM and 400 mM NaCl at seedling stage. The objective of the present study is to understand the adaptive and integrated strategies in roots of wild barleys to salt stress.
Section snippets
Plant growth and salt treatments
Tibetan wild barley accessions XZ26 and XZ169, differing greatly in salt tolerance (Shen et al., 2016), were used in soil and hydroponic experiments. In the soil experiment, seeds of XZ26 and XZ169 were planted into moist mixed soil of peat/vermiculite (9:1) in a 10 L pot in a growth room (22/18 °C, 14/10 h, day/night), with 250 μm m−2s−1 fluorescent lamps. After 2 weeks growth, seedlings were watered by 1 L 400 mM NaCl solution, watering every 3 d. The seedlings watered by tap water were used
The difference of root growth and ion concentration between two wild barley accessions under salt stress
Two Tibetan wild barley accessions, XZ26 and XZ169 were respectively identified as salt tolerant- and sensitive-genotype in terms of shoot relative dry weights under salt conditions (Shen et al., 2016). In this study, XZ26 also showed better root growth than XZ169 under salt stress in both soil and hydroponic culture (Fig. 1a and b). In the hydroponic experiment, root length was obviously inhibited in XZ169 after 7 d salt treatment (Fig. 1b), reducing by 25% and 37% compared with the control in
Discussion
Potassium (K) and sodium (Na) are generally considered as two competitive elements for uptakes and accumulations in plants under salt stress (Chen et al., 2007). In this study, two Tibetan wild barley accessions differing in salt tolerance, XZ26 and XZ169 had the similar K concentration in roots under normal condition (Fig. 2). Under salt stress condition, K concentration was significantly decreased in the roots of the both accessions, but the tolerant accession (XZ26) remained higher K level
Conclusions
In conclusion, Tibetan wild barley accession XZ26 showed better root growth than XZ169 through its superior root adaptive strategies under salt stress, including maintaining a higher K concentration in roots; accumulating more compatible solutes such as proline and inositol; acquiring greater antioxidant ability for coping with ROS and consuming less energy against salt stress. These findings provide a better understanding of molecular responses of root adaptive strategies to salt stress in the
Authors’ contributions
DZ Wu and QF Shen designed the research. DZ Wu, QF Shen, JH Yu, LB Fu, LY Wu and F Dai performed the research. DZ Wu, LX Jiang and QF Shen analyzed the data. DZ Wu, QF Shen and GP Zhang wrote the article.
Acknowledgments
We are grateful to Prof. Dongfa Sun (Huazhong Agricultural University, China) for providing our seeds of Tibetan wild barley accessions. This research was supported by Natural Science Foundation of China (31330055), Natural Science Foundation of Zhejiang Province, China (LY17C130003), Fundamental Research Funds for the Central Universities (2017FZA6010) and Jiangsu Collaborative Innovation Center for Modern Crop Production.
References (53)
- et al.
Plant salt-tolerance mechanisms
Trends Plant Sci.
(2014) - et al.
Salt-tolerant genes from halophytes are potential key players of salt tolerance in glycophytes
Environ. Exp. Bot.
(2016) - et al.
Antioxidative responses of shoots and roots of wheat to increasing NaCl concentrations
J. Plant Physiol.
(1999) - et al.
Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants
J. Exp. Bot.
(2008) - et al.
Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots
Plant Physiol.
(2009) - et al.
The role of Na+ and K+ transporters in salt stress adaptation in glycophytes
Front. Physiol.
(2017) - et al.
Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development
J. Exp. Bot.
(2012) - et al.
Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid
Plant Physiol.
(2012) - et al.
Screening plants for salt tolerance by measuring K+ flux: a case study for barley
Plant Cell Environ.
(2005) - et al.
Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley
Plant Physiol.
(2007)
Understanding and improving salt tolerance in plants
Crop Sci.
Tibet is one of the centers of domestication of cultivated barley
Proc. Natl. Acad. Sci. USA
Transcriptome profiling reveals mosaic genomic origins of modern cultivated barley
Proc. Natl. Acad. Sci. USA
Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment
J. Exp. Bot.
FAO Land and Plant Nutrition Management Service
Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context
Plant Cell Environ.
Salt tolerance and crop potential of halophytes
Crit. Rev. Plant Sci.
A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress
Plant Cell Environ.
Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants
Rice
Tissue-specific expression and functional complementation of a yeast potassium-uptake mutant by a salt-induced ice plant gene mcSKD1
Plant Mol. Biol.
Epidermal bladder cells confer salinity stress tolerance in the halophyte quinoa and Atriplex species
Plant Cell Environ.
iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis
Plant Physiol.
Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies
Front. Plant Sci.
Salinity tolerance of crops-what is the cost?
New Phytol.
Mechanisms of salinity tolerance
Annu. Rev. Plant Biol.
Arabidopsis thaliana isoprenyl diphosphate synthases produce the C-25 intermediate geranylfarnesyl diphosphate
Plant J.
Cited by (54)
Integrated physiological and transcriptomic analyzes reveal the duality of TiO<inf>2</inf> nanoparticles on alfalfa (Medicago sativa L.)
2024, Ecotoxicology and Environmental SafetyThe mechanism of Ca<sup>2+</sup> signal transduction in plants responding to abiotic stresses
2023, Environmental and Experimental BotanyMetabolomic analysis reveals the molecular responses to copper toxicity in rice (Oryza sativa)
2023, Plant Physiology and BiochemistryIntegrated metabolome, transcriptome analysis, and multi-flux full-length sequencing offer novel insights into the function of lignin biosynthesis as a Sesuvium portulacastrum response to salt stress
2023, International Journal of Biological MacromoleculesTime-course transcriptomics analysis reveals key responses of populus to salt stress
2023, Industrial Crops and ProductsCoordination of root growth with root morphology, physiology and defense functions in response to root pruning in Platycladus orientalis
2022, Journal of Advanced Research