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Plant Responses and Tolerance to Salt Stress: Physiological and Molecular Interventions

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (30 August 2021) | Viewed by 75082

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Special Issue Editors

Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka 1207, Bangladesh
Interests: antioxidants; abiotic stress tolerance; plant metabolites; ROS signaling
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Soil salinity is a common problem in different coastal areas around the world, and over 6% of the land area in the world is salt-affected. Soil salinity is expected to affect the world more vigorously and extensively in the coming years. Salinity exerts both ionic and osmotic stress in plants. Salinity is the most severe factor affecting the growth of plants, and most plants do not fully express their original genetic potential for growth, development, and yield under salt stress, which results in declining economic and commercial value. Due to climate change, the area under salinity stress has been increasing day by day. Therefore, exploring the ways to enhance salt tolerance in plants is one of the vital tasks for plant biologists. Understanding plant physiology and molecular biology and tailoring the traits associated with plant salt tolerance can enhance plant productivity under saline conditions. The study of salt uptake mechanisms, including ion channels and the transporters involved therein, is a new avenue for research. Exploring the genetic potential of halophytes is also a potential scope for biosaline agriculture. In this Special Issue of the International Journal of Molecular Sciences, we aim to publish high-quality research articles and reviews on the understanding of plant responses and tolerance to salt stress.

Prof. Dr. Mirza Hasanuzzaman
Prof. Dr. Masayuki Fujita
Guest Editors

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Keywords

  • salinity
  • salt stress
  • oxidative stress
  • osmotic stress
  • ionic toxicity
  • ion homeostasis
  • halophytes
  • osmolytes
  • biosaline agriculture

Published Papers (20 papers)

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Editorial

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6 pages, 223 KiB  
Editorial
Plant Responses and Tolerance to Salt Stress: Physiological and Molecular Interventions
by Mirza Hasanuzzaman and Masayuki Fujita
Int. J. Mol. Sci. 2022, 23(9), 4810; https://doi.org/10.3390/ijms23094810 - 27 Apr 2022
Cited by 32 | Viewed by 2860
Abstract
Salinity is considered one of the most devastating environmental stresses that drastically curtails the productivity and quality of crops across the world [...] Full article

Research

Jump to: Editorial, Review

17 pages, 3982 KiB  
Article
Genome-Wide Analysis of the Apple CBL Family Reveals That Mdcbl10.1 Functions Positively in Modulating Apple Salt Tolerance
by Peihong Chen, Jie Yang, Quanlin Mei, Huayu Liu, Yunpeng Cheng, Fengwang Ma and Ke Mao
Int. J. Mol. Sci. 2021, 22(22), 12430; https://doi.org/10.3390/ijms222212430 - 18 Nov 2021
Cited by 13 | Viewed by 2026
Abstract
Abiotic stresses are increasingly harmful to crop yield and quality. Calcium and its signaling pathway play an important role in modulating plant stress tolerance. As specific Ca2+ sensors, calcineurin B-like (CBL) proteins play vital roles in plant stress response and calcium signaling. [...] Read more.
Abiotic stresses are increasingly harmful to crop yield and quality. Calcium and its signaling pathway play an important role in modulating plant stress tolerance. As specific Ca2+ sensors, calcineurin B-like (CBL) proteins play vital roles in plant stress response and calcium signaling. The CBL family has been identified in many plant species; however, the characterization of the CBL family and the functional study of apple MdCBL proteins in salt response have yet to be conducted in apple. In this study, 11 MdCBL genes were identified from the apple genome. The coding sequences of these MdCBL genes were cloned, and the gene structure and conserved motifs were analyzed in detail. The phylogenetic analysis indicated that these MdCBL proteins could be divided into four groups. The functional identification in Na+-sensitive yeast mutant showed that the overexpression of seven MdCBL genes could confer enhanced salt stress resistance in transgenic yeast. The function of MdCBL10.1 in regulating salt tolerance was also verified in cisgenic apple calli and apple plants. These results provided valuable insights for future research examining the function and mechanism of CBL proteins in regulating apple salt tolerance. Full article
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19 pages, 5583 KiB  
Article
Heterologous Expression of the Melatonin-Related Gene HIOMT Improves Salt Tolerance in Malus domestica
by Kexin Tan, Jiangzhu Zheng, Cheng Liu, Xianghan Liu, Xiaomin Liu, Tengteng Gao, Xinyang Song, Zhiwei Wei, Fengwang Ma and Chao Li
Int. J. Mol. Sci. 2021, 22(22), 12425; https://doi.org/10.3390/ijms222212425 - 17 Nov 2021
Cited by 9 | Viewed by 1778
Abstract
Melatonin, a widely known indoleamine molecule that mediates various animal and plant physiological processes, is formed from N-acetyl serotonin via N-acetylserotonin methyltransferase (ASMT). ASMT is an enzyme that catalyzes melatonin synthesis in plants in the rate-determining step and is homologous to hydroxyindole-O-methyltransferase (HIOMT) [...] Read more.
Melatonin, a widely known indoleamine molecule that mediates various animal and plant physiological processes, is formed from N-acetyl serotonin via N-acetylserotonin methyltransferase (ASMT). ASMT is an enzyme that catalyzes melatonin synthesis in plants in the rate-determining step and is homologous to hydroxyindole-O-methyltransferase (HIOMT) melatonin synthase in animals. To date, little is known about the effect of HIOMT on salinity in apple plants. Here, we explored the melatonin physiological function in the salinity condition response by heterologous expressing the homologous human HIOMT gene in apple plants. We discovered that the expression of melatonin-related gene (MdASMT) in apple plants was induced by salinity. Most notably, compared with the wild type, three transgenic lines indicated higher melatonin levels, and the heterologous expression of HIOMT enhanced the expression of melatonin synthesis genes. The transgenic lines showed reduced salt damage symptoms, lower relative electrolyte leakage, and less total chlorophyll loss from leaves under salt stress. Meanwhile, through enhanced activity of antioxidant enzymes, transgenic lines decreased the reactive oxygen species accumulation, downregulated the expression of the abscisic acid synthesis gene (MdNCED3), accordingly reducing the accumulation of abscisic acid under salt stress. Both mechanisms regulated morphological changes in the stomata synergistically, thereby mitigating damage to the plants’ photosynthetic ability. In addition, transgenic plants also effectively stabilized their ion balance, raised the expression of salt stress–related genes, as well as alleviated osmotic stress through changes in amino acid metabolism. In summary, heterologous expression of HIOMT improved the adaptation of apple leaves to salt stress, primarily by increasing melatonin concentration, maintaining a high photosynthetic capacity, reducing reactive oxygen species accumulation, and maintaining normal ion homeostasis. Full article
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23 pages, 5118 KiB  
Article
ROS-Scavengers, Osmoprotectants and Violaxanthin De-Epoxidation in Salt-Stressed Arabidopsis thaliana with Different Tocopherol Composition
by Ewa Surówka, Dariusz Latowski, Michał Dziurka, Magdalena Rys, Anna Maksymowicz, Iwona Żur, Monika Olchawa-Pajor, Christine Desel, Monika Krzewska and Zbigniew Miszalski
Int. J. Mol. Sci. 2021, 22(21), 11370; https://doi.org/10.3390/ijms222111370 - 21 Oct 2021
Cited by 5 | Viewed by 2127
Abstract
To determine the role of α- and γ-tocopherol (TC), this study compared the response to salt stress (200 mM NaCl) in wild type (WT) Arabidopsis thaliana (L.) Heynh. And its two mutants: (1) totally TC-deficient vte1; (2) vte4 accumulating γ-TC instead of [...] Read more.
To determine the role of α- and γ-tocopherol (TC), this study compared the response to salt stress (200 mM NaCl) in wild type (WT) Arabidopsis thaliana (L.) Heynh. And its two mutants: (1) totally TC-deficient vte1; (2) vte4 accumulating γ-TC instead of α-TC; and (3) tmt transgenic line overaccumulating α-TC. Raman spectra revealed that salt-exposed α-TC accumulating plants were more flexible in regulating chlorophyll, carotenoid and polysaccharide levels than TC deficient mutants, while the plants overaccumulating γ-TC had the lowest levels of these biocompounds. Tocopherol composition and NaCl concentration affected xanthophyll cycle by changing the rate of violaxanthin de-epoxidation and zeaxanthin formation. NaCl treated plants with altered TC composition accumulated less oligosaccharides than WT plants. α-TC deficient plants increased their oligosaccharide levels and reduced maltose amount, while excessive accumulation of α-TC corresponded with enhanced amounts of maltose. Salt-stressed TC-deficient mutants and tmt transgenic line exhibited greater proline levels than WT plants, lower chlorogenic acid levels, and lower activity of catalase and peroxidases. α-TC accumulating plants produced more methylated proline- and glycine- betaines, and showed greater activity of superoxide dismutase than γ-TC deficient plants. Under salt stress, α-TC demonstrated a stronger regulatory effect on carbon- and nitrogen-related metabolites reorganization and modulation of antioxidant patterns than γ-TC. This suggested different links of α- and γ-TCs with various metabolic pathways via various functions and metabolic loops. Full article
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18 pages, 6271 KiB  
Article
BolTLP1, a Thaumatin-like Protein Gene, Confers Tolerance to Salt and Drought Stresses in Broccoli (Brassica oleracea L. var. Italica)
by Lixia He, Lihong Li, Yinxia Zhu, Yu Pan, Xiuwen Zhang, Xue Han, Muzi Li, Chengbin Chen, Hui Li and Chunguo Wang
Int. J. Mol. Sci. 2021, 22(20), 11132; https://doi.org/10.3390/ijms222011132 - 15 Oct 2021
Cited by 15 | Viewed by 2255
Abstract
Plant thaumatin-like proteins (TLPs) play pleiotropic roles in defending against biotic and abiotic stresses. However, the functions of TLPs in broccoli, which is one of the major vegetables among the B. oleracea varieties, remain largely unknown. In the present study, bolTLP1 was identified [...] Read more.
Plant thaumatin-like proteins (TLPs) play pleiotropic roles in defending against biotic and abiotic stresses. However, the functions of TLPs in broccoli, which is one of the major vegetables among the B. oleracea varieties, remain largely unknown. In the present study, bolTLP1 was identified in broccoli, and displayed remarkably inducible expression patterns by abiotic stress. The ectopic overexpression of bolTLP1 conferred increased tolerance to high salt and drought conditions in Arabidopsis. Similarly, bolTLP1-overexpressing broccoli transgenic lines significantly improved tolerance to salt and drought stresses. These results demonstrated that bolTLP1 positively regulates drought and salt tolerance. Transcriptome data displayed that bolTLP1 may function by regulating phytohormone (ABA, ethylene and auxin)-mediated signaling pathways, hydrolase and oxidoreductase activity, sulfur compound synthesis, and the differential expression of histone variants. Further studies confirmed that RESPONSE TO DESICCATION 2 (RD2), RESPONSIVE TO DEHYDRATION 22 (RD22), VASCULAR PLANT ONE-ZINC FINGER 2 (VOZ2), SM-LIKE 1B (LSM1B) and MALATE DEHYDROGENASE (MDH) physically interacted with bolTLP1, which implied that bolTLP1 could directly interact with these proteins to confer abiotic stress tolerance in broccoli. These findings provide new insights into the function and regulation of bolTLP1, and suggest potential applications for bolTLP1 in breeding broccoli and other crops with increased tolerance to salt and drought stresses. Full article
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14 pages, 28251 KiB  
Article
A C2H2-Type Zinc-Finger Protein from Millettia pinnata, MpZFP1, Enhances Salt Tolerance in Transgenic Arabidopsis
by Zhonghua Yu, Hao Yan, Ling Liang, Yi Zhang, Heng Yang, Wei Li, Jaehyuck Choi, Jianzi Huang and Shulin Deng
Int. J. Mol. Sci. 2021, 22(19), 10832; https://doi.org/10.3390/ijms221910832 - 07 Oct 2021
Cited by 12 | Viewed by 2081
Abstract
C2H2 zinc finger proteins (ZFPs) play important roles in plant development and response to abiotic stresses, and have been studied extensively. However, there are few studies on ZFPs in mangroves and mangrove associates, which represent a unique plant community with robust stress tolerance. [...] Read more.
C2H2 zinc finger proteins (ZFPs) play important roles in plant development and response to abiotic stresses, and have been studied extensively. However, there are few studies on ZFPs in mangroves and mangrove associates, which represent a unique plant community with robust stress tolerance. MpZFP1, which is highly induced by salt stress in the mangrove associate Millettia pinnata, was cloned and functionally characterized in this study. MpZFP1 protein contains two zinc finger domains with conserved QALGGH motifs and targets to the nucleus. The heterologous expression of MpZFP1 in Arabidopsis increased the seeds’ germination rate, seedling survival rate, and biomass accumulation under salt stress. The transgenic plants also increased the expression of stress-responsive genes, including RD22 and RD29A, and reduced the accumulation of reactive oxygen species (ROS). These results indicate that MpZFP1 is a positive regulator of plant responses to salt stress due to its activation of gene expression and efficient scavenging of ROS. Full article
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11 pages, 1632 KiB  
Article
Differential Regulation of NAPDH Oxidases in Salt-Tolerant Eutrema salsugineum and Salt-Sensitive Arabidopsis thaliana
by Maria Pilarska, Dorothea Bartels and Ewa Niewiadomska
Int. J. Mol. Sci. 2021, 22(19), 10341; https://doi.org/10.3390/ijms221910341 - 25 Sep 2021
Cited by 5 | Viewed by 2124
Abstract
Reactive oxygen species (ROS) signalling is crucial in modulating stress responses in plants, and NADPH oxidases (NOXs) are an important component of signal transduction under salt stress. The goal of this research was to investigate whether the regulation of NOX-dependent signalling during mild [...] Read more.
Reactive oxygen species (ROS) signalling is crucial in modulating stress responses in plants, and NADPH oxidases (NOXs) are an important component of signal transduction under salt stress. The goal of this research was to investigate whether the regulation of NOX-dependent signalling during mild and severe salinity differs between the halophyte Eutrema salsugineum and the glycophyte Arabidopsis thaliana. Gene expression analyses showed that salt-induced expression patterns of two NOX genes, RBOHD and RBOHF, varied between the halophyte and the glycophyte. Five days of salinity stimulated the expression of both genes in E. salsugineum leaves, while their expression in A. thaliana decreased. This was not accompanied by changes in the total NOX activity in E. salsugineum, while the activity in A. thaliana was reduced. The expression of the RBOHD and RBOHF genes in E. salsugineum leaves was induced by abscisic acid (ABA) and ethephon spraying. The in silico analyses of promoter sequences of RBOHD and RBOHF revealed multiple cis-acting elements related to hormone responses, and their distribution varied between E. salsugineum and A. thaliana. Our results indicate that, in the halophyte E. salsugineum, the maintenance of the basal activity of NOXs in leaves plays a role during acclimation responses to salt stress. The different expression patterns of the RBOHD and RBOHF genes under salinity in E. salsugineum and A. thaliana point to a modified regulation of these genes in the halophyte, possibly through ABA- and/or ethylene-dependent pathways. Full article
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17 pages, 3023 KiB  
Article
The Jacalin-Related Lectin HvHorcH Is Involved in the Physiological Response of Barley Roots to Salt Stress
by Katja Witzel, Andrea Matros, Uwe Bertsch, Tariq Aftab, Twan Rutten, Eswarayya Ramireddy, Michael Melzer, Gotthard Kunze and Hans-Peter Mock
Int. J. Mol. Sci. 2021, 22(19), 10248; https://doi.org/10.3390/ijms221910248 - 23 Sep 2021
Cited by 8 | Viewed by 1956
Abstract
Salt stress tolerance of crop plants is a trait with increasing value for future food production. In an attempt to identify proteins that participate in the salt stress response of barley, we have used a cDNA library from salt-stressed seedling roots of the [...] Read more.
Salt stress tolerance of crop plants is a trait with increasing value for future food production. In an attempt to identify proteins that participate in the salt stress response of barley, we have used a cDNA library from salt-stressed seedling roots of the relatively salt-stress-tolerant cv. Morex for the transfection of a salt-stress-sensitive yeast strain (Saccharomyces cerevisiae YSH818 Δhog1 mutant). From the retrieved cDNA sequences conferring salt tolerance to the yeast mutant, eleven contained the coding sequence of a jacalin-related lectin (JRL) that shows homology to the previously identified JRL horcolin from barley coleoptiles that we therefore named the gene HvHorcH. The detection of HvHorcH protein in root extracellular fluid suggests a secretion under stress conditions. Furthermore, HvHorcH exhibited specificity towards mannose. Protein abundance of HvHorcH in roots of salt-sensitive or salt-tolerant barley cultivars were not trait-specific to salinity treatment, but protein levels increased in response to the treatment, particularly in the root tip. Expression of HvHorcH in Arabidopsis thaliana root tips increased salt tolerance. Hence, we conclude that this protein is involved in the adaptation of plants to salinity. Full article
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18 pages, 3325 KiB  
Article
Comparative Proteomic Analysis of Tolerant and Sensitive Varieties Reveals That Phenylpropanoid Biosynthesis Contributes to Salt Tolerance in Mulberry
by Tiantian Gan, Ziwei Lin, Lijun Bao, Tian Hui, Xiaopeng Cui, Yanzhen Huang, Hexin Wang, Chao Su, Feng Jiao, Minjuan Zhang and Yonghua Qian
Int. J. Mol. Sci. 2021, 22(17), 9402; https://doi.org/10.3390/ijms22179402 - 30 Aug 2021
Cited by 18 | Viewed by 2288
Abstract
Mulberry, an important woody tree, has strong tolerance to environmental stresses, including salinity, drought, and heavy metal stress. However, the current research on mulberry resistance focuses mainly on the selection of resistant resources and the determination of physiological indicators. In order to clarify [...] Read more.
Mulberry, an important woody tree, has strong tolerance to environmental stresses, including salinity, drought, and heavy metal stress. However, the current research on mulberry resistance focuses mainly on the selection of resistant resources and the determination of physiological indicators. In order to clarify the molecular mechanism of salt tolerance in mulberry, the physiological changes and proteomic profiles were comprehensively analyzed in salt-tolerant (Jisang3) and salt-sensitive (Guisangyou12) mulberry varieties. After salt treatment, the malondialdehyde (MDA) content and proline content were significantly increased compared to control, and the MDA and proline content in G12 was significantly lower than in Jisang3 under salt stress. The calcium content was significantly reduced in the salt-sensitive mulberry varieties Guisangyou12 (G12), while sodium content was significantly increased in both mulberry varieties. Although the Jisang3 is salt-tolerant, salt stress caused more reductions of photosynthetic rate in Jisang3 than Guisangyou12. Using tandem mass tags (TMT)-based proteomics, the changes of mulberry proteome levels were analyzed in salt-tolerant and salt-sensitive mulberry varieties under salt stress. Combined with GO and KEGG databases, the differentially expressed proteins were significantly enriched in the GO terms of amino acid transport and metabolism and posttranslational modification, protein turnover up-classified in Guisangyou12 while down-classified in Jisang3. Through the comparison of proteomic level, we identified the phenylpropanoid biosynthesis may play an important role in salt tolerance of mulberry. We clarified the molecular mechanism of mulberry salt tolerance, which is of great significance for the selection of excellent candidate genes for saline-alkali soil management and mulberry stress resistance genetic engineering. Full article
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17 pages, 2065 KiB  
Article
At the Edges of Photosynthetic Metabolic Plasticity—On the Rapidity and Extent of Changes Accompanying Salinity Stress-Induced CAM Photosynthesis Withdrawal
by Michał Nosek, Katarzyna Gawrońska, Piotr Rozpądek, Marzena Sujkowska-Rybkowska, Zbigniew Miszalski and Andrzej Kornaś
Int. J. Mol. Sci. 2021, 22(16), 8426; https://doi.org/10.3390/ijms22168426 - 05 Aug 2021
Cited by 9 | Viewed by 2537
Abstract
The common ice plant (Mesembryanthemum crystallinum L.) is a facultative crassulacean acid metabolism (CAM) plant, and its ability to recover from stress-induced CAM has been confirmed. We analysed the photosynthetic metabolism of this plant during the 72-h response period following salinity stress [...] Read more.
The common ice plant (Mesembryanthemum crystallinum L.) is a facultative crassulacean acid metabolism (CAM) plant, and its ability to recover from stress-induced CAM has been confirmed. We analysed the photosynthetic metabolism of this plant during the 72-h response period following salinity stress removal from three perspectives. In plants under salinity stress (CAM) we found a decline of the quantum efficiencies of PSII (Y(II)) and PSI (Y(I)) by 17% and 15%, respectively, and an increase in nonphotochemical quenching (NPQ) by almost 25% in comparison to untreated control. However, 48 h after salinity stress removal, the PSII and PSI efficiencies, specifically Y(II) and Y(I), elevated nonphotochemical quenching (NPQ) and donor side limitation of PSI (YND), were restored to the level observed in control (C3 plants). Swelling of the thylakoid membranes, as well as changes in starch grain quantity and size, have been found to be components of the salinity stress response in CAM plants. Salinity stress induced an over 3-fold increase in average starch area and over 50% decline of average seed number in comparison to untreated control. However, in plants withdrawn from salinity stress, during the first 24 h of recovery, we observed chloroplast ultrastructures closely resembling those found in intact (control) ice plants. Rapid changes in photosystem functionality and chloroplast ultrastructure were accompanied by the induction of the expression (within 24 h) of structural genes related to the PSI and PSII reaction centres, including PSAA, PSAB, PSBA (D1), PSBD (D2) and cp43. Our findings describe one of the most flexible photosynthetic metabolic pathways among facultative CAM plants and reveal the extent of the plasticity of the photosynthetic metabolism and related structures in the common ice plant. Full article
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17 pages, 2309 KiB  
Article
Transcriptomic Analysis of Salt-Stress-Responsive Genes in Barley Roots and Leaves
by Rim Nefissi Ouertani, Dhivya Arasappan, Ghassen Abid, Mariem Ben Chikha, Rahma Jardak, Henda Mahmoudi, Samiha Mejri, Abdelwahed Ghorbel, Tracey A. Ruhlman and Robert K. Jansen
Int. J. Mol. Sci. 2021, 22(15), 8155; https://doi.org/10.3390/ijms22158155 - 29 Jul 2021
Cited by 24 | Viewed by 3344
Abstract
Barley is characterized by a rich genetic diversity, making it an important model for studies of salinity response with great potential for crop improvement. Moreover, salt stress severely affects barley growth and development, leading to substantial yield loss. Leaf and root transcriptomes of [...] Read more.
Barley is characterized by a rich genetic diversity, making it an important model for studies of salinity response with great potential for crop improvement. Moreover, salt stress severely affects barley growth and development, leading to substantial yield loss. Leaf and root transcriptomes of a salt-tolerant Tunisian landrace (Boulifa) exposed to 2, 8, and 24 h salt stress were compared with pre-exposure plants to identify candidate genes and pathways underlying barley’s response. Expression of 3585 genes was upregulated and 5586 downregulated in leaves, while expression of 13,200 genes was upregulated and 10,575 downregulated in roots. Regulation of gene expression was severely impacted in roots, highlighting the complexity of salt stress response mechanisms in this tissue. Functional analyses in both tissues indicated that response to salt stress is mainly achieved through sensing and signaling pathways, strong transcriptional reprograming, hormone osmolyte and ion homeostasis stabilization, increased reactive oxygen scavenging, and activation of transport and photosynthesis systems. A number of candidate genes involved in hormone and kinase signaling pathways, as well as several transcription factor families and transporters, were identified. This study provides valuable information on early salt-stress-responsive genes in roots and leaves of barley and identifies several important players in salt tolerance. Full article
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19 pages, 5899 KiB  
Article
Haplotype Analysis of BADH1 by Next-Generation Sequencing Reveals Association with Salt Tolerance in Rice during Domestication
by Myeong-Hyeon Min, Thant Zin Maung, Yuan Cao, Rungnapa Phitaktansakul, Gang-Seob Lee, Sang-Ho Chu, Kyu-Won Kim and Yong-Jin Park
Int. J. Mol. Sci. 2021, 22(14), 7578; https://doi.org/10.3390/ijms22147578 - 15 Jul 2021
Cited by 10 | Viewed by 2476
Abstract
Betaine aldehyde dehydrogenase 1 (BADH1), a paralog of the fragrance gene BADH2, is known to be associated with salt stress through the accumulation of synthesized glycine betaine (GB), which is involved in the response to abiotic stresses. Despite the unclear [...] Read more.
Betaine aldehyde dehydrogenase 1 (BADH1), a paralog of the fragrance gene BADH2, is known to be associated with salt stress through the accumulation of synthesized glycine betaine (GB), which is involved in the response to abiotic stresses. Despite the unclear association between BADH1 and salt stress, we observed the responses of eight phenotypic characteristics (germination percentage (GP), germination energy (GE), germination index (GI), mean germination time (MGT), germination rate (GR), shoot length (SL), root length (RL), and total dry weight (TDW)) to salt stress during the germination stage of 475 rice accessions to investigate their association with BADH1 haplotypes. We found a total of 116 SNPs and 77 InDels in the whole BADH1 gene region, representing 39 haplotypes. Twenty-nine haplotypes representing 27 mutated alleles (two InDels and 25 SNPs) were highly (p < 0.05) associated with salt stress, including the five SNPs that have been previously reported to be associated with salt tolerance. We observed three predominant haplotypes associated with salt tolerance, Hap_2, Hap_18, and Hap_23, which were Indica specific, indicating a comparatively high number of rice accessions among the associated haplotypes. Eight plant parameters (phenotypes) also showed clear responses to salt stress, and except for MGT (mean germination time), all were positively correlated with each other. Different signatures of domestication for BADH1 were detected in cultivated rice by identifying the highest and lowest Tajima’s D values of two major cultivated ecotypes (Temperate Japonica and Indica). Our findings on these significant associations and BADH1 evolution to plant traits can be useful for future research development related to its gene expression. Full article
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12 pages, 2830 KiB  
Article
NaCl-Induced Elicitation Alters Physiology and Increases Accumulation of Phenolic Compounds in Melissa officinalis L.
by Barbara Hawrylak-Nowak, Sławomir Dresler, Maria Stasińska-Jakubas, Magdalena Wójciak, Ireneusz Sowa and Renata Matraszek-Gawron
Int. J. Mol. Sci. 2021, 22(13), 6844; https://doi.org/10.3390/ijms22136844 - 25 Jun 2021
Cited by 16 | Viewed by 2506
Abstract
In nature, plants usually produce secondary metabolites as a defense mechanism against environmental stresses. Different stresses determine the chemical diversity of plant-specialized metabolism products. In this study, we applied an abiotic elicitor, i.e., NaCl, to enhance the biosynthesis and accumulation of phenolic secondary [...] Read more.
In nature, plants usually produce secondary metabolites as a defense mechanism against environmental stresses. Different stresses determine the chemical diversity of plant-specialized metabolism products. In this study, we applied an abiotic elicitor, i.e., NaCl, to enhance the biosynthesis and accumulation of phenolic secondary metabolites in Melissa officinalis L. Plants were subjected to salt stress treatment by application of NaCl solutions (0, 50, or 100 mM) to the pots. Generally, the NaCl treatments were found to inhibit the growth of plants, simultaneously enhancing the accumulation of phenolic compounds (total phenolics, soluble flavonols, anthocyanins, phenolic acids), especially at 100 mM NaCl. However, the salt stress did not disturb the accumulation of photosynthetic pigments and proper functioning of the PS II photosystem. Therefore, the proposed method of elicitation represents a convenient alternative to cell suspension or hydroponic techniques as it is easier and cheaper with simple application in lemon balm pot cultivation. The improvement of lemon balm quality by NaCl elicitation can potentially increase the level of health-promoting phytochemicals and the bioactivity of low-processed herbal products. Full article
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17 pages, 4200 KiB  
Article
Microtubule Dynamics Plays a Vital Role in Plant Adaptation and Tolerance to Salt Stress
by Hyun Jin Chun, Dongwon Baek, Byung Jun Jin, Hyun Min Cho, Mi Suk Park, Su Hyeon Lee, Lack Hyeon Lim, Ye Jin Cha, Dong-Won Bae, Sun Tae Kim, Dae-Jin Yun and Min Chul Kim
Int. J. Mol. Sci. 2021, 22(11), 5957; https://doi.org/10.3390/ijms22115957 - 31 May 2021
Cited by 23 | Viewed by 3200
Abstract
Although recent studies suggest that the plant cytoskeleton is associated with plant stress responses, such as salt, cold, and drought, the molecular mechanism underlying microtubule function in plant salt stress response remains unclear. We performed a comparative proteomic analysis between control suspension-cultured cells [...] Read more.
Although recent studies suggest that the plant cytoskeleton is associated with plant stress responses, such as salt, cold, and drought, the molecular mechanism underlying microtubule function in plant salt stress response remains unclear. We performed a comparative proteomic analysis between control suspension-cultured cells (A0) and salt-adapted cells (A120) established from Arabidopsis root callus to investigate plant adaptation mechanisms to long-term salt stress. We identified 50 differentially expressed proteins (45 up- and 5 down-regulated proteins) in A120 cells compared with A0 cells. Gene ontology enrichment and protein network analyses indicated that differentially expressed proteins in A120 cells were strongly associated with cell structure-associated clusters, including cytoskeleton and cell wall biogenesis. Gene expression analysis revealed that expressions of cytoskeleton-related genes, such as FBA8, TUB3, TUB4, TUB7, TUB9, and ACT7, and a cell wall biogenesis-related gene, CCoAOMT1, were induced in salt-adapted A120 cells. Moreover, the loss-of-function mutant of Arabidopsis TUB9 gene, tub9, showed a hypersensitive phenotype to salt stress. Consistent overexpression of Arabidopsis TUB9 gene in rice transgenic plants enhanced tolerance to salt stress. Our results suggest that microtubules play crucial roles in plant adaptation and tolerance to salt stress. The modulation of microtubule-related gene expression can be an effective strategy for developing salt-tolerant crops. Full article
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16 pages, 3320 KiB  
Article
Functional Characterization of PsnNAC036 under Salinity and High Temperature Stresses
by Xuemei Zhang, Zihan Cheng, Wenjing Yao, Kai Zhao, Xueyi Wang and Tingbo Jiang
Int. J. Mol. Sci. 2021, 22(5), 2656; https://doi.org/10.3390/ijms22052656 - 06 Mar 2021
Cited by 6 | Viewed by 1961
Abstract
Plant growth and development are challenged by biotic and abiotic stresses including salinity and heat stresses. For Populus simonii × P. nigra as an important greening and economic tree species in China, increasing soil salinization and global warming have become major environmental challenges. [...] Read more.
Plant growth and development are challenged by biotic and abiotic stresses including salinity and heat stresses. For Populus simonii × P. nigra as an important greening and economic tree species in China, increasing soil salinization and global warming have become major environmental challenges. We aim to unravel the molecular mechanisms underlying tree tolerance to salt stress and high temprerature (HT) stress conditions. Transcriptomics revealed that a PsnNAC036 transcription factor (TF) was significantly induced by salt stress in P. simonii × P. nigra. This study focuses on addressing the biological functions of PsnNAC036. The gene was cloned, and its temporal and spatial expression was analyzed under different stresses. PsnNAC036 was significantly upregulated under 150 mM NaCl and 37 °C for 12 h. The result is consistent with the presence of stress responsive cis-elements in the PsnNAC036 promoter. Subcellular localization analysis showed that PsnNAC036 was targeted to the nucleus. Additionally, PsnNAC036 was highly expressed in the leaves and roots. To investigate the core activation region of PsnNAC036 protein and its potential regulatory factors and targets, we conducted trans-activation analysis and the result indicates that the C-terminal region of 191–343 amino acids of the PsnNAC036 was a potent activation domain. Furthermore, overexpression of PsnNAC036 stimulated plant growth and enhanced salinity and HT tolerance. Moreover, 14 stress-related genes upregulated in the transgenic plants under high salt and HT conditions may be potential targets of the PsnNAC036. All the results demonstrate that PsnNAC036 plays an important role in salt and HT stress tolerance. Full article
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19 pages, 5546 KiB  
Article
Genome-Wide Identification and Characterization of Wheat 14-3-3 Genes Unravels the Role of TaGRF6-A in Salt Stress Tolerance by Binding MYB Transcription Factor
by Wenna Shao, Wang Chen, Xiaoguo Zhu, Xiaoyi Zhou, Yingying Jin, Chuang Zhan, Gensen Liu, Xi Liu, Dongfang Ma and Yongli Qiao
Int. J. Mol. Sci. 2021, 22(4), 1904; https://doi.org/10.3390/ijms22041904 - 14 Feb 2021
Cited by 22 | Viewed by 2518
Abstract
14-3-3 proteins are a large multigenic family of general regulatory factors (GRF) ubiquitously found in eukaryotes and play vital roles in the regulation of plant growth, development, and response to stress stimuli. However, so far, no comprehensive investigation has been performed in the [...] Read more.
14-3-3 proteins are a large multigenic family of general regulatory factors (GRF) ubiquitously found in eukaryotes and play vital roles in the regulation of plant growth, development, and response to stress stimuli. However, so far, no comprehensive investigation has been performed in the hexaploid wheat. In the present study, A total of 17 potential 14-3-3 gene family members were identified from the Chinese Spring whole-genome sequencing database. The phylogenetic comparison with six 14-3-3 families revealed that the majority of wheat 14-3-3 genes might have evolved as an independent branch and grouped into ε and non-ε group using the phylogenetic comparison. Analysis of gene structure and motif indicated that 14-3-3 protein family members have relatively conserved exon/intron arrangement and motif composition. Physical mapping showed that wheat 14-3-3 genes are mainly distributed on chromosomes 2, 3, 4, and 7. Moreover, most 14-3-3 members in wheat exhibited significantly down-regulated expression in response to alkaline stress. VIGS assay and protein-protein interaction analysis further confirmed that TaGRF6-A positively regulated slat stress tolerance by interacting with a MYB transcription factor, TaMYB64. Taken together, our findings provide fundamental information on the involvement of the wheat 14-3-3 family in salt stress and further investigating their molecular mechanism. Full article
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20 pages, 4733 KiB  
Article
Genome-Wide Identification and Functional Characterization of the Cation Proton Antiporter (CPA) Family Related to Salt Stress Response in Radish (Raphanus sativus L.)
by Yan Wang, Jiali Ying, Yang Zhang, Liang Xu, Wanting Zhang, Meng Ni, Yuelin Zhu and Liwang Liu
Int. J. Mol. Sci. 2020, 21(21), 8262; https://doi.org/10.3390/ijms21218262 - 04 Nov 2020
Cited by 22 | Viewed by 2906
Abstract
The CPA (cation proton antiporter) family plays an essential role during plant stress tolerance by regulating ionic and pH homeostasis of the cell. Radish fleshy roots are susceptible to abiotic stress during growth and development, especially salt stress. To date, CPA family genes [...] Read more.
The CPA (cation proton antiporter) family plays an essential role during plant stress tolerance by regulating ionic and pH homeostasis of the cell. Radish fleshy roots are susceptible to abiotic stress during growth and development, especially salt stress. To date, CPA family genes have not yet been identified in radish and the biological functions remain unclear. In this study, 60 CPA candidate genes in radish were identified on the whole genome level, which were divided into three subfamilies including the Na+/H+ exchanger (NHX), K+ efflux antiporter (KEA), and cation/H+ exchanger (CHX) families. In total, 58 of the 60 RsCPA genes were localized to the nine chromosomes. RNA-seq. data showed that 60 RsCPA genes had various expression levels in the leaves, roots, cortex, cambium, and xylem at different development stages, as well as under different abiotic stresses. RT–qPCR analysis indicated that all nine RsNHXs genes showed up regulated trends after 250 mM NaCl exposure at 3, 6, 12, and 24h. The RsCPA31 (RsNHX1) gene, which might be the most important members of the RsNHX subfamily, exhibited obvious increased expression levels during 24h salt stress treatment. Heterologous over-and inhibited-expression of RsNHX1 in Arabidopsis showed that RsNHX1 had a positive function in salt tolerance. Furthermore, a turnip yellow mosaic virus (TYMV)-induced gene silence (VIGS) system was firstly used to functionally characterize the candidate gene in radish, which showed that plant with the silence of endogenous RsNHX1 was more susceptible to the salt stress. According to our results we provide insights into the complexity of the RsCPA gene family and a valuable resource to explore the potential functions of RsCPA genes in radish. Full article
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Review

Jump to: Editorial, Research

18 pages, 1175 KiB  
Review
Gene Mapping, Cloning and Association Analysis for Salt Tolerance in Rice
by Xiaoru Fan, Hongzhen Jiang, Lijun Meng and Jingguang Chen
Int. J. Mol. Sci. 2021, 22(21), 11674; https://doi.org/10.3390/ijms222111674 - 28 Oct 2021
Cited by 15 | Viewed by 2722
Abstract
Soil salinization caused by the accumulation of sodium can decrease rice yield and quality. Identification of rice salt tolerance genes and their molecular mechanisms could help breeders genetically improve salt tolerance. We studied QTL mapping of populations for rice salt tolerance, period and [...] Read more.
Soil salinization caused by the accumulation of sodium can decrease rice yield and quality. Identification of rice salt tolerance genes and their molecular mechanisms could help breeders genetically improve salt tolerance. We studied QTL mapping of populations for rice salt tolerance, period and method of salt tolerance identification, salt tolerance evaluation parameters, identification of salt tolerance QTLs, and fine-mapping and map cloning of salt tolerance QTLs. We discuss our findings as they relate to other genetic studies of salt tolerance association. Full article
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30 pages, 6959 KiB  
Review
Regulation of Reactive Oxygen Species and Antioxidant Defense in Plants under Salinity
by Mirza Hasanuzzaman, Md. Rakib Hossain Raihan, Abdul Awal Chowdhury Masud, Khussboo Rahman, Farzana Nowroz, Mira Rahman, Kamrun Nahar and Masayuki Fujita
Int. J. Mol. Sci. 2021, 22(17), 9326; https://doi.org/10.3390/ijms22179326 - 28 Aug 2021
Cited by 168 | Viewed by 8185
Abstract
The generation of oxygen radicals and their derivatives, known as reactive oxygen species, (ROS) is a part of the signaling process in higher plants at lower concentrations, but at higher concentrations, those ROS cause oxidative stress. Salinity-induced osmotic stress and ionic stress trigger [...] Read more.
The generation of oxygen radicals and their derivatives, known as reactive oxygen species, (ROS) is a part of the signaling process in higher plants at lower concentrations, but at higher concentrations, those ROS cause oxidative stress. Salinity-induced osmotic stress and ionic stress trigger the overproduction of ROS and, ultimately, result in oxidative damage to cell organelles and membrane components, and at severe levels, they cause cell and plant death. The antioxidant defense system protects the plant from salt-induced oxidative damage by detoxifying the ROS and also by maintaining the balance of ROS generation under salt stress. Different plant hormones and genes are also associated with the signaling and antioxidant defense system to protect plants when they are exposed to salt stress. Salt-induced ROS overgeneration is one of the major reasons for hampering the morpho-physiological and biochemical activities of plants which can be largely restored through enhancing the antioxidant defense system that detoxifies ROS. In this review, we discuss the salt-induced generation of ROS, oxidative stress and antioxidant defense of plants under salinity. Full article
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16 pages, 1957 KiB  
Review
Regulation of Plant Responses to Salt Stress
by Shuangshuang Zhao, Qikun Zhang, Mingyue Liu, Huapeng Zhou, Changle Ma and Pingping Wang
Int. J. Mol. Sci. 2021, 22(9), 4609; https://doi.org/10.3390/ijms22094609 - 28 Apr 2021
Cited by 345 | Viewed by 20061
Abstract
Salt stress is a major environmental stress that affects plant growth and development. Plants are sessile and thus have to develop suitable mechanisms to adapt to high-salt environments. Salt stress increases the intracellular osmotic pressure and can cause the accumulation of sodium to [...] Read more.
Salt stress is a major environmental stress that affects plant growth and development. Plants are sessile and thus have to develop suitable mechanisms to adapt to high-salt environments. Salt stress increases the intracellular osmotic pressure and can cause the accumulation of sodium to toxic levels. Thus, in response to salt stress signals, plants adapt via various mechanisms, including regulating ion homeostasis, activating the osmotic stress pathway, mediating plant hormone signaling, and regulating cytoskeleton dynamics and the cell wall composition. Unraveling the mechanisms underlying these physiological and biochemical responses to salt stress could provide valuable strategies to improve agricultural crop yields. In this review, we summarize recent developments in our understanding of the regulation of plant salt stress. Full article
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