Transcriptome and Metabolome Analyses Reveal Potential Salt Tolerance Mechanisms Contributing to Maintenance of Water Balance by the Halophytic Grass Puccinellia nuttalliana

Elevated soil salinity exacerbated by human activities and global climate change poses serious threats to plant survival. Although halophytes provide many important clues concerning salt tolerance in plants, some unanswered questions remain to be addressed, including the processes of water and solute transport regulation. We performed high-throughput RNA-sequencing in roots and metabolome characterizations in roots and leaves of Puccinellia nuttalliana halophytic grass subjected to 0 (control) and 150 mM NaCl. In RNAseq, a total of 31 Gb clean bases generated were de novo assembled into 941,894 transcripts. The PIP2;2 and HKT1;5 transcript levels increased in response to the NaCl treatment implying their roles in water and ion homeostasis. Several transcription factors, including WRKY39, DEK3, HY5, and ABF2, were also overexpressed in response to NaCl. The metabolomic analysis revealed that proline and dopamine significantly increased due to the upregulation of the pathway genes under salt stress, likely contributing to salt tolerance mechanisms. Several phosphatidylcholines significantly increased in roots suggesting that the alterations of membrane lipid composition may be an important strategy in P. nuttalliana for maintaining cellular homeostasis and membrane integrity under salt stress. In leaves, the TCA cycle was enriched suggesting enhanced energy metabolism to cope with salt stress. Other features contributing to the ability of P. nuttalliana to survive under high salinity conditions include salt secretion by the salt glands and enhanced cell wall lignification of the root cells. While most of the reported transcriptomic, metabolomics, and structural alterations may have consequences to water balance maintenance by plants under salinity stress, the key processes that need to be further addressed include the role of the changes in the aquaporin gene expression profiles in the earlier reported enhancement of the aquaporin-mediated root water transport.

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Early effects of salt stress on the physiological and oxidative status of the halophyte Lobularia maritima

Functional Plant Biology ◽

10.1071/fp19303 ◽

2020 ◽

Vol 47 (10) ◽

pp. 912

Author(s):

Anis Ben Hsouna ◽

Thaura Ghneim-Herrera ◽

Walid Ben Romdhane ◽

Amira Dabbous ◽

Rania Ben Saad ◽

...

Keyword(s):

Salt Stress ◽

Salt Tolerance ◽

Expression Profiles ◽

Ion Homeostasis ◽

Accumulation Pattern ◽

Moderate Salinity ◽

Lobularia Maritima ◽

Early Effects ◽

Stress Related Genes ◽

Ionic Imbalance

Soil salinity is an abiotic stress that reduces agricultural productivity. For decades, halophytes have been studied to elucidate the physiological and biochemical processes involved in alleviating cellular ionic imbalance and conferring salt tolerance. Recently, several interesting genes with proven influence on salt tolerance were isolated from the Mediterranean halophyte Lobularia maritima (L.) Desv. A better understanding of salt response in this species is needed to exploit its potential as a source of stress-related genes. We report the characterisation of L. maritima’s response to increasing NaCl concentrations (100–400 mM) at the physiological, biochemical and molecular levels. L. maritima growth was unaffected by salinity up to 100 mM NaCl and it was able to survive at 400 mM NaCl without exhibiting visual symptoms of damage. Lobularia maritima showed a Na+ and K+ accumulation pattern typical of a salt-includer halophyte, with higher contents of Na+ in the leaves and K+ in the roots of salt-treated plants. The expression profiles of NHX1, SOS1, HKT1, KT1 and VHA-E1 in salt-treated plants matched this Na+ and K+ accumulation pattern, suggesting an important role for these transporters in the regulation of ion homeostasis in leaves and roots of L. maritima. A concomitant stimulation in phenolic biosynthesis and antioxidant enzyme activity was observed under moderate salinity, suggesting a potential link between the production of polyphenolic antioxidants and protection against salt stress in L. maritima. Our findings indicate that the halophyte L. maritima can rapidly develop physiological and antioxidant mechanisms to adapt to salt and manage oxidative stress.

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De novo transcriptome in roots of switchgrass (Panicum virgatum L.) reveals gene expression dynamic and act network under alkaline salt stress

10.21203/rs.3.rs-57429/v2 ◽

2020 ◽

Author(s):

Pan Zhang ◽

Tianqi Duo ◽

Fengdan Wang ◽

Xunzhong Zhang ◽

Zouzhuan Yang ◽

...

Keyword(s):

Gene Expression ◽

Salt Stress ◽

Salt Tolerance ◽

De Novo ◽

Ion Homeostasis ◽

Antioxidant Systems ◽

Limiting Factor ◽

Rna Seq ◽

Alkaline Salt ◽

Gene Expression Dynamic

Abstract Background: Soil salinization is a major limiting factor for crop cultivation. Switchgrass is a perennial rhizomatous bunchgrass that is considered an ideal plant for marginal lands, including sites with saline soil. Here, we investigated the physiological responses and transcriptome changes in the roots of Alamo (alkali-tolerant genotype) and AM-314/MS-155 (alkali-sensitive genotype) under alkaline salt stress.Results: Alkaline salt stress significantly affected the membrane, osmotic adjustment and antioxidant systems in switchgrass roots, and the ASTTI values between Alamo and AM-314/MS-155 were divergent at different time points. A total of 108,319 unigenes were obtained after reassembly, including 73,636 unigenes in AM-314/MS-155 and 65,492 unigenes in Alamo. A total of 10,219 DEGs were identified, and the number of upregulated genes in Alamo was much greater than that in AM-314/MS-155 in both the early and late stages of alkaline salt stress. The DEGs in AM-314/MS-155 were mainly concentrated in the early stage, while Alamo showed greater advantages in the late stage. These DEGs were mainly enriched in plant-pathogen interactions, ubiquitin-mediated proteolysis and glycolysis/gluconeogenesis pathways. We characterized 1,480 TF genes into 64 TF families, and the most abundant TF family was the C2H2 family, followed by the bZIP and bHLH families. A total of 1,718 PKs were predicted, including CaMK, CDPK, MAPK and RLK. WGCNA revealed that the DEGs in the blue, brown, dark magenta and light steel blue 1 modules were associated with the physiological changes in roots of switchgrass under alkaline salt stress. The consistency between the qRT-PCR and RNA-Seq results confirmed the reliability of the RNA-seq sequencing data. A molecular regulatory network of the switchgrass response to alkaline salt stress was preliminarily constructed on the basis of transcriptional regulation and functional genes.Conclusions: The alkaline salt tolerance of switchgrass may be achieved by the regulation of ion homeostasis, transport proteins, detoxification, heat shock proteins, dehydration and sugar metabolism. These findings provide a comprehensive analysis of gene expression dynamic and act network induced by alkaline salt stress in two switchgrass genotypes and contribute to the understanding of the alkaline salt tolerance mechanism of switchgrass and the improvement of switchgrass germplasm.

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De novo transcriptome in roots of switchgrass (Panicum virgatum L.) reveals gene expression dynamic and act network under alkaline salt stress

BMC Genomics ◽

10.1186/s12864-021-07368-w ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Pan Zhang ◽

Tianqi Duo ◽

Fengdan Wang ◽

Xunzhong Zhang ◽

Zouzhuan Yang ◽

...

Keyword(s):

Gene Expression ◽

Salt Stress ◽

Salt Tolerance ◽

De Novo ◽

Ion Homeostasis ◽

Antioxidant Systems ◽

Limiting Factor ◽

Rna Seq ◽

Alkaline Salt ◽

Gene Expression Dynamic

Abstract Background Soil salinization is a major limiting factor for crop cultivation. Switchgrass is a perennial rhizomatous bunchgrass that is considered an ideal plant for marginal lands, including sites with saline soil. Here we investigated the physiological responses and transcriptome changes in the roots of Alamo (alkaline-tolerant genotype) and AM-314/MS-155 (alkaline-sensitive genotype) under alkaline salt stress. Results Alkaline salt stress significantly affected the membrane, osmotic adjustment and antioxidant systems in switchgrass roots, and the ASTTI values between Alamo and AM-314/MS-155 were divergent at different time points. A total of 108,319 unigenes were obtained after reassembly, including 73,636 unigenes in AM-314/MS-155 and 65,492 unigenes in Alamo. A total of 10,219 DEGs were identified, and the number of upregulated genes in Alamo was much greater than that in AM-314/MS-155 in both the early and late stages of alkaline salt stress. The DEGs in AM-314/MS-155 were mainly concentrated in the early stage, while Alamo showed greater advantages in the late stage. These DEGs were mainly enriched in plant-pathogen interactions, ubiquitin-mediated proteolysis and glycolysis/gluconeogenesis pathways. We characterized 1480 TF genes into 64 TF families, and the most abundant TF family was the C2H2 family, followed by the bZIP and bHLH families. A total of 1718 PKs were predicted, including CaMK, CDPK, MAPK and RLK. WGCNA revealed that the DEGs in the blue, brown, dark magenta and light steel blue 1 modules were associated with the physiological changes in roots of switchgrass under alkaline salt stress. The consistency between the qRT-PCR and RNA-Seq results confirmed the reliability of the RNA-seq sequencing data. A molecular regulatory network of the switchgrass response to alkaline salt stress was preliminarily constructed on the basis of transcriptional regulation and functional genes. Conclusions Alkaline salt tolerance of switchgrass may be achieved by the regulation of ion homeostasis, transport proteins, detoxification, heat shock proteins, dehydration and sugar metabolism. These findings provide a comprehensive analysis of gene expression dynamic and act network induced by alkaline salt stress in two switchgrass genotypes and contribute to the understanding of the alkaline salt tolerance mechanism of switchgrass and the improvement of switchgrass germplasm.

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De novo transcriptome in roots of switchgrass (Panicum virgatum L.) reveals gene expression dynamic and act network under alkaline salt stress

10.21203/rs.3.rs-57429/v3 ◽

2021 ◽

Author(s):

Pan Zhang ◽

Tianqi Duo ◽

Fengdan Wang ◽

Xunzhong Zhang ◽

Zouzhuan Yang ◽

...

Keyword(s):

Gene Expression ◽

Salt Stress ◽

Salt Tolerance ◽

De Novo ◽

Ion Homeostasis ◽

Antioxidant Systems ◽

Limiting Factor ◽

Rna Seq ◽

Alkaline Salt ◽

Gene Expression Dynamic

Abstract Background: Soil salinization is a major limiting factor for crop cultivation. Switchgrass is a perennial rhizomatous bunchgrass that is considered an ideal plant for marginal lands, including sites with saline soil. Here we investigated the physiological responses and transcriptome changes in the roots of Alamo (alkaline-tolerant genotype) and AM-314/MS-155 (alkaline-sensitive genotype) under alkaline salt stress.Results: Alkaline salt stress significantly affected the membrane, osmotic adjustment and antioxidant systems in switchgrass roots, and the ASTTI values between Alamo and AM-314/MS-155 were divergent at different time points. A total of 108,319 unigenes were obtained after reassembly, including 73,636 unigenes in AM-314/MS-155 and 65,492 unigenes in Alamo. A total of 10,219 DEGs were identified, and the number of upregulated genes in Alamo was much greater than that in AM-314/MS-155 in both the early and late stages of alkaline salt stress. The DEGs in AM-314/MS-155 were mainly concentrated in the early stage, while Alamo showed greater advantages in the late stage. These DEGs were mainly enriched in plant-pathogen interactions, ubiquitin-mediated proteolysis and glycolysis/gluconeogenesis pathways. We characterized 1,480 TF genes into 64 TF families, and the most abundant TF family was the C2H2 family, followed by the bZIP and bHLH families. A total of 1,718 PKs were predicted, including CaMK, CDPK, MAPK and RLK. WGCNA revealed that the DEGs in the blue, brown, dark magenta and light steel blue 1 modules were associated with the physiological changes in roots of switchgrass under alkaline salt stress. The consistency between the qRT-PCR and RNA-Seq results confirmed the reliability of the RNA-seq sequencing data. A molecular regulatory network of the switchgrass response to alkaline salt stress was preliminarily constructed on the basis of transcriptional regulation and functional genes.Conclusions: Alkaline salt tolerance of switchgrass may be achieved by the regulation of ion homeostasis, transport proteins, detoxification, heat shock proteins, dehydration and sugar metabolism. These findings provide a comprehensive analysis of gene expression dynamic and act network induced by alkaline salt stress in two switchgrass genotypes and contribute to the understanding of the alkaline salt tolerance mechanism of switchgrass and the improvement of switchgrass germplasm.

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Characterization of Interactions between the Soybean Salt-Stress Responsive Membrane-Intrinsic Proteins GmPIP1 and GmPIP2

Agronomy ◽

10.3390/agronomy11071312 ◽

2021 ◽

Vol 11 (7) ◽

pp. 1312

Author(s):

Jia Liu ◽

Weicong Qi ◽

Haiying Lu ◽

Hongbo Shao ◽

Dayong Zhang

Keyword(s):

Plasma Membrane ◽

Salt Stress ◽

Salt Tolerance ◽

Expression Profiles ◽

Expression Patterns ◽

Gene Expression Profiles ◽

Early Gene ◽

Plant Responses ◽

Constitutive Overexpression ◽

Important Trait

Salt tolerance is an important trait in soybean cultivation and breeding. Plant responses to salt stress include physiological and biochemical changes that affect the movement of water across the plasma membrane. Plasma membrane intrinsic proteins (PIPs) localize to the plasma membrane and regulate the water and solutes flow. In this study, quantitative real-time PCR and yeast two-hybridization were engaged to analyze the early gene expression profiles and interactions of a set of soybean PIPs (GmPIPs) in response to salt stress. A total of 20 GmPIPs-encoding genes had varied expression profiles after salt stress. Among them, 13 genes exhibited a downregulated expression pattern, including GmPIP1;6, the constitutive overexpression of which could improve soybean salt tolerance, and its close homologs GmPIP1;7 and 1;5. Three genes showed upregulated patterns, including the GmPIP1;6 close homolog GmPIP1;4, when four genes with earlier increased and then decreased expression patterns. GmPIP1;5 and GmPIP1;6 could both physically interact strongly with GmPIP2;2, GmPIP2;4, GmPIP2;6, GmPIP2;8, GmPIP2;9, GmPIP2;11, and GmPIP2;13. Definite interactions between GmPIP1;6 and GmPIP1;7 were detected and GmPIP2;9 performed homo-interaction. The interactions of GmPIP1;5 with GmPIP2;11 and 2;13, GmPIP1;6 with GmPIP2;9, 2;11 and GmPIP2;13, and GmPIP2;9 with itself were strengthened upon salt stress rather than osmotic stress. Taken together, we inferred that GmPIP1 type and GmPIP2 type could associate with each other to synergistically function in the plant cell; a salt-stress environment could promote part of their interactions. This result provided new clues to further understand the soybean PIP–isoform interactions, which lead to potentially functional homo- and heterotetramers for salt tolerance.

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OsNAC45 is Involved in ABA Response and Salt Tolerance in Rice

Rice ◽

10.1186/s12284-020-00440-1 ◽

2020 ◽

Vol 13 (1) ◽

Author(s):

Xiang Zhang ◽

Yan Long ◽

Jingjing Huang ◽

Jixing Xia

Keyword(s):

Transcription Factors ◽

Salt Stress ◽

Salt Tolerance ◽

Stress Responses ◽

Crop Yields ◽

Plant Stress ◽

Root Cells ◽

Nac Transcription Factors ◽

Rice Plants ◽

Plant Stress Responses

Abstract Background Salt stress threatens crop yields all over the world. Many NAC transcription factors have been reported to be involved in different abiotic stress responses, but it remains unclear how loss of these transcription factors alters the transcriptomes of plants. Previous reports have demonstrated that overexpression of OsNAC45 enhances salt and drought tolerance in rice, and that OsNAC45 may regulate the expression of two specific genes, OsPM1 and OsLEA3–1. Results Here, we found that ABA repressed, and NaCl promoted, the expression of OsNAC45 in roots. Immunostaining showed that OsNAC45 was localized in all root cells and was mainly expressed in the stele. Loss of OsNAC45 decreased the sensitivity of rice plants to ABA and over-expressing this gene had the opposite effect, which demonstrated that OsNAC45 played an important role during ABA signal responses. Knockout of OsNAC45 also resulted in more ROS accumulation in roots and increased sensitivity of rice to salt stress. Transcriptome sequencing assay found that thousands of genes were differently expressed in OsNAC45-knockout plants. Most of the down-regulated genes participated in plant stress responses. Quantitative real time RT-PCR suggested that seven genes may be regulated by OsNAC45 including OsCYP89G1, OsDREB1F, OsEREBP2, OsERF104, OsPM1, OsSAMDC2, and OsSIK1. Conclusions These results indicate that OsNAC45 plays vital roles in ABA signal responses and salt tolerance in rice. Further characterization of this gene may help us understand ABA signal pathway and breed rice plants that are more tolerant to salt stress.

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Molecular response of canola to salt stress: insights on tolerance mechanisms

10.7287/peerj.preprints.26716 ◽

2018 ◽

Author(s):

Reza Shokri-Gharelo ◽

Pouya Motie-Noparvar

Keyword(s):

Salt Stress ◽

Salt Tolerance ◽

Edible Oils ◽

Biodiesel Fuel ◽

Molecular Response ◽

Salt Tolerant ◽

Tolerance Mechanisms ◽

Brassica Napus L ◽

Salt Response ◽

The Many

Canola (Brassica napus L.) is widely cultivated around the world for the production of edible oils and biodiesel fuel. Despite many canola varieties being described as ‘salt-tolerant’, plant yield and growth decline drastically with increasing salinity. Although many studies have resulted in better understanding of the many important salt-response mechanisms that control salt signaling in plants, detoxification of ions, and synthesis of protective metabolites, the engineering of salt-tolerant crops has only progressed slowly. Genetic engineering has been considered as an efficient method for improving the salt tolerance of canola but there are many unknown or little-known aspects regarding canola response to salinity stress at the cellular and molecular level. In order to develop highly salt-tolerant canola, it is essential to improve knowledge of the salt-tolerance mechanisms, especially the key components of the plant salt-response network. In this review, we focus on studies of the molecular response of canola to salinity to unravel the different pieces of the salt response puzzle. The paper includes a comprehensive review of the latest studies, particularly of proteomic and transcriptomic analysis, including the most recently identified canola tolerance components under salt stress, and suggests where researchers should focus future studies.

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Early signalling processes in roots play a crucial role in the differential salt tolerance in contrasting Chenopodium quinoa accessions

Journal of Experimental Botany ◽

10.1093/jxb/erab388 ◽

2021 ◽

Author(s):

Nadia Bazihizina ◽

Federico Vita ◽

Raffaella Balestrini ◽

Claudia Kiferle ◽

Stefania Caparrotta ◽

...

Keyword(s):

Salt Tolerance ◽

Root Zone ◽

Regulatory Protein ◽

Membrane Integrity ◽

Chenopodium Quinoa ◽

Root Apex ◽

Tolerance Mechanisms ◽

Bladder Cell ◽

Receptor Kinases ◽

Root Plasma Membrane

Abstract Significant variation in epidermal bladder cell (EBC) density and salt tolerance (ST) exists amongst quinoa accessions, suggesting that salt sequestration in EBCs is not the only mechanism conferring ST in this halophyte. In order to reveal other traits that may operate in tandem with salt sequestration in EBCs and whether these additional tolerance mechanisms acted mainly at the root or shoot level, two quinoa (Chenopodium quinoa) accessions with contrasting ST and EBC densities (Q30, low ST with high EBC density versus Q68, with high ST and low EBC density) were studied. The results indicate that responses in roots, rather than in shoots, contributed to the greater ST in the accession with low EBC density. In particular, the tolerant accession had improved root plasma membrane integrity and K+ retention in the mature root zone in response to salt. Furthermore, superior ST in the tolerant Q68 was associated with faster and root-specific H2O2 accumulation and reactive oxygen species-induced K+ and Ca2+ fluxes in the root apex within 30 min after NaCl application. This was found to be associated with the constitutive up-regulation of the membrane-localized receptor kinases regulatory protein FERONIA in the tolerant accession. Taken together, this study shows that differential root signalling events upon salt exposure are essential for the halophytic quinoa; the failure to do this limits quinoa adaptation to salinity, independently of salt sequestration in EBCs.

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Effect of Calcium on Salt Tolerance of Leaf Epidermal Cells of Ruppia maritima at High Salinity

Microscopy and Microanalysis ◽

10.1017/s143192760002599x ◽

1998 ◽

Vol 4 (S2) ◽

pp. 1174-1175

Author(s):

A.D. Barnabas ◽

R. Jagels ◽

W.J. Przybylowicz ◽

J. Mesjasz-Przybylowicz

Keyword(s):

Salt Stress ◽

Sodium Chloride ◽

Salt Tolerance ◽

High Salinity ◽

Epidermal Cells ◽

Transfer Cell ◽

Ruppia Maritima ◽

Terrestrial Plants ◽

Tolerance Mechanisms ◽

Salt Glands

Ruppia maritima L. is a submerged halophyte which occurs frequently in estuaries where sodium chloride is the dominant salt. Unlike terrestrial halophytes, R. maritima does not possess any specialised salt-secreting structures such as salt glands. Knowledge of salt tolerance mechanisms in this plant is important to our understanding of its biology. In a previous study it was shown that leaf epidermal cells of R. maritima, which possess transfer cell characteristics, are implicated in salt regulation. In the present investigation, the effect of calcium (Ca) on salt tolerance of leaf epidermal cells was studied since Ca has been found to be an important factor in resistance to salt stress in terrestrial plants.Plants were grown in artificial seawater of high salinity (33%) and at two different Ca concentrations : 400 ppm (high Ca) and 100 ppm (low Ca).

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