Integrated transcriptomic and proteomic analysis of Tritipyrum provides insights into the molecular basis of salt tolerance

Background Soil salinity is a major environmental stress that restricts crop growth and yield. Methods Here, crucial proteins and biological pathways were investigated under salt-stress and recovery conditions in Tritipyrum ‘Y1805’ using the data-independent acquisition proteomics techniques to explore its salt-tolerance mechanism. Results In total, 44 and 102 differentially expressed proteins (DEPs) were identified in ‘Y1805’ under salt-stress and recovery conditions, respectively. A proteome-transcriptome-associated analysis revealed that the expression patterns of 13 and 25 DEPs were the same under salt-stress and recovery conditions, respectively. ‘Response to stimulus’, ‘antioxidant activity’, ‘carbohydrate metabolism’, ‘amino acid metabolism’, ‘signal transduction’, ‘transport and catabolism’ and ‘biosynthesis of other secondary metabolites’ were present under both conditions in ‘Y1805’. In addition, ‘energy metabolism’ and ‘lipid metabolism’ were recovery-specific pathways, while ‘antioxidant activity’, and ‘molecular function regulator’ under salt-stress conditions, and ‘virion’ and ‘virion part’ during recovery, were ‘Y1805’-specific compared with the salt-sensitive wheat ‘Chinese Spring’. ‘Y1805’ contained eight specific DEPs related to salt-stress responses. The strong salt tolerance of ‘Y1805’ could be attributed to the strengthened cell walls, reactive oxygen species scavenging, osmoregulation, phytohormone regulation, transient growth arrest, enhanced respiration, transcriptional regulation and error information processing. These data will facilitate an understanding of the molecular mechanisms of salt tolerance and aid in the breeding of salt-tolerant wheat.

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Salinity stress-induced modification of pectin activates stress signaling pathways and requires HERK/THE and FER to attenuate the response

10.1101/2020.12.18.423458 ◽

2020 ◽

Author(s):

Nora Gigli-Bisceglia ◽

Eva Van Zelm ◽

Wenying Huo ◽

Jasper Lamers ◽

Christa Testerink

Keyword(s):

Cell Wall ◽

Salt Stress ◽

Signaling Pathways ◽

Stress Responses ◽

Molecular Mechanisms ◽

Structural Integrity ◽

Marker Gene ◽

Mitogen Activated Protein Kinase ◽

Growth And Yield ◽

Receptor Like Kinase

AbstractSoil salinity is an increasing worldwide problem for agriculture, affecting plant growth and yield. In our attempt to understand the molecular mechanisms activated in response to salt in plants, we investigated the Catharanthus roseus Receptor like Kinase 1 Like (CrRLK1L) family, which contains well described sensors previously shown to be involved in maintaining and sensing the structural integrity of the cell walls. We have observed that herk1the1-4 double mutants, lacking the function of the Arabidopsis thaliana Receptor like Kinase HERKULES1 combined with a gain of function allele of THESEUS1, phenocopied the phenotypes previously reported in plants lacking FERONIA (FER) function. We report that both fer-4 and herk1the1-4 mutants respond strongly to salt application, resulting in a more intense activation of early and late stress responses. We also show that salt triggers de-methyl esterification of loosely bound pectins. These cell wall modifications might be partly responsible for the activation of the signaling pathways required to activate salt stress responses. In fact, by adding calcium chloride or by chemically inhibiting pectin methyl esterase (PME) activity we observed reduced activation of the early signaling protein Mitogen Activated Protein Kinase 6 (MPK6) as well as a reduced amplitude in salt-induced marker gene induction. We show that MPK6 is required for the full induction of the salt-induced gene expression markers we tested. However, the sodium specific root halotropism response is likely regulated by a different branch of the pathway being independent of MPK6 or calcium application but influenced by the cell wall sensors FER/HERK1/THE1-4 and PME activity. We hypothesize a model where salt-triggered modification of pectin requires the functionality of FER alone or the HERK1/THE1 combination to attenuate salt responses. Collectively, our results show the complexity of salt stress responses and salt sensing mechanisms and their connection to cell wall modifications, likely being in part responsible for the response phenotypes observed in salt treated plants.

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Improved salt tolerance in transgenic tobacco by over-expression of poplar NAC13 gene

10.7287/peerj.preprints.27861 ◽

2019 ◽

Author(s):

Xuemei Zhang ◽

Zihan Cheng ◽

Kai Zhao ◽

Renhua Li ◽

Boru Zhou ◽

...

Keyword(s):

Transcription Factor ◽

Salt Stress ◽

Salt Tolerance ◽

Transgenic Tobacco ◽

Stress Responses ◽

Gene Networks ◽

Molecular Mechanisms ◽

Physiological Characterization ◽

Protein Functions ◽

Forest Genetic

Background: NACs are one of the major transcription factor families in plants which play an important role in plant growth and development, as well as in adverse stress responses. Methods: In this study, we cloned a salt-inducible NAC transcription factor gene (NAC13) from a poplar variety 84K, followed by transforming it into both tobacco and Arabidopsis. Results: Stable expression analysis of 35S::NAC13-GFP fusion protein in Arabidopsis indicated that NAC13 was localized to the nucleus. We also obtained five transgenic tobacco lines. Evidence from morphological and physiological characterization and salt treatment analyses indicated that the transgenic tobacco enhanced salt tolerance, suggesting that NAC13 gene may function as a positive regulator in tobacco responses to salt stress. Furthermore, evidence from yeast two-hybrid screening demonstrated that NAC13 protein functions as a transcriptional activator, with an activation domain located in the C-terminal region. Discussion: NAC13 gene plays an important role in response to salt stress in tobacco. Future studies are needed to shed light on molecular mechanisms of gene regulation and gene networks related to NAC13 gene in response to salt stress, which will provide a valuable theoretical basis for forest genetic breeding and resistant breeding.

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Improved salt tolerance in transgenic tobacco by over-expression of poplar NAC13 gene

10.7287/peerj.preprints.27861v1 ◽

2019 ◽

Author(s):

Xuemei Zhang ◽

Zihan Cheng ◽

Kai Zhao ◽

Renhua Li ◽

Boru Zhou ◽

...

Keyword(s):

Transcription Factor ◽

Salt Stress ◽

Salt Tolerance ◽

Transgenic Tobacco ◽

Stress Responses ◽

Gene Networks ◽

Molecular Mechanisms ◽

Physiological Characterization ◽

Protein Functions ◽

Forest Genetic

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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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Genome-wide analysis and expression profile of the bZIP gene family in poplar

BMC Plant Biology ◽

10.1186/s12870-021-02879-w ◽

2021 ◽

Vol 21 (1) ◽

Author(s):

Kai Zhao ◽

Song Chen ◽

Wenjing Yao ◽

Zihan Cheng ◽

Boru Zhou ◽

...

Keyword(s):

Salt Stress ◽

Systems Biology ◽

Gene Family ◽

Stress Responses ◽

Metal Ion ◽

Gene Networks ◽

Expression Patterns ◽

Gene Set Enrichment Analysis ◽

Specific Gene ◽

Biological Processes

Abstract Background The bZIP gene family, which is widely present in plants, participates in varied biological processes including growth and development and stress responses. How do the genes regulate such biological processes? Systems biology is powerful for mechanistic understanding of gene functions. However, such studies have not yet been reported in poplar. Results In this study, we identified 86 poplar bZIP transcription factors and described their conserved domains. According to the results of phylogenetic tree, we divided these members into 12 groups with specific gene structures and motif compositions. The corresponding genes that harbor a large number of segmental duplication events are unevenly distributed on the 17 poplar chromosomes. In addition, we further examined collinearity between these genes and the related genes from six other species. Evidence from transcriptomic data indicated that the bZIP genes in poplar displayed different expression patterns in roots, stems, and leaves. Furthermore, we identified 45 bZIP genes that respond to salt stress in the three tissues. We performed co-expression analysis on the representative genes, followed by gene set enrichment analysis. The results demonstrated that tissue differentially expressed genes, especially the co-expressing genes, are mainly involved in secondary metabolic and secondary metabolite biosynthetic processes. However, salt stress responsive genes and their co-expressing genes mainly participate in the regulation of metal ion transport, and methionine biosynthetic. Conclusions Using comparative genomics and systems biology approaches, we, for the first time, systematically explore the structures and functions of the bZIP gene family in poplar. It appears that the bZIP gene family plays significant roles in regulation of poplar development and growth and salt stress responses through differential gene networks or biological processes. These findings provide the foundation for genetic breeding by engineering target regulators and corresponding gene networks into poplar lines.

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Transcriptomic Analysis of Betula halophila in Response to Salt Stress

International Journal of Molecular Sciences ◽

10.3390/ijms19113412 ◽

2018 ◽

Vol 19 (11) ◽

pp. 3412 ◽

Cited By ~ 10

Author(s):

Fenjuan Shao ◽

Lisha Zhang ◽

Iain Wilson ◽

Deyou Qiu

Keyword(s):

Cell Wall ◽

Salt Stress ◽

Salt Tolerance ◽

Expression Patterns ◽

Soil Salinization ◽

Sphingolipid Metabolism ◽

Sequencing Platform ◽

Resistant Varieties ◽

High Salt Tolerance ◽

Salt Overly Sensitive

Soil salinization is a matter of concern worldwide. It can eventually lead to the desertification of land and severely damage local agricultural production and the ecological environment. Betula halophila is a tree with high salt tolerance, so it is of importance to understand and discover the salt responsive genes of B. halophila for breeding salinity resistant varieties of trees. However, there is no report on the transcriptome in response to salt stress in B. halophila. Using Illumina sequencing platform, approximately 460 M raw reads were generated and assembled into 117,091 unigenes. Among these unigenes, 64,551 unigenes (55.12%) were annotated with gene descriptions, while the other 44.88% were unknown. 168 up-regulated genes and 351 down-regulated genes were identified, respectively. These Differentially Expressed Genes (DEGs) involved in multiple pathways including the Salt Overly Sensitive (SOS) pathway, ion transport and uptake, antioxidant enzyme, ABA signal pathway and so on. The gene ontology (GO) enrichments suggested that the DEGs were mainly involved in a plant-type cell wall organization biological process, cell wall cellular component, and structural constituent of cell wall molecular function. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment showed that the top-four enriched pathways were ‘Fatty acid elongation’, ‘Ribosome’, ‘Sphingolipid metabolism’ and ‘Flavonoid biosynthesis’. The expression patterns of sixteen DEGs were analyzed by qRT-PCR to verify the RNA-seq data. Among them, the transcription factor AT-Hook Motif Nuclear Localized gene and dehydrins might play an important role in response to salt stress in B. halophila. Our results provide an important gene resource to breed salt tolerant plants and useful information for further elucidation of the molecular mechanism of salt tolerance in B. halophila.

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A Functional Alternative Oxidase Modulates Plant Salt Tolerance in Physcomitrella patens

Plant and Cell Physiology ◽

10.1093/pcp/pcz099 ◽

2019 ◽

Vol 60 (8) ◽

pp. 1829-1841 ◽

Cited By ~ 5

Author(s):

Guochun Wu ◽

Sha Li ◽

Xiaochuan Li ◽

Yunhong Liu ◽

Shuangshuang Zhao ◽

...

Keyword(s):

Salt Stress ◽

Salt Tolerance ◽

Stress Responses ◽

Alternative Oxidase ◽

Physcomitrella Patens ◽

Redox Homeostasis ◽

Respiratory Pathway ◽

Functional Link ◽

Salt Stress Condition ◽

Plant Salt Tolerance

Abstract Alternative oxidase (AOX) has been reported to be involved in mitochondrial function and redox homeostasis, thus playing an essential role in plant growth as well as stress responses. However, its biological functions in nonseed plants have not been well characterized. Here, we report that AOX participates in plant salt tolerance regulation in moss Physcomitrella patens (P. patens). AOX is highly conserved and localizes to mitochondria in P. patens. We observed that PpAOX rescued the impaired cyanide (CN)-resistant alternative (Alt) respiratory pathway in Arabidopsis thaliana (Arabidopsis) aox1a mutant. PpAOX transcription and Alt respiration were induced upon salt stress in P. patens. Using homologous recombination, we generated PpAOX-overexpressing lines (PpAOX OX). PpAOX OX plants exhibited higher Alt respiration and lower total reactive oxygen species accumulation under salt stress condition. Strikingly, we observed that PpAOX OX plants displayed decreased salt tolerance. Overexpression of PpAOX disturbed redox homeostasis in chloroplasts. Meanwhile, chloroplast structure was adversely affected in PpAOX OX plants in contrast to wild-type (WT) P. patens. We found that photosynthetic activity in PpAOX OX plants was also lower compared with that in WT. Together, our work revealed that AOX participates in plant salt tolerance in P. patens and there is a functional link between mitochondria and chloroplast under challenging conditions.

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Physiological and transcriptomic analyses reveal the mechanisms underlying the salt tolerance of Zoysia japonica Steud.

10.21203/rs.2.16313/v3 ◽

2020 ◽

Author(s):

Jingjing Wang ◽

Cong An ◽

Hailin Guo ◽

Xiangyang Yang ◽

Jingbo Chen ◽

...

Keyword(s):

Signal Transduction ◽

Salt Stress ◽

Stress Response ◽

Salt Tolerance ◽

Molecular Mechanisms ◽

Salt Tolerant ◽

Zoysia Japonica ◽

Salt Stress Response ◽

Leaves And Roots ◽

Time Point

Abstract Background: Areas with saline soils are sparsely populated and have fragile ecosystems, which severely restricts the sustainable development of local economies. Zoysia grasses are recognized as excellent warm-season turfgrasses worldwide, with high salt tolerance and superior growth in saline-alkali soils. However, the mechanism underlying the salt tolerance of Zoysia species remains unknown. Results: The phenotypic and physiological responses of two contrasting materials, Zoysia japonica Steud. Z004 (salt sensitive) and Z011 (salt tolerant) in response to salt stress were studied. The results show that Z011 was more salt tolerant than was Z004, with the former presenting greater K+/Na+ ratios in both its leaves and roots. To study the molecular mechanisms underlying salt tolerance further, we compared the transcriptomes of the two materials at different time points (0 h, 1 h, 24 h, and 72 h) and from different tissues (leaves and roots) under salt treatment. The 24-h time point and the roots might make significant contributions to the salt tolerance. Moreover, GO and KEGG analyses of different comparisons revealed that the key DEGs participating in the salt-stress response belonged to the hormone pathway, various TF families and the DUF family. Conclusions: Z011 may have improved salt tolerance by reducing Na+ transport from the roots to the leaves, increasing K+ absorption in the roots and reducing K+ secretion from the leaves to maintain a significantly greater K+/Na+ ratio. Twenty-four hours might be a relatively important time point for the salt-stress response of zoysiagrass. The auxin signal transduction family, ABA signal transduction family, WRKY TF family and bHLH TF family may be the most important families in Zoysia salt-stress regulation. This study provides fundamental information concerning the salt-stress response of Zoysia and improves the understanding of molecular mechanisms in salt-tolerant plants.

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Identification of Key Genes in ‘Luang Pratahn’, Thai Salt-Tolerant Rice, Based on Time-Course Data and Weighted Co-expression Networks

Frontiers in Plant Science ◽

10.3389/fpls.2021.744654 ◽

2021 ◽

Vol 12 ◽

Author(s):

Pajaree Sonsungsan ◽

Pheerawat Chantanakool ◽

Apichat Suratanee ◽

Teerapong Buaboocha ◽

Luca Comai ◽

...

Keyword(s):

Salt Stress ◽

Salt Tolerance ◽

Stress Responses ◽

Time Course ◽

Rice Variety ◽

Enrichment Analysis ◽

Normal Growth ◽

Growth Conditions ◽

Pathway Enrichment Analysis ◽

Key Genes

Salinity is an important environmental factor causing a negative effect on rice production. To prevent salinity effects on rice yields, genetic diversity concerning salt tolerance must be evaluated. In this study, we investigated the salinity responses of rice (Oryza sativa) to determine the critical genes. The transcriptomes of ‘Luang Pratahn’ rice, a local Thai rice variety with high salt tolerance, were used as a model for analyzing and identifying the key genes responsible for salt-stress tolerance. Based on 3' Tag-Seq data from the time course of salt-stress treatment, weighted gene co-expression network analysis was used to identify key genes in gene modules. We obtained 1,386 significantly differentially expressed genes in eight modules. Among them, six modules indicated a significant correlation within 6, 12, or 48h after salt stress. Functional and pathway enrichment analysis was performed on the co-expressed genes of interesting modules to reveal which genes were mainly enriched within important functions for salt-stress responses. To identify the key genes in salt-stress responses, we considered the two-state co-expression networks, normal growth conditions, and salt stress to investigate which genes were less important in a normal situation but gained more impact under stress. We identified key genes for the response to biotic and abiotic stimuli and tolerance to salt stress. Thus, these novel genes may play important roles in salinity tolerance and serve as potential biomarkers to improve salt tolerance cultivars.

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