The LRXs-RALFs-FER module controls plant growth and salt stress responses by modulating multiple plant hormones

Abstract Salt stress is a major environmental factor limiting plant growth and productivity. We recently discovered an important new salt tolerance pathway, where the cell wall leucine-rich repeat extensins LRX3/4/5, the RAPID ALKALINIZATION FACTOR (RALF) peptides RALF22/23, and receptor-like kinase FERONIA (FER) function as a module to simultaneously regulate plant growth and salt stress tolerance. However, the intracellular signaling pathways that are regulated by the extracellular LRX3/4/5-RALF22/23-FER module to coordinate growth, cell wall integrity, and salt stress responses are still unknown. Here, we report that the LRX3/4/5-RALF22/23-FER module negatively regulates the levels of jasmonic acid (JA), salicylic acid (SA) and abscisic acid (ABA). Blocking JA pathway rescues the dwarf phenotype of the lrx345 and fer-4 mutants, while disruption of ABA biosynthesis suppresses the salt-hypersensitivity of these mutants. Many salt stress-responsive genes display abnormal expression patterns in the lrx345 and fer-4 mutants, as well as in the wild type plants treated with epigallocatechin gallate (EGCG), an inhibitor of pectin methylesterases, suggesting cell wall integrity as a critical factor that determines the expression pattern of stress-responsive genes. Production of reactive oxygen species (ROS) is constitutively increased in the lrx345 and fer-4 mutants, and inhibition of ROS accumulation suppresses the salt-hypersensitivity of these mutants. Together, our work provides strong evidence that the LRX3/4/5-RALF22/23-FER module controls plant growth and salt stress responses by regulating hormonal homeostasis and ROS accumulation.

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Plant cell wall integrity maintenance and pattern-triggered immunity modulate jointly plant stress responses in Arabidopsis thaliana

10.1101/130013 ◽

2017 ◽

Author(s):

Timo Engelsdorf ◽

Nora Gigli-Bisceglia ◽

Manikandan Veerabagu ◽

Joseph F. McKenna ◽

Frauke Augstein ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Plant Growth ◽

Plant Cell ◽

Stress Responses ◽

Cell Walls ◽

Plant Cell Wall ◽

Cell Wall Integrity ◽

Maintenance Mechanism ◽

Signaling Components

AbstractPlant cells are surrounded by walls, which must often meet opposing functional requirements during plant growth and defense. The cells meet them by modifying wall structure and composition in a tightly controlled and adaptive manner. The modifications seem to be mediated by a dedicated cell wall integrity (CWI) maintenance mechanism. Currently the mode of action of the mechanism is not understood and it is unclear how its activity is coordinated with established plant defense signaling. We investigated responses to induced cell wall damage (CWD) impairing CWI and the underlying mechanism in Arabidopsis thaliana. Interestingly inhibitor- and enzyme-derived CWD induced similar, turgor-sensitive stress responses. Genetic analysis showed that the receptor-like kinase (RLK) FEI2 and the mechano-sensitive, plasma membrane-localized Ca2+- channel MCA1 function downstream of the THE1 RLK in CWD perception. Phenotypic clustering with 27 genotypes identified a core group of RLKs and ion channels, required for activation of CWD responses. By contrast, the responses were repressed by pattern-triggered immune (PTI) signaling components including PEPR1 and 2, the receptors for the immune signaling peptide AtPep1. Interestingly AtPep1 application repressed CWD-induced phytohormone accumulation in a PEPR1/2-dependent manner. These results suggest that PTI suppresses CWD-induced defense responses through elicitor peptide-mediated signaling during defense response activation. If PTI is impaired, the suppression of CWD-induced responses is alleviated, thus compensating for defective PTI.Significance statementStress resistance and plant growth determine food crop yield and efficiency of bioenergy production from ligno-cellulosic biomass. Plant cell walls are essential elements of the biological processes, therefore functional integrity of the cell walls must be maintained throughout. Here we investigate the plant cell wall integrity maintenance mechanism. We characterize its mode of action, identify essential signaling components and show that the AtPep1 signaling peptide apparently coordinates pattern triggered immunity (PTI) and cell wall integrity maintenance in plants. These results suggest how PTI and cell wall modification coordinately regulate biotic stress responses with plants possibly compensating for PTI impairment through enhanced activation of stress responses regulated by the CWI maintenance mechanism.

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ZmACY-1 Antagonistically Regulates Growth and Stress Responses in Nicotiana benthamiana

Frontiers in Plant Science ◽

10.3389/fpls.2021.593001 ◽

2021 ◽

Vol 12 ◽

Author(s):

Dongbin Chen ◽

Junhua Li ◽

Fuchao Jiao ◽

Qianqian Wang ◽

Jun Li ◽

...

Keyword(s):

Salt Stress ◽

Abiotic Stress ◽

Plant Growth ◽

Stress Responses ◽

Nicotiana Benthamiana ◽

Expression Patterns ◽

Balance Of Plant ◽

Drought And Salt Stress ◽

Oxidative Stress Responses ◽

And Oxidative Stress

Aminoacylase-1 is a zinc-binding enzyme that is important in urea cycling, ammonia scavenging, and oxidative stress responses in animals. Aminoacylase-1 (ACY-1) has been reported to play a role in resistance to pathogen infection in the model plant Nicotiana benthamiana. However, little is known about its function in plant growth and abiotic stress responses. In this study, we cloned and analyzed expression patterns of ZmACY-1 in Zea mays under different conditions. We also functionally characterized ZmACY-1 in N. benthamiana. We found that ZmACY-1 is expressed specifically in mature shoots compared with other tissues. ZmACY-1 is repressed by salt, drought, jasmonic acid, and salicylic acid, but is induced by abscisic acid and ethylene, indicating a potential role in stress responses and plant growth. The overexpression of ZmACY-1 in N. benthamiana promoted growth rate by promoting growth-related genes, such as NbEXPA1 and NbEIN2. At the same time, the overexpression of ZmACY-1 in N. benthamiana reduced tolerance to drought and salt stress. With drought and salt stress, the activity of protective enzymes, such as peroxidase (POD), superoxide dismutase (SOD), and catalase (CAT) from micrococcus lysodeikticus was lower; while the content of malondialdehyde (MDA) and relative electrolytic leakage was higher in ZmACY-1 overexpression lines than that in wild-type lines. The results indicate that ZmACY-1 plays an important role in the balance of plant growth and defense and can be used to assist plant breeding under abiotic stress conditions.

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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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The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses inArabidopsis thaliana

Science Signaling ◽

10.1126/scisignal.aao3070 ◽

2018 ◽

Vol 11 (536) ◽

pp. eaao3070 ◽

Cited By ~ 56

Author(s):

Timo Engelsdorf ◽

Nora Gigli-Bisceglia ◽

Manikandan Veerabagu ◽

Joseph F. McKenna ◽

Lauri Vaahtera ◽

...

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Stress Responses ◽

Plant Cell Wall ◽

Cell Wall Integrity ◽

Immune Signaling ◽

Signaling Systems

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Genome-Wide Analysis of the TCP Gene Family in Switchgrass (Panicum virgatum L.)

International Journal of Genomics ◽

10.1155/2019/8514928 ◽

2019 ◽

Vol 2019 ◽

pp. 1-13 ◽

Cited By ~ 2

Author(s):

Yuzhu Huo ◽

Wangdan Xiong ◽

Kunlong Su ◽

Yu Li ◽

Yawen Yang ◽

...

Keyword(s):

Salt Stress ◽

Plant Growth ◽

Gene Family ◽

Stress Responses ◽

Panicum Virgatum ◽

Expression Profiles ◽

Specific Expression ◽

Genome Wide Analysis ◽

Genome Wide ◽

A Genome

The plant-specific transcription factor TCPs play multiple roles in plant growth, development, and stress responses. However, a genome-wide analysis of TCP proteins and their roles in salt stress has not been declared in switchgrass (Panicum virgatum L.). In this study, 42 PvTCP genes (PvTCPs) were identified from the switchgrass genome and 38 members can be anchored to its chromosomes unevenly. Nine PvTCPs were predicted to be microRNA319 (miR319) targets. Furthermore, PvTCPs can be divided into three clades according to the phylogeny and conserved domains. Members in the same clade have the similar gene structure and motif localization. Although all PvTCPs were expressed in tested tissues, their expression profiles were different under normal condition. The specific expression may indicate their different roles in plant growth and development. In addition, approximately 20 cis-acting elements were detected in the promoters of PvTCPs, and 40% were related to stress response. Moreover, the expression profiles of PvTCPs under salt stress were also analyzed and 29 PvTCPs were regulated after NaCl treatment. Taken together, the PvTCP gene family was analyzed at a genome-wide level and their possible functions in salt stress, which lay the basis for further functional analysis of PvTCPs in switchgrass.

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Genome-Wide Identification, Characterization and Expression Patterns of the Pectin Methylesterase Inhibitor Genes in Sorghum bicolor

Genes ◽

10.3390/genes10100755 ◽

2019 ◽

Vol 10 (10) ◽

pp. 755

Author(s):

Angyan Ren ◽

Rana Ahmed ◽

Huanyu Chen ◽

Linhe Han ◽

Jinhao Sun ◽

...

Keyword(s):

Cell Wall ◽

Sorghum Bicolor ◽

Stress Responses ◽

Plant Cell Wall ◽

Defense Mechanism ◽

Expression Patterns ◽

Pectin Methylesterase ◽

Cell Wall Modification ◽

Pectin Methylesterase Inhibitor ◽

Inhibitor Genes

Cell walls are basically complex with dynamic structures that are being involved in several growth and developmental processes, as well as responses to environmental stresses and the defense mechanism. Pectin is secreted into the cell wall in a highly methylesterified form. It is able to perform function after the de-methylesterification by pectin methylesterase (PME). Whereas, the pectin methylesterase inhibitor (PMEI) plays a key role in plant cell wall modification through inhibiting the PME activity. It provides pectin with different levels of degree of methylesterification to affect the cell wall structures and properties. The PME activity was analyzed in six tissues of Sorghum bicolor, and found a high level in the leaf and leaf sheath. PMEI families have been identified in many plant species. Here, a total of 55 pectin methylesterase inhibitor genes (PMEIs) were identified from S. bicolor whole genome, a more detailed annotation of this crop plant as compared to the previous study. Chromosomal localization, gene structures and sequence characterization of the PMEI family were analyzed. Moreover, cis-acting elements analysis revealed that each PMEI gene was regulated by both internal and environmental factors. The expression patterns of each PMEI gene were also clustered according to expression pattern analyzed in 47 tissues under different developmental stages. Furthermore, some SbPMEIs were induced when treated with hormonal and abiotic stress. Taken together, these results laid a strong foundation for further study of the functions of SbPMEIs and pectin modification during plant growth and stress responses of cereal.

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