Integrative physiology and transcriptome reveal salt-tolerance differences between two licorice species: Ion transport, Casparian strip formation and flavonoids biosynthesis
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ABSTRACT:
SUBMITTER: Li X
PROVIDER: S-EPMC11007891 | biostudies-literature | 2024 Jan
REPOSITORIES: biostudies-literature
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Project description:Plant salt-stress response involves complex physiological processes. Previous studies have shown that some factors promote salt tolerance only under high transpiring condition, thus mediating transpiration-dependent salt tolerance (TDST). However, the mechanism underlying crop TDST remains largely unknown. Here, we report that ZmSTL1 (Salt-Tolerant Locus 1) confers natural variation of TDST in maize. ZmSTL1 encodes a dirigent protein (termed ZmESBL) localized to the Casparian strip (CS) domain. Mutants lacking ZmESBL display impaired lignin deposition at endodermal CS domain which leads to a defective CS barrier. Under salt condition, mutation of ZmESBL increases the apoplastic transport of Na+ across the endodermis, and then increases the root-to-shoot delivery of Na+ via transpiration flow, thereby leading to a transpiration-dependent salt hypersensitivity. Moreover, we show that the ortholog of ZmESBL also mediates CS development and TDST in Arabidopsis. Our study suggests that modification of CS barrier may provide an approach for developing salt-tolerant crops.
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Project description:The endodermis in roots acts as a selectivity filter for nutrient and water transport essential for growth and development. This selectivity is enabled by the formation of lignin-based Casparian strips. Casparian strip formation is initiated by the localization of the Casparian strip domain proteins (CASPs) in the plasma membrane, at the site where the Casparian strip will form. Localized CASPs recruit Peroxidase 64 (PER64), a Respiratory Burst Oxidase Homolog F, and Enhanced Suberin 1 (ESB1), a dirigent-like protein, to assemble the lignin polymerization machinery. However, the factors that control both expression of the genes encoding this biosynthetic machinery and its localization to the Casparian strip formation site remain unknown. Here, we identify the transcription factor, MYB36, essential for Casparian strip formation. MYB36 directly and positively regulates the expression of the Casparian strip genes CASP1, PER64, and ESB1. Casparian strips are absent in plants lacking a functional MYB36 and are replaced by ectopic lignin-like material in the corners of endodermal cells. The barrier function of Casparian strips in these plants is also disrupted. Significantly, ectopic expression of MYB36 in the cortex is sufficient to reprogram these cells to start expressing CASP1-GFP, correctly localize the CASP1-GFP protein to form a Casparian strip domain, and deposit a Casparian strip-like structure in the cell wall at this location. These results demonstrate that MYB36 is controlling expression of the machinery required to locally polymerize lignin in a fine band in the cell wall for the formation of the Casparian strip.
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Project description:Although nitrogen (N) is known to affect mineral element homeostasis in plants, the molecular mechanisms of interactions between N and other nutrients remain largely unclear. We report here that N supply affects ion homeostasis in maize. Berberine hemisulfate staining and a propidium iodide penetration assay showed that N luxury significantly delayed Casparian strip (CS) formation in maize roots. We further demonstrated that N-mediated CS formation in maize was independent of RBOHF-activated H2O2 production. N luxury induced the expression of ZmmiR528 in whole roots and root tips. Knockdown and loss-of-function of ZmmiR528 promoted CS formation under both N-luxury and N-deficient conditions. Both ZmMIR528a and ZmMIR528b contribute to early CS formation under different N conditions. RNA-seq and real-time RT-PCR analysis demonstrated that ZmLAC3, but not ZmLAC5, responded to N treatments. Consistent with results obtained with ZmmiR528 TM transgenic maize and mir528a/b loss-of-function mutants, transgenic maize overexpressing ZmLAC3 displayed early CS formation under different N conditions. Under field conditions, K, Ca, Mn, Cu, Mg, and Zn concentrations were greater in the ear leaf of ZmLAC3-overexpressing transgenic maize than in the wild type. These results indicate that ZmmiR528 affects CS formation in maize by regulating the expression of ZmLAC3, and modification of CS formation has the potential to improve maize quality.
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Project description:Inoculation with plant growth-promoting rhizobacteria can increase plant salt resistance. We aimed to reveal bacterial effects on the formation of apoplastic barriers and hormone concentration in relation to maintaining ion homeostasis and growth of salt-stressed plants. The rhizosphere of a durum wheat variety was inoculated with cytokinin-producing Bacillus subtilis and auxin-producing Pseudomonas mandelii strains. Plant growth, deposition of lignin and suberin and concentrations of sodium, potassium, phosphorus and hormones were studied in the plants exposed to salinity. Accumulation of sodium inhibited plant growth accompanied by a decline in potassium in roots and phosphorus in shoots of the salt-stressed plants. Inoculation with both bacterial strains resulted in faster appearance of Casparian bands in root endodermis and an increased growth of salt-stressed plants. B. subtilis prevented the decline in both potassium and phosphorus concentrations and increased concentration of cytokinins in salt-stressed plants. P. mandelii decreased the level of sodium accumulation and increased the concentration of auxin. Growth promotion was greater in plants inoculated with B. subtilis. Increased ion homeostasis may be related to the capacity of bacteria to accelerate the formation of Casparian bands preventing uncontrolled diffusion of solutes through the apoplast. We discuss the relative impacts of the decline in Na accumulation and maintenance of K and P content for growth improvement of salt-stressed plants and their possible relation to the changes in hormone concentration in plants.
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Project description:A cold-induced transcript encoding a Casparian strip membrane domain (CASP)-like protein (ClCASPL) was identified in watermelon (Citrullus lanatus). Fluorescence microscopy analysis showed that ClCASPL-GFP is localized in the plasma membrane. The orthologous gene in Arabidopsis thaliana (AtCASPL4C1) was also found to play an important role in cold tolerance. Expression analysis using a β-glucuronidase (GUS) reporter reveals that AtCASPL4C1 is widely expressed in a variety of organs and is cold inducible. Analysis of AtCASPL4C1 T-DNA knock-out plants showed altered growth dynamics, faster growth, increased biomass (dry weight) and earlier flowering compared to wild type (Col-0) and ClCASPL overexpressing plants. AtCASPL4C1 knock-out plants showed elevated tolerance to cold stress, while overexpressing CICASPL resulted in increased sensitivity to cold stress in Arabidopsis. Interestingly, AtCASPL4C1 knock-out plants did not display significant alterations in the Casparian strip formation in roots. Thus, the combination of these results suggests a role for CICASPL and AtCASPL4C1 beyond Casparian strip formation in roots, possibly indicating a more fundamental role in vascular tissue.
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Project description:Casparian strips are ring-like cell-wall modifications in the root endodermis of vascular plants. Their presence generates a paracellular barrier, analogous to animal tight junctions, that is thought to be crucial for selective nutrient uptake, exclusion of pathogens, and many other processes. Despite their importance, the chemical nature of Casparian strips has remained a matter of debate, confounding further molecular analysis. Suberin, lignin, lignin-like polymers, or both, have been claimed to make up Casparian strips. Here we show that, in Arabidopsis, suberin is produced much too late to take part in Casparian strip formation. In addition, we have generated plants devoid of any detectable suberin, which still establish functional Casparian strips. In contrast, manipulating lignin biosynthesis abrogates Casparian strip formation. Finally, monolignol feeding and lignin-specific chemical analysis indicates the presence of archetypal lignin in Casparian strips. Our findings establish the chemical nature of the primary root-diffusion barrier in Arabidopsis and enable a mechanistic dissection of the formation of Casparian strips, which are an independent way of generating tight junctions in eukaryotes.
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Project description:Here we show that the CASPARIAN STRIP INTEGRITY FACTOR 2 peptide induces SCHENGEN3 (SGN3) receptor-kinase dependent transcriptional changes both in short-term (30 min) and long-term (480 min) transcriptional changes in roots of Arabidopsis thaliana. We deposit RNA-seq data of wildtype, sgn3, and cif1,2 with or without the CIF2 peptide treatment. Wildtype and cif1,2 presented large transcriptional changes, while the sgn3 receptor mutant showed almost no difference after the treatment.
2020-04-22 | GSE144182 | GEO
Project description:Lignin has enabled plants to colonize land, grow tall, transport water within their bodies, and protect themselves against various stresses. Consequently, this polyphenolic polymer, impregnating cellulosic plant cell walls, is the second most abundant polymer on Earth. Yet, despite its great physiological, ecological, and economical importance, our knowledge of lignin biosynthesis in vivo, especially the polymerization steps within the cell wall, remains vague-specifically, the respective roles of the two polymerizing enzymes classes, laccases and peroxidases. One reason for this lies in the very high numbers of laccases and peroxidases encoded by 17 and 73 homologous genes, respectively, in Arabidopsis Here, we have focused on a specific lignin structure, the ring-like Casparian strips (CSs) within the root endodermis. By reducing candidate numbers using cellular resolution expression and localization data and by boosting stacking of mutants using CRISPR-Cas9, we mutated the majority of laccases in Arabidopsis in a nonuple mutant-essentially abolishing laccases with detectable endodermal expression. Yet, we were unable to detect even slight defects in CS formation. By contrast, we were able to induce a complete absence of CS formation in a quintuple peroxidase mutant. Our findings are in stark contrast to the strong requirement of xylem vessels for laccase action and indicate that lignin in different cell types can be polymerized in very distinct ways. We speculate that cells lignify differently depending on whether lignin is localized or ubiquitous and whether cells stay alive during and after lignification, as well as the composition of the cell wall.
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Project description:Arabidopsis Casparian strip membrane domain proteins (CASPs) form a transmembrane scaffold to recruit lignin biosynthetic enzymes for Casparian strip (CS) formation. Rice is a semi-aquatic plant with a more complex root structure than Arabidopsis to adapt its growing conditions, where the different deposition of lignin and suberin is crucial for adaptive responses. Here, we observed the structure of rice primary and small lateral roots (SLRs), particularly the deposition patterns of lignin and suberin in wild type and Oscasp1 mutants. We found that the appearance time and structure of CS in the roots of rice are different from those of Arabidopsis and observed suberin deposition in the sclerenchyma in wild type roots. Rice CASP1 is highly similar to AtCASPs, but its expression is concentrated in SLR tips and can be induced by salt stress especially in the steles. The loss of OsCASP1 function alters the expression of the genes involved in suberin biosynthesis and the deposition of suberin in the endodermis and sclerenchyma and leads to delayed CS formation and uneven lignin deposition in SLRs. These different depositions may alter nutrient uptake, resulting in ion imbalance in plant, withered leaves, fewer tillers, and reduced tolerance to salt stress. Our findings suggest that OsCASP1 could play an important role in nutrient homeostasis and adaptation to the growth environment.
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