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Root system architecture analysis in Mesembryanthemum crystallinum (ice plant) seedlings reveals characteristic root halotropic response.

ABSTRACT: One of the major environmental stress factors that affect root growth is salinity. Arabidopsis thaliana, a glycophyte, shows halotropism, whereby it alters the direction of root growth in a non-gravitropic pattern to evade high soil salinity. Asymmetric auxin distribution regulated by the relocation of auxin-efflux carrier proteins is a key cellular event in the halotropic response. However, there are no reports of halotropism in halophytes. Here, we investigated root growth traits in Mesembryanthemum crystallinu m (ice plant), under high salinity conditions. We hypothesized that ice plant roots would show halotropic responses different from those of Arabidopsis Notably, similar to halotropism observed in Arabidopsis, ice plant roots showed continuous root bending under salinity stress. However, the root elongation rate did not change in ice plants. Expression analyses of several genes revealed that auxin transport might be partially involved in ice plant halotropism. This study enhances our understanding of halophyte root adaptation to high salinity stress.

SUBMITTER: Otsuka M

PROVIDER: S-EPMC8034872 | biostudies-literature | 2021 Mar

REPOSITORIES: biostudies-literature

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Root system architecture analysis in Mesembryanthemum crystallinum (ice plant) seedlings reveals characteristic root halotropic response.

Otsuka Mayuko M Kato Hikaru H Yamada Shyota S Nakayama Tatsuhiko T Sakaoka Satomi S Morikami Atsushi A Tsukagoshi Hironaka H

Biology open 20210329 3

One of the major environmental stress factors that affect root growth is salinity. Arabidopsis thaliana, a glycophyte, shows halotropism, whereby it alters the direction of root growth in a non-gravitropic pattern to evade high soil salinity. Asymmetric auxin distribution regulated by the relocation of auxin-efflux carrier proteins is a key cellular event in the halotropic response. However, there are no reports of halotropism in halophytes. Here, we investigated root growth traits in ...[more]

PMID: 32816696

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Project description:The halophyte Mesembryanthemum crystallinum (common or crystalline ice plant) is a useful model for studying molecular mechanisms of salt tolerance. The morphology, physiology, metabolism, and gene expression of ice plant have been studied and large-scale analyses of gene expression profiling have drawn an outline of salt tolerance in ice plant. A rapid root growth to a sudden increase in salinity was observed in ice plant seedlings. Using a fluorescent dye to detect Na(+), we found that ice plant roots respond to an increased flux of Na(+) by either secreting or storing Na(+) in specialized cells. High-throughput sequencing was used to identify small RNA profiles in 3-day-old seedlings treated with or without 200 mM NaCl. In total, 135 conserved miRNAs belonging to 21 families were found. The hairpin precursor of 19 conserved mcr-miRNAs and 12 novel mcr-miRNAs were identified. After 6 h of salt stress, the expression of most mcr-miRNAs showed decreased relative abundance, whereas the expression of their corresponding target genes showed increased mRNA relative abundance. The cognate target genes are involved in a broad range of biological processes: transcription factors that regulate growth and development, enzymes that catalyze miRNA biogenesis for the most conserved mcr-miRNA, and proteins that are involved in ion homeostasis and drought-stress responses for some novel mcr-miRNAs. Analyses of the functions of target genes revealed that cellular processes, including growth and development, metabolism, and ion transport activity are likely to be enhanced in roots under salt stress. The expression of eleven conserved miRNAs and two novel miRNAs were correlated reciprocally with predicted targets within hours after salt stress exposure. Several conserved miRNAs have been known to regulate root elongation, root apical meristem activity, and lateral root formation. Based upon the expression pattern of miRNA and target genes in combination with the observation of Na(+) distribution, ice plant likely responds to increased salinity by using Na(+) as an osmoticum for cell expansion and guard cell opening. Excessive Na(+) could either be secreted through the root epidermis or stored in specialized leaf epidermal cells. These responses are regulated in part at the miRNA-mediated post-transcriptional level.

Project description:BackgroundIce plant (Mesembryanthemum crystallinum L.) is a model plant for studying salt-tolerant mechanisms in higher plants. Many salt stress-responsive ice plant genes have been identified with molecular and biochemical approaches. However, no further functional characterization of these genes in host plant due to lack of easy and effective transformation protocols.ResultsTo establish efficient transformation system of ice plants, three types of ice plant materials, hypocotyl-derived callus, aseptically-grown seedlings and pot-grown juvenile plants, were used to develop Agrobacterium-mediated transformation protocols. The highest transient transformation efficiency was with 5-day-old ice plant callus co-incubated with an Agrobacterium tumefaciens at 2.5 × 109 cells mL-1 for 48 h. The 3-day-old ice plant seedlings with root tip removed were successfully infected with A. tumefaciens or A. rhizogenes, and obtained 85% and 33-100% transient transformation rates, respectively. The transient transformation assays in ice plant callus and seedlings demonstrated that the concentrations of Agrobacteria, the durations of co-incubation time, and the plant growth stages were three important factors affecting the transient transformation efficiencies. Additionally, pot-grown juvenile plants were syringe-injected with two A. rhizogenes strains A8196 and NCPPB 1855, to establish transformed roots. After infections, ice plants were grown hydroponically and showed GUS expressions in transformed roots for 8 consecutive weeks.ConclusionsOur Agrobacterium-mediated transformation protocols utilized hypocotyl-derived callus and seedlings as plant materials, which can be easily obtained in large quantity. The average successful transient transformation rates were about 2.4-3.0% with callus and 33.3-100.0% with seedlings. We also developed a rapid and efficient protocol to generate transgenic roots by A. rhizogenes infections without laborious and challenging tissue culture techniques. This protocol to establish composite ice plant system demonstrates excellent improvements in efficiency, efficacy, and ease of use over previous ice plant transformation protocols. These Agrobacterium-mediated transformation protocols can be versatile and efficient tools for exploring gene functions at cellular and organ levels of ice plants.

Project description:Common ice plant (Mesembryanthemum crystallinum L.) is a novel edible plant with a succulent and savory flavor. The plants display prominent epidermal bladder cells (EBCs) on the surface of the leaves that store water and sodium chloride (NaCl). The plants have high nutritional value and are adapted to saline soils. Previous research has determined the impact of NaCl on the growth and mineral content of ice plant, but as NaCl has an impact on a food’s sensory properties, an interesting question is whether saline growth media can affect the plant’s taste and texture, and if this alters consumers’ sensory response to ice plant. The objective of this study was to evaluate the sensory aspects of ice plant, as well as consumer liking in response to increasing NaCl concentration in hydroponic nutrient solution. Four-week-old seedlings of ice plant were transplanted into deep water culture (DWC) hydroponic systems and treated with five NaCl concentrations (0 M [control], 0.05 M, 0.10 M, 0.20 M, and 0.40 M NaCl). Eight-week-old plants (after four weeks of NaCl treatment) were harvested, and the middle leaves of each plant were sampled for consumer testing. A total of 115 participants evaluated various flavor, texture, and appearance aspects of ice plant and provided their liking ratings. The consumers were able to discriminate differences in salt intensity from the plants based on NaCl treatment in the hydroponic nutrient solution. Low NaCl concentrations (0.05–0.10 M) did not have obvious adverse effect on consumer liking, which aligns with the result of previous research that 0.05–0.10 M NaCl could largely stimulate the growth of ice plant. NaCl concentrations higher than 0.20 M are not recommended from both a production and consumer perspective. With increased NaCl level in plant samples, the consumers detected more saltiness, sourness, and fishiness, less green flavor, and similar levels of bitterness and sweetness. NaCl treatment had no effects on leaf appearance and texture, and the consumers’ overall liking was mainly determined by flavor. Overall, ice plant presents some unique attributes (salty and juicy) compared to other edible salad greens; however, consumer awareness of ice plant is very low, and purchase intent is relatively low as well. Consumers picture ice plant being used mainly in salads and in restaurants.

Project description:Background: The halophyte Mesembryanthemum crystallinum (ice plant) is a model for studying salt tolerance. The morphology, physiology, metabolism, and gene expression of ice plant have been studied for over 40 years. Although the complete genome sequence has not been revealed, large-scale analyses of gene expression profiling have drawn an outline of salt tolerance in ice plant. Despite ample information in the transcriptome, miRNA information has not been documented. Results: We examined responses to a sudden increase in salinity in ice plant seedlings. Using a fluorescent dye to detect Na+, we found that ice plant roots respond to an increased flux of Na+ by either secreting or storing Na+ in specialized cells. High-throughput sequencing was used to identify small RNA profiles in three-day-old seedlings treated with or without 200 mM NaCl. Totally 132 conserved miRNAs belonging to 22 families were found. The hairpin precursor of 19 conserved mcr-miRNAs and 12 novel mcr-miRNAs were identified. Target genes are involved in a broad range of biological processes: transcription factors that regulate growth and development, enzymes that catalyze miRNA biogenesis for the most conserved mcr-miRNA, and proteins that are involved in ion homeostasis and drought-stress responses for some novel mcr-miRNAs. After 6 h of salt stress, the expressions of most mcr-miRNAs were down-regulated, whereas the expressions of their corresponding target genes were up-regulated. Analyses of the functions of target genes revealed that cellular processes, including growth and development, metabolism, and ion transport activity were up-regulated in roots under salt stress. Conclusions: Analyses of small RNA profile of ice plant seedlings identified many conserved miRNA families and several novel miRNAs. The expression of ten conserved miRNAs and three novel miRNAs were reciprocally correlated to predicted targets hourly after salt stress. Based on the expression pattern of miRNA and target genes in combination with the observation of Na+ distribution, we suggest that ice plant roots respond effectively to increased salinity by using Na+ as an osmoticum for cell expansion and guard cell opening. Excessive Na+ could either be secreted through root epidermis or stored in specialized leaf epidermal cells. These responses are partially regulated at the miRNA-mediated post-transcriptional level.

Project description:Ice plant (Mesembryanthemum crystallinum L.) is a halophyte and an inducible CAM plant. Ice plant seedlings display moderate salt tolerance, with root growth unaffected by 200 mM NaCl treatments, though hypocotyl elongation is hindered in salt-stressed etiolated seedlings. Superoxide anion accumulation was prominent in cotyledons and primary leaves but decreased in root tissues over time, with no significant effect from salt treatment. Hydrogen peroxide levels initially surged in both control and salt-treated seedlings, with higher and more persistent accumulation in the salt-treated seedlings. The activities of H2O2-scavenging ascorbate-glutathione cycle enzymes ascorbate peroxidase (APX), monodehydroascorbate reductase, and dehydroascorbate reductase increased, while guaiacol-dependent peroxidase activity decreased and catalase activity showed no change, indicating APX activity as the primary response to salt stress. Salt-induced APX activities were detected mainly in the microsomal fraction for light-grown seedlings and the cytosolic fraction for etiolated seedlings, highlighting plastids as the primary site of ROS accumulation under salt stress. An RNA-seq analysis of etiolated seedlings revealed about 8% unigenes showing more than a four-fold change in expression after a 6-h 200 mM NaCl treatment. GO enrichment analysis indicated that differentially expressed genes (DEGs) with increased transcript abundance were associated with ion transport, antioxidant activity, and stress responses, while DEGs with decreased transcript abundance were linked to metabolic and biosynthesis processes such as ribosomal protein synthesis and cell wall formation. This indicates that salt stress hinders growth but enhances ion homeostasis and stress response mechanisms. The expression of all eight APX genes were induced by a 48-hour salt treatment, with varying expression patterns. For class III peroxidase family, 14 out of 53 identified unigenes qualified as DEGs. The time-course expression patterns revealed that the transcript levels of McPrx4.1, McPrx12.1, and McPrx12.3 increased, while McPrx60.3 decreased. These findings highlight the distinct roles of class III peroxidases in balancing plant growth and stress responses, advancing our understanding of the mechanisms behind salt tolerance in halophytes. This study comprehensively analyzed changes in gene expression, antioxidant enzyme activity, and ROS accumulation in ice plant seedlings. Unveiling these responses will advance our understanding of the growth-stress balance in the intrinsic salt tolerance in halophytes.

Dataset Information

Root system architecture analysis in Mesembryanthemum crystallinum (ice plant) seedlings reveals characteristic root halotropic response.

Publications

Root system architecture analysis in <i>Mesembryanthemum crystallinum</i> (ice plant) seedlings reveals characteristic root halotropic response.

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