Dataset Information

Sexual Reproduction via a 1-Aminocyclopropane-1-Carboxylic Acid-Dependent Pathway Through Redox Modulation in the Marine Red Alga Pyropia yezoensis (Rhodophyta).

ABSTRACT: The transition from the vegetative to sexually reproductive phase is the most dynamic change to occur during a plant's life cycle. In the present study, we showed that the ethylene precursor 1-aminocylopropane-1-carboxylic acid (ACC) induces sexual reproduction in the marine red alga Pyropia yezoensis independently from ethylene. Exogenous application of ACC, which contains a three membered carbocyclic ring, promoted the formation of spermatia and carporspores in gametophytes, whereas ethephon, an ethylene-releasing compound, did not stimulate sexual reproduction. In addition, an ACC analog, 1-aminocyclobutane-1-carboxylic acid (ACBC), which contains a four membered carbocyclic ring, promoted sexual reproduction and enhanced tolerance to oxidative stress in the same manner as ACC, but 1-aminocyclopentane-1-carboxylic acid (cycloleucine; which contains a cyclopentane ring) did not. The application of ACC increased the generation of reactive oxygen species (ROS) and induced the expression of PyRboh gene encoding NADPH oxidase. ACC also stimulated the synthesis of ascorbate (AsA) by inducing transcripts of PyGalLDH, which encodes galactono-1,4-lactone dehydrogenase, the catalyst for the final enzymatic step of the AsA biosynthetic pathway. Conversely, ACC caused a decrease in the synthesis of glutathione (GSH) by repressing transcripts of PyGCL, which encodes glutamate cysteine ligase, the catalyst for the rate-limiting step in the formation of GSH. These results suggest a possible role played by ACC as a signaling molecule independent from ethylene in the regulation of sexual reproduction through alterations to the redox state in P. yezoensis.

SUBMITTER: Uji T

PROVIDER: S-EPMC7028691 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Sexual Reproduction via a 1-Aminocyclopropane-1-Carboxylic Acid-Dependent Pathway Through Redox Modulation in the Marine Red Alga Pyropia yezoensis (Rhodophyta).

Uji Toshiki T Endo Harune H Mizuta Hiroyuki H

Frontiers in plant science 20200212

The transition from the vegetative to sexually reproductive phase is the most dynamic change to occur during a plant's life cycle. In the present study, we showed that the ethylene precursor 1-aminocylopropane-1-carboxylic acid (ACC) induces sexual reproduction in the marine red alga Pyropia yezoensis independently from ethylene. Exogenous application of ACC, which contains a three membered carbocyclic ring, promoted the formation of spermatia and carporspores in gametophytes, whereas eth ...[more]

PMID: 32117396

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Project description:BackgroundAlginate lyases belonging to polysaccharide lyase family-7 (PL-7) are the most well studied on their structures and functions among whole alginate lyases. However, all characterized PL-7 alginate lyases are from prokaryotic bacteria cells. Here we report the first identification of eukaryotic PL-7 alginate lyase from marine red alga Pyropia yezoensis.MethodsThe cDNA encoding an alginate lyase PyAly was cloned and was used for the construction of recombinant PyAly (rPyAly) expression system in Escherichia coli. Purified rPyAly was assayed to identify its enzymatic properties. Its expression pattern in P. yessoensis was also investigated.ResultsPyAly is likely a secreted protein consisting of an N-terminal signal peptide of 25 residues and a catalytic domain of 216 residues. The amino-acid sequence of the catalytic domain showed 19-29% identities to those of bacterial characterized alginate lyases classified into family PL-7. Recombinant PyAly protein, rPyAly, which was produced with E. coli BL21(DE3) by cold-inducible expression system, drastically decreased the viscosity of alginate solution in the early stage of reaction. The most preferable substrate for rPyAly was the poly(M) of alginate with an optimal temperature and pH at 35oC and 8.0, respectively. After reaction, unsaturated tri- and tetra-saccharides were produced from poly(M) as major end products. These enzymatic properties indicated that PyAly is an endolytic alginate lyase belonging to PL-7. Moreover, we found that the PyAly gene is split into 4 exons with 3 introns. PyAly was also specifically expressed in the gametophytic haplopid stage.ConclusionThis study demonstrates that PyAly in marine red alga P. yezoensis is a novel PL-7 alginate lyase with an endolytic manner. PyAly is a gametophyte-specifically expressed protein and its structural gene is composed of four exons and three introns. Thus, PyAly is the first enzymatically characterized eukaryotic PL-7 alginate lyase.

Project description:BACKGROUND:Pyropia yezoensis (Rhodophyta) is widely cultivated in East Asia and plays important economic, ecological and research roles. Although inorganic carbon utilization of P. yezoensis has been investigated from a physiological aspect, the carbon concentration mechanism (CCM) of P. yezoensis remains unclear. To explore the CCM of P. yezoensis, especially during its different life stages, we tracked changes in the transcriptome, photosynthetic efficiency and in key enzyme activities under different inorganic carbon concentrations. RESULTS:Photosynthetic efficiency demonstrated that sporophytes were more sensitive to low carbon (LC) than gametophytes, with increased photosynthesis rate during both life stages under high carbon (HC) compared to normal carbon (NC) conditions. The amount of starch and number of plastoglobuli in cells corresponded with the growth reaction to different inorganic carbon (Ci) concentrations. We constructed 18 cDNA libraries from 18 samples (three biological replicates per Ci treatment at two life cycles stages) and sequenced these using the Illumina platform. De novo assembly generated 182,564 unigenes, including approximately 275 unigenes related to CCM. Most genes encoding internal carbonic anhydrase (CA) and bicarbonate transporters involved in the biophysical CCM pathway were induced under LC in comparison with NC, with transcript abundance of some PyCAs in gametophytes typically higher than that in sporophytes. We identified all key genes participating in the C4 pathway and showed that their RNA abundances changed with varying Ci conditions. High decarboxylating activity of PEPCKase and low PEPCase activity were observed in P. yezoensis. Activities of other key enzymes involved in the C4-like pathway were higher under HC than under the other two conditions. Pyruvate carboxylase (PYC) showed higher carboxylation activity than PEPC under these Ci conditions. Isocitrate lyase (ICL) showed high activity, but the activity of malate synthase (MS) was very low. CONCLUSION:We elucidated the CCM of P. yezoensis from transcriptome and enzyme activity levels. All results indicated at least two types of CCM in P. yezoensis, one involving CA and an anion exchanger (transporter), and a second, C4-like pathway belonging to the PEPCK subtype. PYC may play the main carboxylation role in this C4-like pathway, which functions in both the sporophyte and gametophyte life cycles.

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Dataset Information

Sexual Reproduction via a 1-Aminocyclopropane-1-Carboxylic Acid-Dependent Pathway Through Redox Modulation in the Marine Red Alga Pyropia yezoensis (Rhodophyta).

Publications

Sexual Reproduction <i>via</i> a 1-Aminocyclopropane-1-Carboxylic Acid-Dependent Pathway Through Redox Modulation in the Marine Red Alga <i>Pyropia yezoensis</i> (Rhodophyta).

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