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Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response.

Kanehara K, Yu CY, Cho Y, Cheong WF, Torta F, Shui G, Wenk MR, Nakamura Y - PLoS Genet. (2015)

Bottom Line: The seedlings of plc2-1 mutant showed growth defect that was complemented by heterologous expression of AtPLC2, suggesting that phosphoinositide-specific phospholipase C activity borne by AtPLC2 is required for seedling growth.Moreover, the plc2-1 mutant showed hypersensitive response to ER stress as evidenced by changes in relevant phenotypes and gene expression profiles.Our results revealed the primary enzyme in phosphoinositide metabolism, its involvement in seedling growth and an emerging link between phosphoinositide and the ER stress response.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan; Molecular and Biological Agricultural Sciences Program, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan; Graduate Institute of Biotechnology and Department of Life Sciences, National Chung-Hsing University, Taichung, Taiwan; Muroran Institute of Technology, Muroran, Japan.

ABSTRACT
Phosphoinositides represent important lipid signals in the plant development and stress response. However, multiple isoforms of the phosphoinositide biosynthetic genes hamper our understanding of the pivotal enzymes in each step of the pathway as well as their roles in plant growth and development. Here, we report that phosphoinositide-specific phospholipase C2 (AtPLC2) is the primary phospholipase in phosphoinositide metabolism and is involved in seedling growth and the endoplasmic reticulum (ER) stress responses in Arabidopsis thaliana. Lipidomic profiling of multiple plc mutants showed that the plc2-1 mutant increased levels of its substrates phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate, suggesting that the major phosphoinositide metabolic pathway is impaired. AtPLC2 displayed a distinct tissue expression pattern and localized at the plasma membrane in different cell types, where phosphoinositide signaling occurs. The seedlings of plc2-1 mutant showed growth defect that was complemented by heterologous expression of AtPLC2, suggesting that phosphoinositide-specific phospholipase C activity borne by AtPLC2 is required for seedling growth. Moreover, the plc2-1 mutant showed hypersensitive response to ER stress as evidenced by changes in relevant phenotypes and gene expression profiles. Our results revealed the primary enzyme in phosphoinositide metabolism, its involvement in seedling growth and an emerging link between phosphoinositide and the ER stress response.

No MeSH data available.


Related in: MedlinePlus

Gene expression patterns of AtPLC1, AtPLC2, AtPLC3, and AtPLC4.(A) Developmental stage-specific expression patterns of AtPLC1, AtPLC2, AtPLC3, and AtPLC4. Left to right, germinating seed, seedling, young rosette, developed rosette, bolting rosette, young flower, developed flower, flower and silique, mature silique, senescence. “HIGH”, “MEDIUM”, and “LOW” expression were calculated by microarray assay. The number of samples indicates microarray gene expression data collected by GENEVESTIGATOR (www.genevestigator.com). (B) Heat map of tissue-specific expression pattern of AtPLC1, AtPLC2, AtPLC3, and AtPLC4. Data were analyzed with GENEVESTIGATOR.
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pgen.1005511.g002: Gene expression patterns of AtPLC1, AtPLC2, AtPLC3, and AtPLC4.(A) Developmental stage-specific expression patterns of AtPLC1, AtPLC2, AtPLC3, and AtPLC4. Left to right, germinating seed, seedling, young rosette, developed rosette, bolting rosette, young flower, developed flower, flower and silique, mature silique, senescence. “HIGH”, “MEDIUM”, and “LOW” expression were calculated by microarray assay. The number of samples indicates microarray gene expression data collected by GENEVESTIGATOR (www.genevestigator.com). (B) Heat map of tissue-specific expression pattern of AtPLC1, AtPLC2, AtPLC3, and AtPLC4. Data were analyzed with GENEVESTIGATOR.

Mentions: To examine differential gene expression profiles of AtPLC genes whose mutants were obtained in Fig 1, we utilized the publicly available gene expression database (GENEVESTIGATOR; www.genevestigator.com). Data for AtPLC6 were not available. We found differential expression patterns of these four AtPLC genes during plant growth and development (Fig 2A); AtPLC2 had the highest expression level of the four isoforms consistently throughout the development. While AtPLC3 and AtPLC4 showed stable expression pattern as well, AtPLC1 expression was increased during vegetative growth, remained high during flower development but was dramatically decreased along with senescence. Regarding tissue-specificity, AtPLC2 expressed rather ubiquitously in most of tissues except roots including primary root and root tip (Fig 2B). However, the other isoforms have clearer tissue specificity; AtPLC1 at stele, AtPLC3 at the shoot apex, abscission zone and hypocotyl, and AtPLC4 in male reproductive parts of flowers. These data suggest that AtPLC2 is the primarily and ubiquitously expressed isoform.


Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response.

Kanehara K, Yu CY, Cho Y, Cheong WF, Torta F, Shui G, Wenk MR, Nakamura Y - PLoS Genet. (2015)

Gene expression patterns of AtPLC1, AtPLC2, AtPLC3, and AtPLC4.(A) Developmental stage-specific expression patterns of AtPLC1, AtPLC2, AtPLC3, and AtPLC4. Left to right, germinating seed, seedling, young rosette, developed rosette, bolting rosette, young flower, developed flower, flower and silique, mature silique, senescence. “HIGH”, “MEDIUM”, and “LOW” expression were calculated by microarray assay. The number of samples indicates microarray gene expression data collected by GENEVESTIGATOR (www.genevestigator.com). (B) Heat map of tissue-specific expression pattern of AtPLC1, AtPLC2, AtPLC3, and AtPLC4. Data were analyzed with GENEVESTIGATOR.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4581737&req=5

pgen.1005511.g002: Gene expression patterns of AtPLC1, AtPLC2, AtPLC3, and AtPLC4.(A) Developmental stage-specific expression patterns of AtPLC1, AtPLC2, AtPLC3, and AtPLC4. Left to right, germinating seed, seedling, young rosette, developed rosette, bolting rosette, young flower, developed flower, flower and silique, mature silique, senescence. “HIGH”, “MEDIUM”, and “LOW” expression were calculated by microarray assay. The number of samples indicates microarray gene expression data collected by GENEVESTIGATOR (www.genevestigator.com). (B) Heat map of tissue-specific expression pattern of AtPLC1, AtPLC2, AtPLC3, and AtPLC4. Data were analyzed with GENEVESTIGATOR.
Mentions: To examine differential gene expression profiles of AtPLC genes whose mutants were obtained in Fig 1, we utilized the publicly available gene expression database (GENEVESTIGATOR; www.genevestigator.com). Data for AtPLC6 were not available. We found differential expression patterns of these four AtPLC genes during plant growth and development (Fig 2A); AtPLC2 had the highest expression level of the four isoforms consistently throughout the development. While AtPLC3 and AtPLC4 showed stable expression pattern as well, AtPLC1 expression was increased during vegetative growth, remained high during flower development but was dramatically decreased along with senescence. Regarding tissue-specificity, AtPLC2 expressed rather ubiquitously in most of tissues except roots including primary root and root tip (Fig 2B). However, the other isoforms have clearer tissue specificity; AtPLC1 at stele, AtPLC3 at the shoot apex, abscission zone and hypocotyl, and AtPLC4 in male reproductive parts of flowers. These data suggest that AtPLC2 is the primarily and ubiquitously expressed isoform.

Bottom Line: The seedlings of plc2-1 mutant showed growth defect that was complemented by heterologous expression of AtPLC2, suggesting that phosphoinositide-specific phospholipase C activity borne by AtPLC2 is required for seedling growth.Moreover, the plc2-1 mutant showed hypersensitive response to ER stress as evidenced by changes in relevant phenotypes and gene expression profiles.Our results revealed the primary enzyme in phosphoinositide metabolism, its involvement in seedling growth and an emerging link between phosphoinositide and the ER stress response.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan; Molecular and Biological Agricultural Sciences Program, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan; Graduate Institute of Biotechnology and Department of Life Sciences, National Chung-Hsing University, Taichung, Taiwan; Muroran Institute of Technology, Muroran, Japan.

ABSTRACT
Phosphoinositides represent important lipid signals in the plant development and stress response. However, multiple isoforms of the phosphoinositide biosynthetic genes hamper our understanding of the pivotal enzymes in each step of the pathway as well as their roles in plant growth and development. Here, we report that phosphoinositide-specific phospholipase C2 (AtPLC2) is the primary phospholipase in phosphoinositide metabolism and is involved in seedling growth and the endoplasmic reticulum (ER) stress responses in Arabidopsis thaliana. Lipidomic profiling of multiple plc mutants showed that the plc2-1 mutant increased levels of its substrates phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate, suggesting that the major phosphoinositide metabolic pathway is impaired. AtPLC2 displayed a distinct tissue expression pattern and localized at the plasma membrane in different cell types, where phosphoinositide signaling occurs. The seedlings of plc2-1 mutant showed growth defect that was complemented by heterologous expression of AtPLC2, suggesting that phosphoinositide-specific phospholipase C activity borne by AtPLC2 is required for seedling growth. Moreover, the plc2-1 mutant showed hypersensitive response to ER stress as evidenced by changes in relevant phenotypes and gene expression profiles. Our results revealed the primary enzyme in phosphoinositide metabolism, its involvement in seedling growth and an emerging link between phosphoinositide and the ER stress response.

No MeSH data available.


Related in: MedlinePlus