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Arabidopsis Phospholipase C3 is Involved in Lateral Root Initiation and ABA Responses in Seed Germination and Stomatal Closure


Zhang, Qianqian; van Wijk, Ringo; Shahbaz, Muhammad; Roels, Wendy; van Schooten, Bas; Vermeer, Joop E M; Zarza, Xavier; Guardia, Aisha; Scuffi, Denise; García-Mata, Carlos; Laha, Debabrata; Williams, Phoebe; Willems, Leo A J; Ligterink, Wilco; Hoffmann-Benning, Susanne; Gillaspy, Glenda; Schaaf, Gabriel; Haring, Michel A; Laxalt, Ana M; Munnik, Teun (2018). Arabidopsis Phospholipase C3 is Involved in Lateral Root Initiation and ABA Responses in Seed Germination and Stomatal Closure. Plant & Cell Physiology, 59(3):469-486.

Abstract

Phospholipase C (PLC) is well known for its role in animal signaling, where it generates the second messengers, inositol 1,4,5-trisphosphate (IP3) and diacylglycerol (DAG) by hydrolyzing the minor phospholipid, phosphatidylinositol 4,5-bisphosphate (PIP2) upon receptor stimulation. In plants, PLC's role is still unclear, especially because the primary targets of these second messengers are lacking, i.e. the ligand-gated Ca2+ channel and protein kinase C, but also because PIP2 levels are extremely low. Nonetheless, the Arabidopsis genome encodes 9 PLCs. We used a reversed-genetic approach to explore PLC's function in Arabidopsis and report here that PLC3 is required for proper root development, seed germination and stomatal opening. Two independent knock-down mutants, plc3-2 and plc3-3, were found to exhibit reduced lateral root densities by 10-20%. Mutant seeds germinated slower but were less sensitive to ABA to prevent germination. Guard cells of plc3 were also compromised in ABA-dependent stomatal closure. Promoter-GUS analyses confirmed PLC3 expression in guard cells and germinating seeds, and revealed that the majority is expressed in vascular tissue, most likely phloem companion cells, i.e. in roots, leaves and flowers. In vivo 32Pi-labeling revealed that ABA stimulated the formation of PIP2 in germinating seeds and guard cell-enriched leaf peels, which was significantly reduced in plc3 mutants. Overexpression of PLC3 had no effect on root system architecture or seed germination, but increased the plant's tolerance to drought. Our results provide genetic evidence for PLC's involvement in plant development and ABA signaling, and confirm earlier observations that overexpression increases drought tolerance. Potential molecular mechanisms for the above observations are discussed.

Abstract

Phospholipase C (PLC) is well known for its role in animal signaling, where it generates the second messengers, inositol 1,4,5-trisphosphate (IP3) and diacylglycerol (DAG) by hydrolyzing the minor phospholipid, phosphatidylinositol 4,5-bisphosphate (PIP2) upon receptor stimulation. In plants, PLC's role is still unclear, especially because the primary targets of these second messengers are lacking, i.e. the ligand-gated Ca2+ channel and protein kinase C, but also because PIP2 levels are extremely low. Nonetheless, the Arabidopsis genome encodes 9 PLCs. We used a reversed-genetic approach to explore PLC's function in Arabidopsis and report here that PLC3 is required for proper root development, seed germination and stomatal opening. Two independent knock-down mutants, plc3-2 and plc3-3, were found to exhibit reduced lateral root densities by 10-20%. Mutant seeds germinated slower but were less sensitive to ABA to prevent germination. Guard cells of plc3 were also compromised in ABA-dependent stomatal closure. Promoter-GUS analyses confirmed PLC3 expression in guard cells and germinating seeds, and revealed that the majority is expressed in vascular tissue, most likely phloem companion cells, i.e. in roots, leaves and flowers. In vivo 32Pi-labeling revealed that ABA stimulated the formation of PIP2 in germinating seeds and guard cell-enriched leaf peels, which was significantly reduced in plc3 mutants. Overexpression of PLC3 had no effect on root system architecture or seed germination, but increased the plant's tolerance to drought. Our results provide genetic evidence for PLC's involvement in plant development and ABA signaling, and confirm earlier observations that overexpression increases drought tolerance. Potential molecular mechanisms for the above observations are discussed.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
Dewey Decimal Classification:580 Plants (Botany)
Language:English
Date:1 March 2018
Deposited On:09 Feb 2018 14:02
Last Modified:08 Mar 2018 02:03
Publisher:Oxford University Press
ISSN:0032-0781
OA Status:Closed
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1093/pcp/pcx194
PubMed ID:29309666

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