Regulation of pollen lipid body biogenesis by MAP kinases and downstream WRKY transcription factors in Arabidopsis.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101239074 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7404 (Electronic) Linking ISSN: 15537390 NLM ISO Abbreviation: PLoS Genet Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, c2005-

Arabidopsis/*metabolism ; Arabidopsis Proteins/*metabolism ; Lipid Droplets/*metabolism ; Mitogen-Activated Protein Kinases/*metabolism ; Pollen/*metabolism ; Transcription Factors/*metabolism; Arabidopsis/genetics ; Arabidopsis/growth & development ; Arabidopsis Proteins/genetics ; Lipogenesis ; Mitogen-Activated Protein Kinase Kinases/genetics ; Mitogen-Activated Protein Kinase Kinases/metabolism ; Mitogen-Activated Protein Kinases/genetics ; Models, Biological ; Monosaccharide Transport Proteins/genetics ; Monosaccharide Transport Proteins/metabolism ; Mutation ; Plants, Genetically Modified ; Pollen/growth & development ; Promoter Regions, Genetic ; Transcription Factors/genetics

Signaling pathways that control the activities in non-photosynthetic plastids, important sites of plant metabolism, are largely unknown. Previously, we demonstrated that WRKY2 and WRKY34 transcription factors play an essential role in pollen development downstream of mitogen-activated protein kinase 3 (MPK3) and MPK6 in Arabidopsis. Here, we report that GLUCOSE-6-PHOSPHATE/PHOSPHATE TRANSLOCATOR 1 (GPT1) is a key target gene of WRKY2/WRKY34. GPT1 transports glucose-6-phosphate (Glc6P) into plastids for starch and/or fatty acid biosynthesis depending on the plant species. Loss of function of WRKY2/WRKY34 results in reduced GPT1 expression, and concomitantly, reduced accumulation of lipid bodies in mature pollen, which leads to compromised pollen viability, germination, pollen tube growth, and male transmission in Arabidopsis. Pollen-specific overexpression of GPT1 rescues the pollen defects of wrky2 wrky34 double mutant. Furthermore, gain-of-function activation of MPK3/MPK6 enhances GPT1 expression; whereas GPT1 expression is reduced in mkk4 mkk5 double mutant. Together, this study revealed a cytoplasmic/nuclear signaling pathway capable of coordinating the metabolic activities in plastids. High-level expression of GPT1 at late stages of pollen development drives Glc6P from cytosol into plastids, where Glc6P is used for fatty acid biosynthesis, an important step of lipid body biogenesis. The accumulation of lipid bodies during pollen maturation is essential to pollen fitness and successful reproduction.
Competing Interests: The authors have declared that no competing interests exist.

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0 (Arabidopsis Proteins)
0 (Monosaccharide Transport Proteins)
0 (Transcription Factors)
0 (WRKY34 protein, Arabidopsis)
EC 2.7.11.24 (AtMPK3 protein, Arabidopsis)
EC 2.7.11.24 (MPK6 protein, Arabidopsis)
EC 2.7.11.24 (Mitogen-Activated Protein Kinases)
EC 2.7.12.2 (Mitogen-Activated Protein Kinase Kinases)

Date Created: 20181227 Date Completed: 20190304 Latest Revision: 20200309

20240829

PMC6324818

10.1371/journal.pgen.1007880

30586356