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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.

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