The translation initiation factor eIF3M2 upregulates HEAT SHOCK PROTEIN 70 to maintain pollen tube membrane integrity during heat shock

Abstract

Pollen germination and pollen tube (PT) growth are extremely sensitive to high temperatures. During heat stress (HS), global translation shuts down and favors the maintenance of the essential cellular proteome for cell viability and protection against protein misfolding. Here, we demonstrate that under normal conditions, the Arabidopsis (Arabidopsis thaliana) eukaryotic translation initiation factor subunit eif3m1/eif3m2 double mutant exhibits poor pollen germination, loss of PT integrity and an increased rate of aborted seeds. Surprisingly, under HS at 37 °C, eif3m1 pollen germination outperformed wild-type Col-0, showing enhanced PT integrity. We established that the improved thermotolerance of the eif3m1 PT was due to increased expression of its putative paralog eIF3M2, which in turn upregulated Heat Shock protein 70 (HSP70) mRNA and protein levels. Indeed, eIF3M2 overexpression upregulated HSP70 expression, whereas eif3m2 knockdown showed reduced HSP70.1 promoter activity and increased in PT burst under HS conditions. Moreover, we show that eIF3M2 coimmunoprecipitates with HSP70 in PTs and directly interacts with cytoplasmic HSP70.1/2/4 and eIF4G in Nicotiana benthamiana pavement cells. Collectively, our data revealed that plants employ the eIF3M2-HSP70 module as a regulator of thermotolerance to maintain PT membrane integrity and improve fertilization and seed set adaptation under high temperatures.