Heat stress leads to rapid lipid remodeling and transcriptional adaptations in Nicotiana tabacum pollen tubes

After reaching the stigma, pollen grains germinate and form a pollen tube that transports the sperm cells to the ovule. Due to selection pressure between pollen tubes, pollen grains likely evolved mechanisms to quickly adapt to temperature changes to sustain elongation at the highest possible rate. We investigated these adaptions in tobacco (Nicotiana tabacum) pollen tubes grown in vitro under 22 degrees C and 37 degrees C by a multi-omics approach including lipidomic, metabolomic, and transcriptomic analysis. Both glycerophospholipids and galactoglycerolipids increased in saturated acyl chains under heat stress (HS), while triacylglycerols (TGs) changed less in respect to desaturation but increased in abundance. Free sterol composition was altered, and sterol ester levels decreased. The levels of sterylglycosides and several sphingolipid classes and species were augmented. Most amino acid levels increased during HS, including the noncodogenic amino acids gamma-amino butyrate and pipecolate. Furthermore, the sugars sedoheptulose and sucrose showed higher levels. Also, the transcriptome underwent pronounced changes with 1,570 of 24,013 genes being differentially upregulated and 813 being downregulated. Transcripts coding for heat shock proteins and many transcriptional regulators were most strongly upregulated but also transcripts that have so far not been linked to HS. Transcripts involved in TG synthesis increased, while the modulation of acyl chain desaturation seemed not to be transcriptionally controlled, indicating other means of regulation. In conclusion, we show that tobacco pollen tubes are able to rapidly remodel their lipidome under HS likely by post-transcriptional and/or post-translational regulation. Nicotiana tabacum pollen tubes react to heat stress with metabolomic adaptations, transcriptional adjustments, and rapid and reversible lipid remodeling.