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

Abstract

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, they likely evolved mechanisms to quickly adapt to temperature changes to sustain an elongation at the highest possible rate. We investigated these adaptions in Nicotiana tabacum pollen tubes grown in vitro under 22 °C and 37 °C by a multi-omic approach including lipidomic, metabolomic and transcriptomic analysis. Both glycerophospholipids and galactoglycerolipids increased in saturated acyl chains under heat stress while triacylglycerols changed less in respect to desaturation but showed higher levels. Free sterol composition was altered, and sterol ester levels decreased. The levels of sterylglycosides and several sphingolipid classes and species were augmented. Most amino acids increased during heat stress, including the non-codogenic amino acids γ-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 up- 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 heat stress. Transcripts involved in triacylglycerol synthesis were increased, while the modulation of acyl chain desaturation seemed not to be transcriptionally controlled indicating other means of regulation.One sentence summaryNicotiana tabacum pollen tubes react to heat stress with metabolomic adaptations, transcriptional adjustments, and a rapid and reversible lipid remodelling.

Finding new friends and revisiting old ones – how plant lipid droplets connect with other subcellular structures

“…While traditionally considered to be just subcellular storage depots for neutral lipids, such as triacylglycerols (TAGs) and sterol esters (SEs), the described functions of plant LDs have expanded in recent years to include roles as both a source and sink for various hydrophobic compounds and their building blocks (Ischebeck et al ., 2020). Hence, plant LDs are now known to be important for fueling a wide range of developmental processes, such as seed germination, and also for membrane remodeling during abiotic stress (de Vries & Ischebeck, 2020; Krawczyk et al ., 2022a). In addition, LDs support plant defenses through the production of volatiles (Garbowicz et al ., 2018) and phytoalexins (Shimada et al ., 2014; Fernandez‐Santos et al ., 2020), and based on their reported proteomes, LDs likely have numerous other functions that remain to be elucidated (Ischebeck et al ., 2020).…”

“…Here, it is speculated that the free fatty acids derived from stress‐induced membrane lipid breakdown and remodeling are channeled into TAG to prevent lipotoxicity, making LDs an effective sink (de Vries & Ischebeck, 2020). SEs, however, decrease during heat stress in tobacco pollen tubes possibly to increase the amount of free sterols and sterol glycosides (Krawczyk et al ., 2022a), which could sustain membrane integrity by counteracting heat‐increased membranes fluidity (Dufourc, 2008). In this regard, LDs could act as both a sink and source at the same time.…”