Chloroplast proteomics reveals transgenerational cross-stress priming in Pinus radiata

Abstract

Plants do have stress memory and chloroplast signaling has been revealed as crucial element to acquire and extend this memory into future generations, allowing plant adaptation to changing environments and providing novel tools in the field of crop improvement. Despite the process is known, how a plant is capable to transfer some aspects of its “life-long learning” to progeny, as well as the role of chloroplast proteome mediating transgenerational cross-stress priming effects, remain unknown. To fill this gap, this study examines the impact of the physiological status of Pinus radiata parentals over the capacity of their progeny to acclimate to their first stress period in a common garden experiment. Seedlings were originated in subpopulations with the same genetic background, but grown in two locations with contrasting environments (stressed vs non-stressed plants). Physiological measurements (fluorescence-based and biochemistry) and chloroplast proteomics were employed to study plant stress responses. Results demonstrated a differential seed priming. Those seedlings originated from stressed plants responded quicker and more efficiently than those originated from unstressed counterparts. Unprimed responses showed proteome remodeling driven by lipid peroxidation and photoinhibition, whereas primed subpopulation quickly faced stress rearranging secondary metabolism, replacing damaged lipids, reducing photooxidative damage, and promoting photorespiration and redox homeostasis in order to reduce lipoperoxidation and maintain photosynthesis. These results not only delve into cross-stress memory in long-lived species, but also suggest a new biotechnological potential for current seed orchards if adequate management is performed. • Parental growing conditions have transgenerational cross-stress priming effects. • Subpopulation originated from stressed plants responded quicker and more efficiently. • Primed responses were driven by photorespiration, redox, and secondary metabolism. • Knowledge acquired suggests a new biotechnological potential for seed orchards.