Carotology: Are apocarotenoids conserved modulators of streptophyte physiology?

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One major challenge for the earliest land plants was overcoming environmental stressors. The plastid of land plants is recognized as a hub for sensing environmental cues by emanating signals, linking plastid and cell physiology. A major class of these signals are the apocarotenoids that emerge from cleavage of carotenoids. In the first funding period of MAdLand, my team and I have garnered data that land plants and streptophyte algae share the production of a range of stress-relevant apocarotenoids known as signals in embryophytes. Now, we want to understand which physiological and molecular responses these molecules elicit. We will test the hypothesis that the apocarotenoids β-cyclocitral, β-ionone, and dihydroactinidiolide induce conserved response patterns tied with stress signaling; for all work, we will use the MAdLand systems Mesotaenium endlicherianum, Zygnema circumcarinatum, and Physcomitrium patens as a land plant reference. To dissect responses to apocarotenoids, we will pursue three synergistic objectives: (1) Measure the impact of apocarotenoids on zygnematophyte and land plant growth, photophysiology, and feedbacks on upstream isoprenoid metabolism; we will illuminate the physiological impact of apocarotenoids shared by land plants and algae. (2) Infer apocarotenoid-triggered global response patterns shared across 600 million years of streptophyte evolution; integrating RNAseq and phosphoproteomic data will pinpoint comprehensive response patterns—candidates for signal transduction to downstream responses—that we can compare to infer a shared homologous signaling network. (3) Probe the conservation of the signaling pathway; while a range of effects of apocarotenoids will be assessed in 1 and 2 in a top-down approach, we also have clear candidates: the phytohormone salicylic acid and (co-)orthologs of ELONGATED HYPOCOTYL 5 (HY5) and PHYTOCHROME INTERACTING FACTOR 3 (PIF3) in Mesotaenium, Zygnema, and Physcomitrium. We will test for the conservation of these routes via (i) inter-species complementation experiments with the algal genes in Physcomitrium patens hy5 and pif knock-out mutants that were already generated and (ii) salicylic acid quantification. In sum, we will obtain comprehensive data on the physiological impact of apocarotenoids; concomitantly, we will delve into signaling using a top-down and a targeted candidate-based approach. Our data will be projected onto the phylogeny of Phragmoplastophyta and compared to published data on land plants and co-expression data on streptophyte algae. Combined, we will address four defined core topics of MAdLand (i-iv): (i) testing that a molecular chassis for modulation of stress physiology through apocarotenoids evolved in streptophyte algae; (ii) inferring that these regulatory patterns occurred in the last common ancestor of land plants and Zygnematophyceae; (iii) probing their role as molecular adaptations in the response to (iv) abiotic terrestrial challenges.