Darkened leaves use different metabolic strategies for senescence and survival
Plant Physiol. 2018; 177 (1):132-150

Law SR, Chrobok D, Juvany M, Delhomme N, Lindén P, Brouwer B, Ahad A, Moritz T, Jansson S, Gardestrom P, Keech O

In plants, an individually darkened leaf (IDL) initiates senescence much more rapidly than a leaf from a whole darkened plant (DP). Combining transcriptomic and metabolomic approaches in Arabidopsis thaliana, we present an overview of the metabolic strategies that are employed in response to different darkening treatments. Under DP conditions, the perception of carbon starvation drove a profound metabolic readjustment in which lipids, branched-chain amino acids, and potentially monosaccharides released from cell wall loosening became important substrates for maintaining minimal ATP production. Concomitantly, the increased accumulation of amino acids with a high nitrogen:carbon ratio may provide a safety mechanism for the storage of metabolically-derived cytotoxic ammonium and a pool of nitrogen for use upon returning to typical growth conditions. Conversely, in IDL, the metabolic profiling that followed our 13C enrichment assays revealed a temporal and differential exchange of metabolites, including sugars and amino acids, between the darkened leaf and the rest of the plant. This active transport could be the basis for a progressive metabolic shift in the substrates fuelling mitochondrial activities, which are central to the catabolic reactions facilitating the retrieval of nutrients from the senescing leaf. We propose a model illustrating the specific metabolic strategies employed by leaves in response to these two darkening treatments, which either support rapid senescence or a strong capacity for survival.

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