Timing Is Everything In Autumn – Coordination Of Senescence Onset By A Transcriptional Program In Response To Environmental And Phytohormone Signals

European aspen (Populus tremula L.) undergoes a coordinated senescence program during autumn; however, it is not known what exactly triggers it. To identify the cellular program leading to senescence, we utilized natural variation among Swedish aspen genotypes in a common garden to study senescence timing and the underlying changes in leaf phytohormone and transcriptome profiles. Apart from the patterns of major transcriptional cascade that was similar between the genotypes and closely associated with cytokinin and auxin metabolite levels and gradually decreasing air temperature during autumn, we detected patterns that consistently preceded or coincided with senescence onset in individual genotypes. Another cascade seemed to respond to short-term changes in weather conditions that re-wired the transcriptional network; the up-regulation of genes related to ethylene and abiotic stress, programmed cell death and translation occurred first in the early-senescing genotypes and later in the late one. Network analyses displayed a connection between the two cascades, metabolic stress and immunity responses mediated by salicylic acid (SA)-signalling pathway that was repressed along with SA levels at senescence onset. We propose that autumn senescence in aspen trees is affected by environmental variation that evokes stress and the timing is fine-tuned by their stress tolerance mechanism.