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 highly 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. We found that the senescence process was coordinated by two major transcriptional cascades that change in parallel during autumn. Apart from the major temporal transcriptome patterns, senescence-associated gene (SAG) expression and cytokinin and auxin metabolite levels that showed similar patterns between the genotypes and were closely associated with gradually decreasing air temperature during autumn, we detected patterns that consistently preceded or coincided with senescence onset in individual genotypes. The second cascade seemed to respond to short-term changes in weather conditions that affected the transcriptome markedly in a genotype-dependent manner; the re-wiring of the transcriptional network and the up-regulation of genes related to ethylene and abiotic stress responses, programmed cell death and protein translation occurred first in the early-senescing genotypes and later in the late one. However, we could not identify a single gene or hormone marker that could be used as a predictor for the robust differences in the timing of autumn senescence. Instead, we found the two transcriptional cascades interlinked with the salicylic acid (SA)-mediated transcriptional program that was repressed along with SA levels at senescence onset. Co-expression network analyses displayed a connection between the transcriptional programs involving SAGs, abiotic and metabolic stress responses and stress-induced phytohormones accounting for plant immunity. Our results implicated that the activation of the SA-signalling pathway may promote stress tolerance by alleviating redox homeostasis and endoplasmic reticulum function and thus fine-tune the timing of senescence onset under challenging environmental conditions in autumn.