miR156-independent repression of the ageing pathway by longevity-promoting AHL proteins in Arabidopsis

Plants age by transition through distinct developmental phases, with the juvenile- to adult vegetative and the adult vegetative to reproductive phase change as two consecutive important post-embryonic phase transitions. During the transition from the juvenile- to adult vegetative phase, also known as the vegetative phase change (VPC), many plants undergo specific morphological and physiological changes. In the model plant Arabidopsis thaliana (Arabidopsis), for example, the VPC is marked by clear heteroblastic changes in leaf shape and size and the appearance of trichomes on the abaxial side of leaves. The VPC and the vegetative to reproductive transition are promoted by the SQUAMOSA PROMOTOR BINDING PROTEIN-LIKE (SPL) family of transcription factors and repressed by miR156 and miR157 that target the SPL transcripts. Here we present data that the plant longevity promoting AT-HOOK MOTIF NUCLEAR LOCALIZED protein 15 (AHL15) and family members also repress the SPL-driven ageing pathway. Arabidopsis ahl loss-of-function mutants showed an accelerated VPC and flowering time, whereas AHL15 overexpression dramatically delayed the VPC and flowering time in both Arabidopsis and Nicotiana tabacum . Expression analysis and tissue-specific AHL15 overexpression revealed that AHL15 affects the VPC and flowering time directly through its expression in the shoot apical meristem and young leaves. In addition, we found evidence that AHL15 represses SPL gene expression in a miR156/157-independent manner. The juvenile traits of spl loss-of-function mutants appeared to be dependent on the enhanced expression of the AHL15 gene, providing evidence for a reciprocal negative feedback between AHL15 and SPL genes. Antagonistically to AHLs, SPLs promote axillary meristem (AM) maturation and thus prevent vegetative growth from these meristems by repressing AHL15 expression. Taken together, our results place AHL15 and family members at a central position in the SPL-driven ageing pathway as suppressors of the VPC, flowering time and AM maturation.