Control of organ size by TAS3A

Plant organ size depends on the coordination of cell proliferation and expansion, a process regulated by numerous factors, including transcription factors and small RNAs. However, how different small-RNA pathways are integrated with growth-regulating transcriptional networks remains only partly understood. Here, we studied how the Arabidopsis TRANS-ACTING siRNA3A (TAS3A)-derived trans-acting small RNA pathway controls organ size in Arabidopsis thaliana. We found that TAS3A overexpression increased leaf and floral organ size, whereas tas3a mutants showed reduced organ growth. We show that TAS3A acts by modulating AUXIN-RESPONSE-FACTOR2 (ARF2) activity and that plants expressing a trans-acting siRNA (tasiRNA)-resistant ARF2 allele showed reduced organ growth. In turn, ARF2 repressed several GROWTH-REGULATING FACTOR (GRF) genes, including GRF3, which is a direct ARF2 target and is also controlled by microRNA miR396. Furthermore, uncoupling GRF activity from ARF2 repression was sufficient to increase floral organ size. Interestingly, whereas the TAS3A-ARF2-GRF module regulates leaf and petal growth predominantly through changes in cell proliferation, gynoecium growth involves a more complex balance between cell proliferation and elongation. Together, our results identify ARF2 as a central molecular node connecting tasiRNA- and miRNA-dependent pathways and establish TAS3A as a key regulator of Arabidopsis aerial organ growth.