Paf1C denoises transcription and growth patterns to achieve organ shape reproducibility

Abstract

In multicellular systems, all cells exhibit transcriptional noise. However, its exact contribution to morphogenesis often remains unclear, especially in animals where cells can also move. Here we take advantage of walled plant cells, where transcriptional noise happens in tissues with a fixed topology. Using synchronously growing guard cells in stomata, we demonstrate that mutation in VIP3, a subunit of the conserved polymerase-associated factor 1 complex (Paf1C), increases transcriptional noise in Arabidopsis. This conclusion could be generalized to other group of cells at the shoot apex. Such noise translates into growth and shape defects. Indeed, in vip3 sepals, we measured higher growth heterogeneity between adjacent cells, with molecular evidence of increased local mechanical conflicts. This even culminated with the presence of negatively growing cells in specific growth conditions. Interestingly, such increased local noise makes the regional pattern of growth less clear-cut. Reduced regional conflicts lead to delay in organ growth arrest, ultimately making final organ shapes and sizes more variable. We propose that transcriptional noise is managed by Paf1C to ensure organ robustness by building up mechanical conflicts at the regional scale, instead of the local scale. HIGHLIGHTSO_LIPaf1C controls transcriptional noise in Arabidopsis C_LIO_LIPaf1C reduces growth heterogeneity and dampens local mechanical conflicts C_LIO_LIImpairing both Paf1C and microtubules can trigger negative growth in Arabidopsis C_LIO_LIScaling up local conflicts to regional ones with sharp boundaries contributes to organ shape robustness C_LI