OBERON3 and SUPPRESSOR OF MAX2 1-LIKE proteins form a regulatory module driving phloem development.

Spatial specificity of cell fate decisions is central for organismal development. The phloem tissue mediates long-distance transport of energy metabolites along plant bodies and is characterized by an exceptional degree of cellular specialization. How a phloem-specific developmental program is implemented is, however, unknown. Here we reveal that the ubiquitously expressed PHD-finger protein OBE3 forms a central module with the phloem-specific SMXL5 protein for establishing the phloem developmental program in Arabidopsis thaliana. By protein interaction studies and phloem-specific ATAC-seq analyses, we show that OBE3 and SMXL5 proteins form a complex in nuclei of phloem stem cells where they promote a phloem-specific chromatin profile. This profile allows expression of OPS, BRX, BAM3, and CVP2 genes acting as mediators of phloem differentiation. Our findings demonstrate that OBE3/SMXL5 protein complexes establish nuclear features essential for determining phloem cell fate and highlight how a combination of ubiquitous and local regulators generate specificity of developmental decisions in plants.

Strigolactone- and Karrikin-Independent SMXL Proteins Are Central Regulators of Phloem Formation.

Plant stem cell niches, the meristems, require long-distance transport of energy metabolites and signaling molecules along the phloem tissue. However, currently it is unclear how specification of phloem cells is controlled. Here we show that the genes SUPPRESSOR OF MAX2 1-LIKE3 (SMXL3), SMXL4, and SMXL5 act as cell-autonomous key regulators of phloem formation in Arabidopsis thaliana. The three genes form an uncharacterized subclade of the SMXL gene family that mediates hormonal strigolactone and karrikin signaling. Strigolactones are endogenous signaling molecules regulating shoot and root branching [1] whereas exogenous karrikin molecules induce germination after wildfires [2]. Both activities depend on the F-box protein and SCF (Skp, Cullin, F-box) complex component MORE AXILLARY GROWTH2 (MAX2) [3-5]. Strigolactone and karrikin perception leads to MAX2-dependent degradation of distinct SMXL protein family members, which is key for mediating hormonal effects [6-12]. However, the nature of events immediately downstream of SMXL protein degradation and whether all SMXL proteins mediate strigolactone or karrikin signaling is unknown. In this study we demonstrate that, within the SMXL gene family, specifically SMXL3/4/5 deficiency results in strong defects in phloem formation, altered sugar accumulation, and seedling lethality. By comparing protein stabilities, we show that SMXL3/4/5 proteins function differently to canonical strigolactone and karrikin signaling mediators, although being functionally interchangeable with those under low strigolactone/karrikin signaling conditions. Our observations reveal a fundamental mechanism of phloem formation and indicate that diversity of SMXL protein functions is essential for a steady fuelling of plant meristems.

Tor1 and CK2 kinases control a switch between alternative ribosome biogenesis pathways in a growth-dependent manner.

Ribosome biogenesis is a major energy-consuming process in the cell that has to be rapidly down-regulated in response to stress or nutrient depletion. The target of rapamycin 1 (Tor1) pathway regulates synthesis of ribosomal RNA (rRNA) at the level of transcription initiation. It remains unclear whether ribosome biogenesis is also controlled directly at the posttranscriptional level. We show that Tor1 and casein kinase 2 (CK2) kinases regulate a rapid switch between a productive and a non-productive pre-rRNA processing pathways in yeast. Under stress, the pre-rRNA continues to be synthesized; however, it is processed differently, and no new ribosomes are produced. Strikingly, the control of the switch does not require the Sch9 kinase, indicating that an unrecognized Tor Complex 1 (TORC1) signaling branch involving CK2 kinase directly regulates ribosome biogenesis at the posttranscriptional level.