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.

SUPPRESSOR OF MAX2 1-LIKE 5 promotes secondary phloem formation during radial stem growth.

As a pre-requisite for constant growth, plants produce vascular tissues at different sites within their post-embryonic body. Interestingly, the formation of vascular tissues during longitudinal and radial expansion of shoot and root axes differs fundamentally with respect to its anatomical configuration. This raises the question to which level regulatory mechanisms of vascular tissue formation are shared throughout plant development. Here, we show that, similar to primary phloem formation during longitudinal growth, the cambium-based formation of secondary phloem depends on the function of SUPPRESSOR OF MAX2 1-LIKE (SMXL) genes. In particular, local SMXL5 deficiency results in the absence of secondary phloem. Moreover, the additional disruption of SMXL4 activity increases tissue production in the cambium region without secondary phloem being formed. Using promoter-reporter lines, we observed that SMXL4 and SMXL5 activities are associated with different stages of secondary phloem formation in the Arabidopsis stem. Based on genome-wide transcriptional profiling and expression analyses of phloem-related markers, we concluded that early steps of phloem formation are impaired in smxl4;smxl5 double mutants and that the additional cambium-derived cells fail to establish phloem-related features. Our results showed that molecular mechanisms determining primary and secondary phloem formation share important properties, but differ slightly with SMXL5 playing a more dominant role in the formation of secondary phloem.

The Phloem as a Mediator of Plant Growth Plasticity.

Developmental plasticity, defined as the capacity to respond to changing environmental conditions, is an inherent feature of plant growth. Recent studies have brought the phloem tissue, the quintessential conduit for energy metabolites and inter-organ communication, into focus as an instructive developmental system. Those studies have clarified long-standing questions about essential aspects of phloem development and function, such as the pressure flow hypothesis, mechanisms of phloem unloading, and source-sink relationships. Interestingly, plants with impaired phloem development show characteristic changes in body architecture, thereby highlighting the capacity of the phloem to integrate environmental cues and to fine-tune plant development. Therefore, understanding the plasticity of phloem development provides scenarios of how environmental stimuli are translated into differential plant growth. In this Review, we summarize novel insights into how phloem identity is established and how phloem cells fulfil their core function as transport units. Moreover, we discuss possible interfaces between phloem physiology and development as sites for mediating the plastic growth mode of plants.

Radial plant growth.

One of the extraordinary features of plants is their growth capacity. Depending on the species and the environment, body forms are manifold and, at the same time, constantly reshaped. An important basis of this plastic variation and life-long accumulation of biomass is radial growth. Here, we use this term to describe the ability to grow in girth by the formation of wood, bast and cork. The more technical term for radial growth is secondary growth, which distinguishes the process from primary growth taking place at the tips of stems and roots during plant elongation.