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PLANTSTEMS Report Summary

Project ID: 647148
Funded under: H2020-EU.1.1.

Periodic Reporting for period 1 - PLANTSTEMS (Decoding the Lateral Expansion of Plant Stems)

Reporting period: 2015-09-01 to 2017-02-28

Summary of the context and overall objectives of the project

In contrast to animals, in which tissue proliferation in adult individuals is often pathological and deleterious, plants have evolved an indefinite growth habit. A remarkable but under-investigated example is the thickening of plant stems and roots: It is a purely postembryonic growth process and the group of stem cells responsible – the cambium – is derived from and embedded in fully differentiated tissues. Consequently, lateral plant growth has to integrate and overcome developmental and physical constraints imposed by participating tissues. This is especially significant in the context of the extracellular matrix, which fixes the position of plant cells relative to each other and provides mechanical support for the plant body. However, how cells sense and modulate their environment during this process is completely unknown. This project leverages the unique growth mode of plants and explores the process of lateral stem growth in the reference plant Arabidopsis thaliana as a paradigm for postembryonic growth and tissue remodeling. Thereby it addresses the fundamental question of how cell identities are reprogrammed in vivo and how basic cellular functions like interaction between cells and their matrix contribute to this process.

This is achieved by deciphering the influence of the extracellular matrix on stem cell activity, by decoding the complex role of hormonal signaling, by recording specific cell fate signatures; and by identifying novel signalling cascades connecting the extracellular matrix with underlying cells. Together these results will provide unprecedented insight into lateral stem growth – a process responsible for the accumulation of wood and a large proportion of terrestrial biomass and will reveal fundamental concepts of growth processes in adult organisms. Because plants are the primary producers of biomass on earth and underlying growth processes are found in adult structures, it is vital to reveal inherent regulatory principles. Enlightening these principles will provide possibilities to overcome growth constraints in plants and illustrate how multicellular organisms are able to accommodate life-long growth.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

In the first project period, tools for accessing individual plant stem tissues were successfully established allowing modulation of tissue properties in the second project period. Importantly, the importance of differential hormone signaling in different tissues was revealed providing the possibility to dissect its impact on distinct cell wall properties. As a fundamental tool, Brillouin spectroscopy was established in the group, an emerging technology for probing mechanical properties of subcellular structures.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

As a major progress beyond the state of the art, essential determinants of the formation of phloem tissues were identified. Plant stem cell niches, like the cambium, require long-distance transport of energy metabolites and signaling molecules along the phloem tissue which, in turn, is one of the major tissues produced by the cambium. However, so far it was unclear how specification of phloem cells is controlled. In the context of this study we could 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 uncharacterised subclade of the SMXL gene family which mediates hormonal strigolactone and karrikin signaling. Strigolactones are endogenous signaling molecules regulating shoot and root branching whereas exogenous karrikin molecules induce germination after wildfires. Both activities depend on the F-box protein and SCF (Skp, Cullin, F-box) complex component MORE AXILLARY GROWTH2 (MAX2). Strigolactone and karrikin perception leads to MAX2-dependent degradation of distinct SMXL protein family members, which is key for mediating hormonal effects. 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 fueling of plant meristems. It is envisaged that the identification of key determinants of phloem formation opens up possibilities to modulate log-distance transport capacities for sugars along plant bodies in breeding programs, to influence the storage of energy metabolites in crop species resulting in an increased agricultural productivity.

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