The role of strigolactones in secondary growth regulation

In addition to longitudinal growth, lateral expansion of growth axes is essential for land plants to create extended shoot and root systems. Lateral or secondary growth is mediated by the activity of the cambium, a two-dimensional meristematic tissue, which is organised in a tube-like domain enclosing the centre of growth axes. Tissue formation by the cambium is mostly limited to vascular tissue, which is essential for increasing the transport capacity and mechanical support of shoot and root systems. Surprisingly, in spite of its essential role for many aspects of plant growth, knowledge of the molecular regulation of the cambium is very limited. In our lab, we have identified strigolactones (SLs), a group of plant hormones recently discovered to be essential for the regulation of shoot branching, as novel regulators of secondary growth. Shoot branching and secondary growth are influenced by environmental stimuli, and natural variation of these responses within species has been reported. Based on our observations, we hypothesise that plants employ SL signalling to adjust their growth to different environmental conditions and that differences in SL signalling have contributed to changes in plant growth forms during evolution. In this study, we want to explore this hypothesis by elucidating in detail the role of SLs in the control of secondary growth, which we regard as a novel SL response. In close collaboration with established groups from the field, we will exploit natural variation between Arabidopsis accessions to explore SL signalling-based adaptation and to identify novel factors influencing secondary growth. Due to the relevance of the project for our understanding of secondary growth and of the regulation of cell fate in higher organisms by long- and short- distance signalling, the results produced by this project will have a significant impact on our understanding of plant development and be of wide interest. We expect to open up paths to modulate shoot stability, transport capacity and the accumulation of biomass by pharmacological approaches in a broad range of species not accessible for transgenic approaches.

Long distance cell-to-cell communication is critical for the development of multicellular organisms. In this respect, plants are especially demanding as they constantly integrate environmental inputs to adjust growth processes to different conditions. One example is thickening of shoots and roots, also designated as secondary growth. Secondary growth is mediated by the vascular cambium, a stem cell-like tissue whose cell-proliferating activity is regulated over long distance by the plant hormone auxin. How auxin signalling is integrated at the level of cambium cells and how cambium activity is coordinated with other growth processes were largely unknown. During this project, we generated physiological, genetic, and pharmacological evidence that strigolactones (SLs), a group of plant hormones recently described to be involved in the repression of shoot branching, positively regulate cambial activity and that this function is conserved among species. More precisely, we showed by using the reference plant Arabidopsis thaliana that SL signalling in the vascular cambium itself is sufficient for cambium stimulation and that it interacts strongly with the auxin signalling pathway. In fact, genetic and pharmacological analyses suggested that SLs act downstream of auxin signalling. Based on our observations, we propose that auxin signalling promotes SL biosynthesis and signalling in cambium cells. Importantly, we identified SMXL5, a member of a recently identified family of putative SL signalling repressors, as being specifically expressed in cambium cells. Combination of a mutation in SMXL5 with a mutation in SMXL4, the closest homolog of SMXL5, resulted in a strong increase of cambium activity, growth retardation of the primary root and the enhanced formation of adventitious roots. All these responses are promoted by the SL signalling pathway and, therefore, our observations support a role of SMXL5 and SMXL4 as repressors of SL signalling. These observations also suggest that there is an SL-dependent and non-cell autonomous effect on meristem activity and that different growth processes are differentially regulated by SMXL5/4 Collectively, we propose that SLs function as modulators used by plants to switch between two growth forms: a bushier form displaying a strong outgrowth of many side shoots and a weak main stem, and a form in which the main shoot dominates and displays enhanced secondary growth. Our results provide a model of how auxin-based long-distance signalling is translated into cambium activity and suggest that SLs act as general modulators of plant growth forms linking the control of branching with the thickening of stems and roots.