Plant development is a highly plastic process that, in order to properly function, requires the integration of a plethora of signals. These can be both extrinsic (e.g. soil type, nutrients, water availability) as well as intrinsic (e.g. gene expression, hormones, cell wall modification). Plant morphogenesis is entirely determined by local growth rates and growth directions. At its core, this can be reduced to how individual cells maintain and modulate their cell shape during development and how this is coordinated with the surrounding cells. Plant cells are interconnected through their cell walls and growth largely depends on the interplay between turgor pressure and dynamics of this rigid extracellular matrix.
We still only marginally understand the molecular mechanisms that evolved in plants to modulate cell volume and shape during development. Most knowledge on how plants integrate biochemical and mechanical signals during development comes from studies using epidermal layers due to their accessibility. However, we still do not understand how cell volume control and mechanotransduction are integrated during developmental processes that require establishment of 3-dimensional (3D) differential growth. Lateral roots originate from a subset of pericycle cells deep inside the main root and need to overcome the mechanical constraints provided by the overlying cell layers in order to emerge. In Arabidopsis thaliana (Arabidopsis) the communication between the pericycle and its direct neighbour, the endodermis, is essential for lateral root formation. Although cell volume regulation and mechanotransduction have been implicated in this process, mechanistic insights are still lacking. Using the pericycle/endodermis communication system, I and my team showed that both cell autonomous and non-cell autonomous auxin signalling regulate cytoskeleton reorganisation in order for the pericycle cells to undergo asymmetric expansion. However, key pieces still missing to this puzzle are the regulators: we still do not know which proteins are orchestrating this process. In this proposal, I and my team will investigate how a family of microtubule-associated proteins and local protein phosphorylation work to integrate biochemical and mechanical signals to establish and regulate 3D-differential growth. To this end I have designed a set of experiments in Arabidopsis and the moss Phycomitrium patens (Physcomitrium). We will use the latest innovative techniques, such as CRISPR/Cas9-mediated tissue specific mutations to create cell type or organ specific mutants and employ synthetic hormone signaling approaches. The questions I seek to answer will result in a great advancement of our understanding of plant development in general, but will also help us elucidate to what extent these mechanisms are conserved in different plant lineages.
Beyond its importance for lateral root formation as an important agricultural trait, this research will provide new fundamental biological insights that will be of interest to the whole field of (plant) biology. In particular for those investigating other developmental processes that heavily depend on communication with their surrounding tissue. These include the growth of pollen tubes and infection threads, the development of sclerenchyma fiber cells during wood formation, and also the intracellular accommodation of symbionts. As the process of lateral root formation prior to emergence can be considered a form of invasive growth, the findings of our work might also provide unique new insights into this process. In applied terms, this reverse engineering of these responses could provide a new strategy to make plants more resistant to the infection by different pathogens.