Transcription factor networks regulating the cell specific gene expression required for C4 photosynthesis

In many organisms distinct cell types carry out defined functions. One excellent example of this is found in plants that use the so-called C4 photosynthetic pathway. In these species the fundamental photosynthetic process takes place in two cell types known as mesophyll and bundle sheath cells. How genes encoding photosynthesis proteins are regulated such that part of pathway is restricted to mesophyll cells, and others are expressed only in the bundle sheath has been studied for decades. Using the C3 model Arabidopsis that also has these cells we have recently identified a transcription factor module that is able to pattern genes to bundle sheath cells.
We can detect the hallmarks of this module in C4 photosynthesis genes and we now wish to determine if this mechanism is used to compartment these genes into the C4 bundle sheath. Furthermore, we also wish to understand how the transcription factors that we have identified as being necessary and sufficient for expression in the bundle sheath generate this output, and also how they themselves are regulated. The work will provide fundamental insight into the spatial regulation of gene expression in multicellular organisms, and in particular provide key insights into how C4 gene expression is brought about.

Improvements in photosynthetic efficiency during land plant evolution are associated with increased cellular specialisation in the leaf. The mechanisms that restrict photosynthesis gene expression to each cell type have been unclear for decades but in C3 Arabidopsis we recently identified the first transcription factors responsible directing gene expression in the bundle sheath, a ring of specialised cells surrounding the leaf vasculature. The regulatory module consists of a bipartite interaction between members of the MYC and MYB families. Whilst MYBs are restricted to the bundle sheath, the MYCs are expressed everywhere. We have now found that C4 genes that are specifically expressed in the bundle sheath of the C4 plant Gynandropsis gynandra also contain the MYC and MYB motifs, and the transcription factors are patterned to the same cells as Arabidopsis. in Arabidopsis we have developed a conceptual model based on three factors to explain how the bundle sheath specific MYBs and the non-specific MYCs lead to cell specific expression of their targets. There are parallels between our model and the AB and BC function genes that interact to specify petals and stamens respectively in the ABC model of floral organ development. By leveraging our insights we now wish to: 1) Determine whether and how the MYC-MYB module controls the canonical expression of C4 enzymes in bundle sheath cells of the C4 leaf; 2) Determine how the MYC-MYB module leads to cell-specific gene expression in Arabidopsis. In so doing, we aim to elucidate how genes are expressed in specific cell-types of C3 and C4 plants.