Spatial expression patterns of genes encoding sugar sensors in leaves of C(4) and C(3) grasses

BACKGROUND AND AIMS: The mechanisms of sugar sensing in grasses remain elusive, especially those using C(4) photosynthesis even though a large proportion of the world's agricultural crops utilize this pathway. We addressed this gap by comparing the expression of genes encoding components of sugar sensors in C(3) and C(4) grasses, with a focus on source tissues of C(4) grasses. Given C(4) plants evolved into a two-cell carbon fixation system, it was hypothesized this may have also changed how sugars were sensed. METHODS: For six C(3) and eight C(4) grasses, putative sugar sensor genes were identified for target of rapamycin (TOR), SNF1-related kinase 1 (SnRK1), hexokinase (HXK) and those involved in the metabolism of the sugar sensing metabolite trehalose-6-phosphate (T6P) using publicly available RNA deep sequencing data. For several of these grasses, expression was compared in three ways: source (leaf) versus sink (seed), along the gradient of the leaf, and bundle sheath versus mesophyll cells. KEY RESULTS: No positive selection of codons associated with the evolution of C(4) photosynthesis was identified in sugar sensor proteins here. Expressions of genes encoding sugar sensors were relatively ubiquitous between source and sink tissues as well as along the leaf gradient of both C(4) and C(3) grasses. Across C(4) grasses, SnRK1β1 and TPS1 were preferentially expressed in the mesophyll and bundle sheath cells, respectively. Species-specific differences of gene expression between the two cell types were also apparent. CONCLUSIONS: This comprehensive transcriptomic study provides an initial foundation for elucidating sugar-sensing genes within major C(4) and C(3) crops. This study provides some evidence that C(4) and C(3) grasses do not differ in how sugars are sensed. While sugar sensor gene expression has a degree of stability along the leaf, there are some contrasts between the mesophyll and bundle sheath cells.