Compartmentation of photosynthesis gene expression between mesophyll and bundle sheath cells of C4maize is dependent on time of day

Abstract

AbstractCompared with the ancestral C3state, C4photosynthesis enables higher rates of photosynthesis as well as improved water and nitrogen use efficiencies. In both C3and C4plants rates of photosynthesis increase with light intensity and so are maximal around midday. We report that in the absence of light or temperature fluctuations, photosynthesis in maize peaks in the middle of the subjective photoperiod. To investigate molecular processes associated with these changes, we undertook RNA-sequencing of maize mesophyll and bundle sheath strands over a 24-hour time-course. Cell-preferential expression of C4cycle genes was strongest between six and ten hours after dawn when rates of photosynthesis were highest. For the bundle sheath, DNA motif enrichment and gene co-expression analyses suggested members of the DOF and MADS-domain transcription factor families mediate diurnal fluctuations in C4gene expression, andtrans-activation assaysin plantaconfirmed their ability to activate promoter fragments from bundle sheath expressed genes. The work thus identifies transcriptional regulators as well as peaks in cell-specific C4gene expression coincident with maximum rates of photosynthesis in the maize leaf at midday.