Abstract

Plants coordinate the expression of photosynthesis-related genes in response to growth and environmental changes. In species that conduct two-cell C4 photosynthesis, expression of photosynthesis genes is partitioned such that leaf mesophyll and bundle sheath cells accumulate different components of the photosynthetic pathway. The identities of the regulatory networks that facilitate this partitioning are unknown. Here, we show that differences in light perception between mesophyll and bundle sheath cells facilitate differential regulation and accumulation of photosynthesis gene transcripts in the C4 crop maize (Zea mays). Key components of the photosynthesis gene regulatory network differentially accumulated between mesophyll and bundle sheath cells, indicative of differential network activity across cell types. We further show that blue (but not red) light is necessary and sufficient to activate photosystem II assembly in mesophyll cells in etiolated maize. Finally, we demonstrate that 61% of all light-induced mesophyll and bundle sheath genes were induced only by blue light or only by red light, but not both. These findings provide evidence that subdivision of light signaling networks is a component of cellular partitioning of C4 photosynthesis in maize.

Highlights

  • Light is of fundamental importance to photoautotrophs, who harness energy from photons to synthesise sugars

  • Through spectrum specific de-etiolation experiments we show that blue light but not red resulted in rapid accumulation of chlorophyll fluorescence from functional photosystem II (PSII) assembly

  • To estimate the extent to which the gene regulatory network for photosynthesis was partitioned between bundle sheath and mesophyll cells in maize, the complete set of maize genes that are orthologous to Arabidopsis genes that encode known photoreceptors or light-modulated transcription factors were identified and analysed

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Summary

Introduction

Light is of fundamental importance to photoautotrophs, who harness energy from photons to synthesise sugars. In the model plant Arabidopsis thaliana, five families of photoreceptors, of varying spectral sensitivities, allow discrimination between different wavelengths of light. These families comprise the phytochromes, cryptochromes, phototropins, UVRs, and Zeitlupe proteins (Christie et al, 2015; Lin, 2000; Rizzini et al, 2011; Schepens et al, 2004; Smith, 2000). By linking light cues to the regulation of photosynthesis genes, plants are able to coordinate development of chloroplasts and optimise photosynthetic rates in mature leaf tissue under changing environmental conditions (Ohashi-Kaneko et al, 2006; Ort et al, 2011; Waters and Langdale, 2009)

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