Comparative Transcriptome Analysis of Emerging Young and Mature Leaves of Bienertia sinuspersici, a Single-Cell C4 Plant

Abstract

Abstract Efficient carbon capture by plants is crucial to meet the increasing demands for food, fiber, feed, and fuel worldwide. One potential strategy to improve photosynthetic performance of plants is the conversion of C3-type crops to C4-type crops, enabling them to perform photosynthesis at higher temperatures and with less water. C4-type crops, such as corn, possess a distinct Kranz anatomy, where photosynthesis occurs in two distinct cell types. Remarkably, Bienertia sinuspersici is one of the four known land plant species to perform C4 photosynthesis within a single cell, characterized by dimorphic chloroplasts and corresponding intracellular biochemistry. The young emerging leaves exhibit C3 anatomy which differentiate into the unique single cell C4 anatomy as the leaves mature. A comparative transcriptome analysis yielded a total of 72,820 unique transcripts in young and 72,253 transcripts in mature leaves of B. sinuspersici. In the young leaf, enrichment of processes associated with the cell cycle, cellular developmental patterning, and transcriptional regulatory mechanisms was observed. The mature leaf displayed enrichment of processes associated with photosynthesis, chloroplast components, translational components, and post-translational modifications. Notably, several transcription factors such as auxin response factor (ARF), basic helix-loop-helix (bHLH), GATA, homeodomain (HD), MYB, NAC, squamosa promoter-binding protein-like (SPL), and zinc finger (ZF) family were differentially expressed in in the young leaf. These data expand our insights into the molecular basis of Bienertia’s unique cellular compartmentalization, chloroplast dimorphism, and single-cell C4 biochemistry, and the information can be useful in the ongoing efforts to transform C3-type crops into C-4 type.