Comparative Transcriptome Analysis of Hypocotyls During the Developmental Transition of C₃ cotyledons to C₄ Leaves in Halimocnemis mollissima Bunge

Abstract

Identification of signaling pathways that control C₄ photosynthesis development is essential for introducing the C₄ pathway into C₃ crops. Species with dual photosynthesis in their life cycle are interesting models to study such regulatory mechanisms. The species used here Halimocnemis mollissima Bunge, belonging to the Caroxyleae tribe, displays C₃ photosynthesis in its cotyledons and a NAD-ME subtype of C₄ photosynthesis in the First leaves (FLs) onwards. We explored the long-distance signaling pathways that are probably implicated in the shoot-root coordination associated with the manifestation of the C₄ traits, including efficient resource usage by comparing the mRNA content of hypocotyls before and after the C₄ first leave’s formation. Histological examination showed the presence of C₃ anatomy in cotyledons and C₄ anatomy in the FLs. Our transcriptome analyses verified the performance of the NAD-ME subtype of C₄ in FLs and revealed differential transcript abundance of several potential mobile regulators and their associated receptors or transporters in two developmentally different hypocotyls of H. mollissima Bunge. These differentially expressed genes (DEGs) belong to diverse functional groups, including various transcription factor (TF) families, phytohormones metabolism, and signaling peptides, part of which could be related to hypocotyl development. Our findings support the higher nitrogen and water use efficiency associated with C₄ photosynthetic and provide insights into the coordinated above- and under-ground tissue communication during the developmental transition of C₃ to C₄ photosynthesis in this species.