Comparative Transcriptome Analysis of Hypocotyls During the Developmental Transition of C 3 Cotyledons to C 4 Leaves in Halimocnemis mollissima Bunge

Identification of signaling pathways that control C 4 photosynthesis development is essential for introducing the C 4 pathway into C 3 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 C 3 photosynthesis in its cotyledons and a NAD-ME subtype of C 4 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 C 4 traits, including efficient resource usage by comparing the mRNA content of hypocotyls before and after the C 4 first leave’s formation. Histological examination showed the presence of C 3 anatomy in cotyledons and C 4 anatomy in the FLs. Our transcriptome analyses verified the performance of the NAD-ME subtype of C 4 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 C 4 photosynthetic and provide insights into the coordinated above- and under-ground tissue communication during the developmental transition of C 3 –C 4 photosynthesis in this species. Graphical Abstract