Comparative Transcriptome Analysis of Hypocotyls During the Developmental Transition of C₃cotyledons to C₄Leaves inHalimocnemis mollissimaBunge

AbstractIdentification of signaling pathways that control C4photosynthesis development is essential for introducing the C4pathway into C3crops. Species with dual photosynthesis in their life cycle are interesting models to study such regulatory mechanisms. The species used hereHalimocnemis mollissimaBunge, belonging to the Caroxyleae tribe, displays C3photosynthesis in its cotyledons and a NAD-ME subtype of C4photosynthesis 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 C4traits, including efficient resource usage by comparing the mRNA content of hypocotyls before and after the C4first leave’s formation. Histological examination showed the presence of C3anatomy in cotyledons and C4anatomy in the FLs. Our transcriptome analyses verified the performance of the NAD-ME subtype of C4in FLs and revealed differential transcript abundance of several potential mobile regulators and their associated receptors or transporters in two developmentally different hypocotyls ofH. mollissimaBunge. 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 C4photosynthetic and provide insights into the coordinated above- and under-ground tissue communication during the developmental transition of C3to C4photosynthesis in this species.