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Identification of various aspects of C4 photosynthesis regulation 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 through comparative analysis due to the lack of phylogenetic noises. Accordingly, the present research used Halimocnemis mollissima, which belonged to the Caroxyleae tribe, with C3 (in cotyledons) and NAD-ME subtype of C4 photosynthesis (in first leaves onwards) in its annual life cycle. We focused on exploring 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 C4 first leaves formation. As most likely part of the gene expression changes in hypocotyls observed in our study reflect those involved in the development of hypocotyls, we tried to exclude them by comparing our data with differentially expressed genes (DEGs) that had previously been identified in developing hypocotyls of flax and hemp. Our analyses revealed that several mobile regulators were differentially expressed in two developmentally different hypocotyls of H. mollissima, which belong to various transcription factors (TFs), phytohormones metabolism, and signaling peptides. Moreover, several up-regulated TFs in hypocotyls after establishing the C4 first leaves were stress-responsive. Our results provide insights into the necessity of above- and under-ground tissue communication during the developmental transition of photosynthesis strategy in this species to manifest functional C4 traits, especially nitrogen and water use efficiency and drought resistance.

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