Comparative Gene Expression and Physiological Analyses Reveal Molecular Mechanisms in Wound-Induced Spore Formation in the Edible Seaweed Nori

Abstract

Genetic reprogramming of differentiated cells is studied broadly in multicellular Viridiplantae as an adaptation to herbivory or damage; however, mechanisms underlying cell development and redifferentiation are largely unknown in red algae, their nearest multicellular relatives. Here we investgate cell reprogramming in the widely cultivated, edible seaweed Neopyropia yezoesis (“nori”), where vegetative cells in wounded blades differentiate and release as large numbers of asexual spores. Based upon physiological changes and transcriptomic dynamics after wound stress in N. yezoensis and its congener Neoporphyra haitanensis, another cultivar that does not differentiate spores after wounding, we propose a three-phase model of wound-induced spore development in N. yezoensis. In Phase I, propagation of ROS by RBOH and SOD elicites systematic transduction of the wound signal, while Ca2+ dependent signaling induces cell reprogramming. In Phase II, a TOR signaling pathway and regulation of cyclin and CDK genes result in cell divisions that spread inward from the wound edge. Once sporangia form, Phase III involves expression of proteins required for spore maturation and cell wall softening. Our analyses not only provide the first model for core molecular processes controlling cellular reprogramming in rhodophytes, but also have practical implications for achieving greater control over seeding in commercial nori farming.

Histone acetylation functions in the wound-induced spore formation in nori

“…To further identify genes that were associated with wound-induced cell fate transition and potentially regulated by HDACs, we selected genes that meet the following three criteria: a, exhibited significant transcriptional up-regulation at 6h in control medium; b, exhibited weak variation, or down-regulation in SAHA-treated medium; c, orthologs in Pyropia haitanensis also exhibited weak variation or down-regulation at 6h after wounding ( Guan et al., 2022 ). We identified 291 genes in this manner ( Figure 4C ; Supplementary Table S3 ).…”

“…Somatic cells in P. yezoensis thalli experience dedifferentiation and reprogram into asexual spores when they are under wound stress ( Chen et al., 2020 ). These complex physiological processes are associated with dynamic transcriptional responses ( Guan et al., 2022 ). However, little is known about the molecular mechanism that directs the wound-induced gene expression changes and subsequent cellular reprogramming.…”

“…Cutting thalli into fragments was performed exactly as described by Guan et al. ( Guan et al., 2022 ). SAHA (APExBIO, A4084) was dissolved in DMSO to prepare a 1.0 M stock solution.…”

“…According to morphological observation and gene expression analysis, it can be divided into three phases, including systematic transduction of the wound signals, cell proliferation, and spore maturation, in each of which many genes (including those related to ROS and Calcium signaling pathways, cell division, cell wall remodeling etc.) exhibit sequential transcriptional changes at certain time points ( Guan et al., 2022 ). However, the regulatory mechanisms that coordinate the gene expression remain unknown.…”

“…Despite the importance of epigenetic regulation in cell fate reprogramming in both animals and land plants, the biological relevance of histone acetylation in red algae is still elusive, except several genes encoding the SWI chromatin remodeling factors, which are the “sensors” of histone modification status, were identified in Pyropia genomes ( Stiller et al., 2018 ). The wound-induced spore formation in P. yezoensis , combining the availability of genome information, makes P. yezoensis an ideal research model of cell reprogramming in red algae ( Guan et al., 2022 ). In this study, we investigated the effect of SAHA on wound-induced spore formation in P. yezoensis and revealed that HDACs act as an essential epigenetic switch that renders the cell reprogramming of vegetative cells by modulating transcriptional levels of candidate target genes.…”