Transcriptional architecture underlying development, adaptation, and domestication in Northern Wild Rice (Zizania palustris L.)

Abstract

AO_SCPLOWBSTRACTC_SCPLOWZizania palustris (Northern Wild Rice) is an aquatic grass native to North America and a crop wild relative of Oryza sativa with ecological, cultural, and agricultural significance. Here, we present a transcriptomic atlas spanning 20 tissues across six major developmental stages. Seed tissues showed shifts in abscisic acid, gibberellin, and ethylene pathways that define the hormonal basis of deep dormancy in this recalcitrant species and its release. Leaf development showed stage-specific reprogramming, from hypoxia-responsive programs in submerged tissues to cell wall remodeling and redox regulation during aquatic-aerial transitions, with photosynthesis and carbohydrate metabolism defining flag leaves and SRG1 divergence emerging as a defining feature of leaf development in Z. palustris. Reproductive tissues expressed duplicated homologs of well-recognized shattering genes with divergent regulation, consistent with subfunctionalization after whole-genome duplication. These findings provide new insight into traits underlying ecological adaptation and domestication in Z. palustris and related grasses. CORE IDEASO_LIA first transcriptomic atlas for Northern Wild Rice maps gene expression across 20 tissues and six developmental stages, providing a foundational functional genomics resource for Zizania palustris. C_LIO_LISeed dormancy and release are driven by coordinated hormone reprogramming, with shifts in ABA, GA, and ethylene pathways across whole seed, embryo, and endosperm. C_LIO_LILeaf development is defined by aquatic-to-aerial transcriptional transitions, moving from hypoxia-responsive programs in submerged tissues to cell wall remodeling, redox regulation, and photosynthesis/metabolism in aerial and flag leaves. C_LIO_LIWhole-genome duplication underlies regulatory divergence in domestication traits, as duplicated homologs of canonical seed shattering genes show paralog- and tissue-specific expression consistent with subfunctionalization. C_LIO_LIThe atlas identifies tissue-specific modules and stable housekeeping candidates, enabling improved experimental design (e.g., expression normalization) and accelerating candidate prioritization for breeding, GWAS/eQTL, and trait discovery. C_LI PLAIN LANGUAGE SUMMARYNorthern Wild Rice (Zizania palustris) is an aquatic grass native to North America that is important for ecosystems, agriculture, and Indigenous cultures. In this study, we created a detailed gene expression map across 20 different tissues and six stages of plant development. We found that seeds strongly regulate plant hormones that control dormancy, helping explain why Northern Wild Rice seeds remain dormant for long periods and how they eventually germinate. Leaves showed clear changes in gene activity as plants moved from underwater growth to above-water growth, shifting from low-oxygen stress responses to processes that support photosynthesis and structural strength. In flowers, we identified duplicated genes involved in seed shattering that are regulated differently, likely due to past genome duplication events. Together, these results improve our understanding of how Northern Wild Rice is adapted to aquatic environments and how key traits relevant to domestication have evolved.