Rewiring of chromatin regulation underlies the evolution of brown algal multicellularity

Chromatin structure plays a central role in regulating transcription, genome stability, and epigenetic inheritance in eukaryotes. Much of our understanding of chromatin architecture and histone post-translational modifications (hPTMs) comes from a narrow set of animal and plant models, but emerging data from non-model lineages are challenging canonical views of how chromatin functions across the tree of life. Brown algae are complex multicellular eukaryotes that provide a unique perspective on chromatin evolution given their independent origin of complex multicellularity. Here, we compile the chromatin toolkit of brown algae and show that canonical silencing systems involving DNA cytosine methylation and PRC2-mediated H3K27 methylation were lost early in their evolution. By generating hPTM profiles from diverse brown algal clades, we resolve the nature and regulatory roles of chromatin states in this lineage and show how H3K79 methylation emerged and diversified as a repressive system. We further uncover sex-specific reconfigurations in species with varying degrees of sexual dimorphism and reconstruct the ancestral regulatory landscape that likely preceded the emergence of brown algae. Together, our findings illuminate the dynamic evolution of chromatin regulation in a distinct multicellular lineage and challenge assumptions about the universality of chromatin-based mechanisms across eukaryotes.

染色质结构在真核生物的转录调控、基因组稳定性维持以及表观遗传继承过程中发挥核心作用。目前学界对染色质架构与组蛋白翻译后修饰（histone post-translational modifications，简称hPTMs）的认知大多局限于有限的动物与植物模式物种，但来自非模式物种谱系的新兴数据正不断挑战我们关于整个生命之树中染色质功能的经典认知。褐藻是一类复杂的多细胞真核生物，因其复杂多细胞性的独立起源，为染色质演化研究提供了独特视角。本研究整合了褐藻的染色质工具包，证实其演化早期便丢失了涉及DNA胞嘧啶甲基化与PRC2介导的H3K27甲基化的经典沉默系统。本研究通过获取多样褐藻支系的组蛋白翻译后修饰谱，解析了该谱系中染色质状态的本质与调控功能，并揭示了H3K79甲基化如何演化并分化为一套抑制性调控系统。我们还进一步发现了在不同程度性二态性物种中存在的性别特异性染色质重塑，并重构了褐藻起源前可能存在的祖先调控图谱。综上，本研究阐明了这一独特多细胞谱系中染色质调控的动态演化过程，同时挑战了学界关于真核生物中基于染色质的调控机制具有普适性的既有假设。