A Simple Auxin Transcriptional Response System Regulates Multiple Morphogenetic Processes in the Liverwort Marchantia polymorpha

In land plants comparative genomics has revealed that members of basal lineages share a common set of transcription factors with the derived flowering plants, despite sharing few homologous structures. The plant hormone auxin has been implicated in many facets of development in both basal and derived lineages of land plants. We functionally characterized the auxin transcriptional response machinery in the liverwort Marchantia polymorpha, a member of the basal lineage of extant land plants. All components known from flowering plant systems are present in M. polymorpha, but they exist as single orthologs: a single MpTOPLESS (TPL) corepressor, a single MpTRANSPORT INHIBITOR RESPONSE 1 auxin receptor, single orthologs of each class of AUXIN RESPONSE FACTOR (ARF; MpARF1, MpARF2, MpARF3), and a single negative regulator AUXIN/INDOLE-3-ACETIC ACID (MpIAA). Phylogenetic analyses suggest this simple system is the ancestral condition for land plants. We experimentally demonstrate that these genes act in an auxin response pathway — chimeric fusions of the MpTPL corepressor with heterodimerization domains of MpARF1, MpARF2, or their negative regulator, MpIAA, generate auxin insensitive plants that lack the capacity to pattern and transition into mature stages of development. Our results indicate auxin mediated transcriptional regulation acts as a facilitator of branching, differentiation and growth, rather than acting to determine or specify tissues during the haploid stage of the M. polymorpha life cycle. We hypothesize that the ancestral role of auxin is to modulate a balance of differentiated and pluri- or totipotent cell states, whose fates are determined by interactions with combinations of unrelated transcription factors.陆生植物比较基因组学研究显示，尽管基部类群与衍生的被子植物共享的同源结构极少，但二者拥有一套共有的转录因子。植物激素生长素（auxin）已被证实参与陆生植物基部类群与衍生类群的诸多发育过程。我们对现存陆生植物基部类群成员——地钱（Marchantia polymorpha）中的生长素转录响应机制开展了功能表征。被子植物系统中已知的所有组分均存在于地钱基因组中，但均以单一直系同源基因（ortholog）形式存在：单个MpTOPLESS（TPL）共抑制因子、单个MpTRANSPORT INHIBITOR RESPONSE 1生长素受体、每类生长素响应因子（AUXIN RESPONSE FACTOR，ARF；MpARF1、MpARF2、MpARF3）的单一直系同源基因，以及单个负调控因子生长素/吲哚-3-乙酸（AUXIN/INDOLE-3-ACETIC ACID，MpIAA）。系统发育分析表明，这一简化系统代表了陆生植物的祖先状态。我们通过实验证实，这些基因参与生长素响应通路：将MpTPL共抑制因子与MpARF1、MpARF2或其负调控因子MpIAA的异二聚化结构域进行嵌合融合，可获得生长素不敏感植株，此类植株丧失了模式建成与向发育成熟阶段转变的能力。我们的研究结果显示，在地钱生命周期的单倍体阶段，生长素介导的转录调控主要发挥分枝、分化与生长的促进作用，而非参与组织的命运决定或特化过程。我们推测，生长素的祖先功能是调控分化细胞与多能/全能细胞状态间的平衡，而细胞命运由其与其他无关转录因子组合的相互作用所决定。