Dalle Carbonare Laura, van Veen Hans, Shukla Vinay, Perri Monica, Bui Liem, Holdsworth Michael J, Licausi Francesco
School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK; Department of Biology, University of Oxford, Oxford OX1 3RB, UK.
Groningen Institute of Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands.
Mol Plant. 2025 Jun 2;18(6):1072-1087. doi: 10.1016/j.molp.2025.05.015. Epub 2025 May 28.
The transcriptional response to low oxygen (hypoxia) in flowering plants is mediated by group VII Ethylene Response Factor (ERFVII) transcription factors, whose proteolysis is oxygen-dependent via the PLANT CYSTEINE OXIDASE (PCO) N-degron pathway. However, when and how this hypoxia response evolved in land plants remains unknown. In this study, we investigated the conservation and divergence of transcriptional responses to hypoxia across major land plant clades. We found that the induction of gene functions associated with glycolysis and fermentation is part of a conserved response across all land plant divisions.Evolutinary analyses suggest that ERFVIIs emerged in the last common ancestor of vascular plants with true roots, coinciding with the evolution of oxygen-dependent destabilization mechanisms that regulate hypoxia-adaptive genes. Proteins from other ERF groups have been independently recruited multiple times in different clades as substrates of the PCO N-degron pathway. Taken together, our results demonstrate that the response of land plants to hypoxia has been refined in derived clades through the evolution of ERFVIIs as transcriptional transducers, which occurred concurrently with the emergence of vascular systems and roots as foraging structures in hypoxic soils.
开花植物对低氧（缺氧）的转录反应由VII类乙烯反应因子（ERFVII）转录因子介导，其蛋白水解通过植物半胱氨酸氧化酶（PCO）N-降解途径依赖于氧气。然而，这种缺氧反应在陆地植物中何时以及如何进化仍不清楚。在本研究中，我们调查了主要陆地植物分支对缺氧的转录反应的保守性和差异性。我们发现，与糖酵解和发酵相关的基因功能的诱导是所有陆地植物门类保守反应的一部分。进化分析表明，ERFVIIs出现在具有真正根的维管植物的最后一个共同祖先中，这与调节缺氧适应性基因的氧依赖性不稳定机制的进化相吻合。来自其他ERF组的蛋白质在不同分支中多次被独立招募为PCO N-降解途径的底物。综上所述，我们的结果表明，陆地植物对缺氧的反应在衍生分支中通过ERFVIIs作为转录传感器的进化而得到优化，这与维管系统和根作为缺氧土壤中的觅食结构的出现同时发生。
