Department of Biochemistry and Molecular Biology, Dalhousie University, Sir Charles Tupper Medical Building, 5850 College Street, Halifax, NS, B3H 4R2, Canada.
Institute of Microbiology, Technische Universität Braunschweig, Spielmannstr. 7, 38106, Braunschweig, Germany.
Plant J. 2020 Aug;103(3):1025-1048. doi: 10.1111/tpj.14782. Epub 2020 May 16.
All land plants (embryophytes) share a common ancestor that likely evolved from a filamentous freshwater alga. Elucidating the transition from algae to embryophytes - and the eventual conquering of Earth's surface - is one of the most fundamental questions in plant evolutionary biology. Here, we investigated one of the organismal properties that might have enabled this transition: resistance to drastic temperature shifts. We explored the effect of heat stress in Mougeotia and Spirogyra, two representatives of Zygnematophyceae - the closest known algal sister lineage to land plants. Heat stress induced pronounced phenotypic alterations in their plastids, and high-performance liquid chromatography-tandem mass spectroscopy-based profiling of 565 transitions for the analysis of main central metabolites revealed significant shifts in 43 compounds. We also analyzed the global differential gene expression responses triggered by heat, generating 92.8 Gbp of sequence data and assembling a combined set of 8905 well-expressed genes. Each organism had its own distinct gene expression profile; less than one-half of their shared genes showed concordant gene expression trends. We nevertheless detected common signature responses to heat such as elevated transcript levels for molecular chaperones, thylakoid components, and - corroborating our metabolomic data - amino acid metabolism. We also uncovered the heat-stress responsiveness of genes for phosphorelay-based signal transduction that links environmental cues, calcium signatures and plastid biology. Our data allow us to infer the molecular heat stress response that the earliest land plants might have used when facing the rapidly shifting temperature conditions of the terrestrial habitat.
所有陆地植物（胚胎植物）都有一个共同的祖先，这个祖先可能是从丝状淡水藻类进化而来的。阐明从藻类到胚胎植物的转变——以及最终征服地球表面——是植物进化生物学中最基本的问题之一。在这里，我们研究了可能使这种转变成为可能的生物体特性之一：抵抗剧烈的温度变化。我们探索了热应激对两个丝藻纲代表植物——最接近陆地植物的藻类姐妹群——满江红和水绵的影响。热应激导致它们的质体发生明显的表型改变，基于高效液相色谱-串联质谱分析的 565 个主要中心代谢物的分析揭示了 43 种化合物的显著变化。我们还分析了热引发的全局差异基因表达反应，生成了 92.8 Gbp 的序列数据，并组装了一套由 8905 个表达良好的基因组成的综合数据集。每个生物体都有其独特的基因表达谱；它们共享的基因中不到一半表现出一致的基因表达趋势。然而，我们检测到了一些共同的热应激反应特征，例如分子伴侣、类囊体成分的转录水平升高，以及——与我们的代谢组学数据相呼应——氨基酸代谢。我们还发现了基于磷酸接力的信号转导基因对热的反应性，这种信号转导将环境线索、钙特征和质体生物学联系起来。我们的数据使我们能够推断出最早的陆地植物在面对陆地栖息地快速变化的温度条件时可能使用的分子热应激反应。
