Plant responses to coincident nutrient deficiencies cannot be predicted from the responses to individual deficiencies. Although copper (Cu) and iron (Fe) are essential micronutrients for plant growth that are often and concurrently limited in soils, the combinatorial response to Cu‐Fe deficiency remains elusive. In the present study, we characterised the responses of Arabidopsis thaliana plants deprived of Cu, Fe or both (‐Cu‐Fe) at the level of plant development, mineral composition, and reconfiguration of transcriptomes, proteomes and metabolomes. Compared to single deficiencies, simultaneous ‐Cu‐Fe leads to a distinct pattern in leaf physiology and microelement concentration characterised by lowered protein content and enhanced manganese and zinc levels. Conditional networking analysis of molecular changes indicates that biological processes also display different co‐expression patterns among single and double deficiencies. Indeed, the interaction between Cu and Fe deficiencies causes distinct expression profiles for 15% of all biomolecules, leading to specific enhancement of general stress responses and protein homeostasis mechanisms, at the same time as severely arresting photosynthesis. Accordingly, central carbon metabolites, in particular photosynthates, decrease especially under ‐Cu‐Fe conditions, whereas the pool of free amino acids increases. Further meta‐analysis of transcriptomes and proteomes corroborated that protein biosynthesis and folding capacity were readjusted during the combinatorial response and unveiled important rearrangements in the metabolism of organic acids. Consequently, our results demonstrate that the response to ‐Cu‐Fe imposes a distinct reconfiguration of large sets of molecules, not triggered by single deficiencies, resulting into a switch from autotrophy to heterotrophy and involving organic acids such as fumaric acid as central mediators of the response.

中文翻译：

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拟南芥对同时缺铜和缺铁的反应的系统生物学。

无法从对单个营养素的反应中预测植物对同时发生的营养素缺乏的反应。尽管铜（Cu）和铁（Fe）是植物生长所必需的微量营养素，并且经常并发地限制在土壤中，但是对Cu-Fe缺乏的组合响应仍然难以捉摸。在本研究中，我们表征了拟南芥的反应。在植物发育，矿物质组成以及转录组，蛋白质组和代谢组重新配置的水平上，被剥夺了铜，铁或两者（铜-铁）的植物。与单一缺陷相比，同时发生Cu-Fe会导致叶片生理和微量元素浓度的明显变化，其特征是蛋白质含量降低，锰和锌含量提高。分子变化的条件网络分析表明，生物学过程在单缺陷和双缺陷中也表现出不同的共表达模式。确实，铜和铁缺乏之间的相互作用导致所有生物分子中15％的表达谱不同，从而导致一般应激反应和蛋白质稳态机制的特异性增强，同时严重阻止了光合作用。因此，中心碳代谢物，特别是光合产物，在铜-铁条件下尤其会减少，而游离氨基酸库增加。转录组和蛋白质组的进一步荟萃分析证实，在组合反应过程中蛋白质生物合成和折叠能力得到了重新调整，并揭示了有机酸代谢中的重要重排。因此，我们的研究结果表明，对铜铁的响应对大型分子构成了明显的重构，而并非由单一缺陷触发，导致从自养向异养转变，并涉及诸如富马酸的有机酸作为富马酸的主要介质。响应。转录组和蛋白质组的进一步荟萃分析证实了在组合反应过程中蛋白质生物合成和折叠能力得到了重新调整，并揭示了有机酸代谢中的重要重排。因此，我们的研究结果表明，对铜铁的响应对大型分子构成了明显的重构，而并非由单一缺陷触发，导致从自养向异养转变，并涉及诸如富马酸的有机酸作为富马酸的主要介质。响应。转录组和蛋白质组的进一步荟萃分析证实了在组合反应过程中蛋白质生物合成和折叠能力得到了重新调整，并揭示了有机酸代谢中的重要重排。因此，我们的研究结果表明，对铜铁的响应对大型分子构成了明显的重构，而并非由单一缺陷触发，导致从自养向异养转变，并涉及诸如富马酸的有机酸作为富马酸的主要介质。响应。