School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK.
Department of Life Sciences, University of Warwick, Coventry CV4 7AL, UK.
Cell Syst. 2021 May 19;12(5):419-431.e4. doi: 10.1016/j.cels.2021.04.006. Epub 2021 May 10.
Mitochondria in plant cells exist largely as individual organelles which move, colocalize, and interact, but the cellular priorities addressed by these dynamics remain incompletely understood. Here, we elucidate these principles by studying the dynamic "social networks" of mitochondria in Arabidopsis thaliana wildtype and mutants, describing the colocalization of individuals over time. We combine single-cell live imaging of hypocotyl mitochondrial dynamics with individual-based modeling and network analysis. We identify an inevitable tradeoff between mitochondrial physical priorities (an even cellular distribution of mitochondria) and "social" priorities (individuals interacting, to facilitate the exchange of chemicals and information). This tradeoff results in a tension between maintaining mitochondrial spacing and facilitating colocalization. We find that plant cells resolve this tension to favor efficient networks with high potential for exchanging contents. We suggest that this combination of physical modeling coupled to experimental data through network analysis can shed light on the fundamental principles underlying these complex organelle dynamics. A record of this paper's transparent peer review process is included in the supplemental information.
植物细胞中的线粒体主要作为单个细胞器存在，这些细胞器会移动、共定位并相互作用，但这些动态所涉及的细胞优先级仍不完全清楚。在这里，我们通过研究拟南芥野生型和突变体中线粒体的动态“社交网络”来阐明这些原则，描述了个体随时间的共定位。我们将下胚轴线粒体动力学的单细胞实时成像与基于个体的建模和网络分析相结合。我们发现线粒体的物理优先级（线粒体在细胞中的均匀分布）和“社交”优先级（个体相互作用，以促进化学物质和信息的交换）之间存在不可避免的权衡。这种权衡导致了维持线粒体间距和促进共定位之间的紧张关系。我们发现，植物细胞解决了这种紧张关系，有利于建立高效的网络，从而实现更高的物质交换潜力。我们认为，通过网络分析将物理建模与实验数据相结合，可以揭示这些复杂细胞器动态的基本原则。本论文的透明同行评审过程记录包含在补充信息中。
