Network analysis of Arabidopsis mitochondrial dynamics reveals a resolved tradeoff between physical distribution and social connectivity.
Network analysis of Arabidopsis mitochondrial dynamics reveals a resolved tradeoff between physical distribution and social connectivity.
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DOI：
10.1016/j.cels.2021.04.006
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发表时间：
2021-05-19
期刊：
影响因子：
9.3
通讯作者：
Johnston IG
中科院分区：
文献类型：
--
作者：
Chustecki JM;Gibbs DJ;Bassel GW;Johnston IG
植物细胞中的线粒体主要作为单独的细胞器存在，它们移动、共定位和相互作用，但这些动力学所解决的细胞优先级仍然不完全清楚。在这里，我们通过研究拟南芥野生型和突变体线粒体的动态“社会网络”来阐明这些原则，描述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。我们确定了线粒体物理优先级（线粒体的均匀细胞分布）和“社会”优先级（个体相互作用，促进化学物质和信息的交换）之间不可避免的权衡。这种权衡导致了维持线粒体间隔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，倾向于具有高交换内容潜力的高效网络。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力学背后的基本原理。本文的透明同行评议过程记录包含在补充信息中。植物线粒体的动态社会网络反映了细胞器的物理相遇网络分析和建模显示了线粒体运动的优先级和权衡植物细胞中的线粒体权衡了物理间隔与社会联系植物细胞倾向于具有高信息交换潜力的高效网络植物细胞中的线粒体具有高度的运动性，并且作为个体移动（与其他类群中经常高度连接的网络相反）。这一动议的原因尚不清楚。本研究使用拟南芥的单细胞活成像来表征线粒体之间相遇的“社会”网络。网络分析和建模揭示了维持线粒体物理间隔和它们的社会互动之间的细胞权衡。线粒体动力学通过为代谢和遗传信息的交换提供有效的网络来解决这种权衡，同时保持细胞器的良好传播。细胞器的物理和社会异质性是这种效率的必然结果。
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. Dynamic social networks of plant mitochondria reflect physical organellar encounters Network analysis and modeling show priorities and tradeoffs for mitochondrial motion Mitochondria in plant cells trade off physical spacing against social connectivity Plant cells favor efficient networks with high potential for information exchange Mitochondria in plant cells are highly motile and move as individuals (in contrast to the often highly connected networks in other taxa). The reasons for this motion remain unclear. This study uses single-cell live imaging of Arabidopsis to characterize “social” networks of encounters between mitochondria. Network analysis and modeling reveal a cellular tradeoff between maintaining the physical spacing of mitochondria and their social interactions. Mitochondrial dynamics resolve this tradeoff by providing efficient networks for the exchange of metabolic and genetic information, while keeping organelles well spread. Physical and social heterogeneity of organelles arises as a necessary result of this efficiency.
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影响因子：
5.6
作者：
Jaipargas EA;Barton KA;Mathur N;Mathur J
通讯作者：
Mathur J
影响因子：
4
作者：
Barton, Kiah A.;Wozny, Michael R.;Mathur, Jaideep
通讯作者：
Mathur, Jaideep
影响因子：
1.6
作者：
Doniwa, Yoko;Arimura, Shin-ichi;Tsutsumi, Nobuhiro
通讯作者：
Tsutsumi, Nobuhiro
DOI：
10.1002/bies.201400188
发表时间：
2015-06
期刊：
BioEssays : news and reviews in molecular, cellular and developmental biology
影响因子：
--
作者：
Hoitzing H;Johnston IG;Jones NS
通讯作者：
Jones NS
影响因子：
11.4
作者：
Liu, Xingguo;Weaver, David;Hajnoczky, Gyoergy
通讯作者：
Hajnoczky, Gyoergy