Autophagy and its mediated mitochondrial quality control maintain pollen tube growth and male fertility in Arabidopsis.
Autophagy and its mediated mitochondrial quality control maintain pollen tube growth and male fertility in Arabidopsis.
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自噬及其介导的线粒体质量控制维持拟南芥花粉管生长和雄性生育力
DOI：
10.1080/15548627.2022.2095838
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发表时间：
2023-03
期刊：
影响因子：
13.3
通讯作者：
Wang, Hao
中科院分区：
文献类型：
--
作者：
Yan, He;Zhuang, Menglong;Xu, Xiaoyu;Li, Shanshan;Yang, Mingkang;Li, Nianle;Du, Xiaojuan;Hu, Kangwei;Peng, Xiaomin;Huang, Wei;Wu, Hong;Tse, Yu Chung;Zhao, Lifeng;Wang, Hao
宏自噬/自噬是真核生物主要的分解代谢途径，参与植物的有性繁殖，包括雄配子发生和自交不亲和反应。花粉管的快速生长是另一个重要的生殖过程，它在代谢上要求很高，以推动细胞的旺盛生长，以交付被子植物受精的雄配子。自噬是否以及如何维持花粉管的动态平衡尚不清楚。在这里，我们提供的证据表明，自噬在生长的花粉管中是升高的，并且在拟南芥的花粉管生长和雄性育性过程中是至关重要的。我们证明，SH3P2是植物自噬的关键非ATG调节因子，在生长的花粉管中，在自噬小体的生物发生过程中，SH3P2与有代表性的ATG蛋白共存。SH3P2表达下调显著干扰拟南芥花粉萌发和花粉管生长。细胞器动力学的进一步分析表明，在磷脂酰肌醇3-激酶被抑制后，自噬小体和泡前隔室之间存在串扰。此外，对ATG8e标记的自噬小体和去极化线粒体的时间推移成像和跟踪表明，它们通过ATG8家族相互作用基序(AIM)对接位点特异性地相互作用，介导有丝分裂。对有丝分裂噬菌体和另外两种自噬小体的超微结构鉴定表明，多种类型的自噬很可能在花粉管中同时发挥作用。总之，我们的结果表明，在花粉管生长过程中，自噬对于调节线粒体质量控制和典型的细胞质循环是至关重要的。缩写：目的：ATG8家族相互作用基序；ATG8：自噬相关8；ATG5：自噬相关5；ATG7：自噬相关7；BTH：酸苯基-S-甲基；地塞米松；DNP：2，4-二硝基酚；GFP：绿色荧光蛋白；YFP：黄色荧光蛋白；PtdIns3K：磷脂酰肌醇-3-激酶；PtdIns3P：磷脂酰肌醇-3-磷酸；PVC：前泡间隔；SH3P2：SH3结构域蛋白2。
Macroautophagy/autophagy, a major catabolic pathway in eukaryotes, participates in plant sexual reproduction including the processes of male gametogenesis and the self-incompatibility response. Rapid pollen tube growth is another essential reproductive process that is metabolically highly demanding to drive the vigorous cell growth for delivery of male gametes for fertilization in angiosperms. Whether and how autophagy operates to maintain the homeostasis of pollen tubes remains unknown. Here, we provide evidence that autophagy is elevated in growing pollen tubes and critically required during pollen tube growth and male fertility in Arabidopsis. We demonstrate that SH3P2, a critical non-ATG regulator of plant autophagy, colocalizes with representative ATG proteins during autophagosome biogenesis in growing pollen tubes. Downregulation of SH3P2 expression significantly disrupts Arabidopsis pollen germination and pollen tube growth. Further analysis of organelle dynamics reveals crosstalk between autophagosomes and prevacuolar compartments following the inhibition of phosphatidylinositol 3-kinase. In addition, time-lapse imaging and tracking of ATG8e-labeled autophagosomes and depolarized mitochondria demonstrate that they interact specifically via the ATG8-family interacting motif (AIM)-docking site to mediate mitophagy. Ultrastructural identification of mitophagosomes and two additional forms of autophagosomes imply that multiple types of autophagy are likely to function simultaneously within pollen tubes. Altogether, our results suggest that autophagy is functionally crucial for mediating mitochondrial quality control and canonical cytoplasm recycling during pollen tube growth. Abbreviations: AIM: ATG8-family interacting motif; ATG8: autophagy related 8; ATG5: autophagy related 5; ATG7: autophagy related 7; BTH: acibenzolar-S-methyl; DEX: dexamethasone; DNP: 2,4-dinitrophenol; GFP: green fluorescent protein; YFP: yellow fluorescent protein; PtdIns3K: phosphatidylinositol 3-kinase; PtdIns3P: phosphatidylinositol-3-phosphate; PVC: prevacuolar compartment; SH3P2: SH3 domain-containing protein 2.
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