Singlet Oxygen Leads to Structural Changes to Chloroplasts during their Degradation in the Arabidopsis thaliana plastid ferrochelatase two Mutant

Singlet Oxygen Leads to Structural Changes to Chloroplasts during their Degradation in the Arabidopsis thaliana plastid ferrochelatase two Mutant
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DOI:
10.1093/pcp/pcab167
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发表时间:
2021-12-11
影响因子:
4.9
通讯作者:
Woodson, Jesse D.
Woodson, Jesse D.
中科院分区:
生物学2区
文献类型:
--
作者:
Fisher, Karen E.;Krishnamoorthy, Praveen;Woodson, Jesse D.

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在胁迫过程中,叶绿体产生大量的活性氧(ROS)。叶绿体还含有许多营养物质,包括叶片80%的氮供应。因此,为了保护细胞免受光氧化损伤,并将营养物质重新分配到水槽组织,叶绿体是降解的主要目标。光氧化胁迫或营养饥饿可诱导多种叶绿体降解途径,但对受损或衰老的叶绿体被鉴定、运输到中央液泡并降解的机制还不清楚。在此,我们研究了拟南芥质体亚铁螯合酶2(fc2)突变体中参与ROS单线态氧(O-1(2))诱导的叶绿体降解的结构。在轻度O-1(2)胁迫下,fc2叶绿体多数正常,但淀粉含量降低。叶绿体的一个子集是降解,和一些突出到中央液泡通过“起泡”结构。三维电子显微镜分析表明,高达35%的降解叶绿体含有这样的结构。虽然叶绿体在细胞内的位置并不影响其降解的可能性,海绵叶肉细胞中的叶绿体降解速率高于栅栏叶肉细胞中的叶绿体。为了确定降解的叶绿体是否具有独特的结构特征,使它们能够与健康的叶绿体区分开来,我们分析了在不同水平的光氧化胁迫下生长的fc2幼苗。叶绿体肿胀、O-1(2)信号和降解状态之间存在相关性。最后,参与叶绿体解体的质体小球(PG)酶被上调,而PG增加了它们与类囊体基粒的联系,暗示O-1(2)诱导的叶绿体降解和衰老途径之间的相互作用。
During stress, chloroplasts produce large amounts of reactive oxygen species (ROS). Chloroplasts also contain many nutrients, including 80% of a leaf's nitrogen supply. Therefore, to protect cells from photo-oxidative damage and to redistribute nutrients to sink tissues, chloroplasts are prime targets for degradation. Multiple chloroplast degradation pathways are induced by photo-oxidative stress or nutrient starvation, but the mechanisms by which damaged or senescing chloroplasts are identified, transported to the central vacuole and degraded are poorly defined. Here, we investigated the structures involved with degrading chloroplasts induced by the ROS singlet oxygen (O-1(2)) in the Arabidopsis thaliana plastid ferrochelatase two (fc2) mutant. Under mild O-1(2) stress, most fc2 chloroplasts appeared normal, but had reduced starch content. A subset of chloroplasts was degrading, and some protruded into the central vacuole via 'blebbing' structures. A 3D electron microscopy analysis demonstrated that up to 35% of degrading chloroplasts contained such structures. While the location of a chloroplast within a cell did not affect the likelihood of its degradation, chloroplasts in spongy mesophyll cells were degraded at a higher rate than those in palisade mesophyll cells. To determine if degrading chloroplasts have unique structural characteristics, allowing them to be distinguished from healthy chloroplasts, we analyzed fc2 seedlings grown under different levels of photo-oxidative stress. A correlation was observed among chloroplast swelling, O-1(2) signaling and the state of degradation. Finally, plastoglobule (PG) enzymes involved in chloroplast disassembly were upregulated while PGs increased their association with the thylakoid grana, implicating an interaction between O-1(2)-induced chloroplast degradation and senescence pathways.