Chloroplasts extend stromules independently and in response to internal redox signals

Chloroplasts extend stromules independently and in response to internal redox signals
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DOI:
10.1073/pnas.1511570112
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发表时间:
2015-08-11
影响因子:
11.1
通讯作者:
Zambryski, Patricia C.
Zambryski, Patricia C.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Brunkard, Jacob O.;Runkel, Anne M.;Zambryski, Patricia C.

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植物细胞生物学的一个基本谜团是“基质”的发生,这是由叶绿体(如叶绿体)形成的充满基质的管状延伸,在植物中普遍观察到,但其功能实际上是完全未知的。一种流行的假说是,种间菌在叶绿体和其他亚细胞室之间交换信号或代谢物,并且种间菌在胁迫期间被诱导。到目前为止,还没有发现起源于叶绿体的信号机制来调节球茎的活动,这是这一假说中缺失的关键一环。使用共聚焦和超分辨率3D显微镜,我们已经证明了叶绿体内光敏氧化还原信号的响应形成了球茎。在白天或在用化学物质处理后,球茎频率增加,这种化学物质特别是在叶绿体中产生活性氧物种。叶绿体氧化还原信号通路的中心枢纽叶绿体NADPH依赖的硫氧还蛋白还原酶的沉默表达增加了叶绿体基质部的频率,而与叶绿体基因组表达和四吡咯生物合成相关的核基因的沉默对基质部没有影响。不会进行光合作用的白细胞体在白天也会产生更多的球茎。白质体对相同的氧化还原信号通路没有反应,而是在暴露于光合作用的主要产物蔗糖时增加了球茎的形成,尽管蔗糖对叶绿体球茎的频率没有影响。因此,不同类型的叶绿体会对不同的信号做出反应。最后,分离的叶绿体从细胞质中提取后可以独立地产生种球,这表明叶绿体相关因子足以产生种球。这些发现表明,叶绿体是非常自主的细胞器,可以根据内部信号转导途径改变其球茎频率。
A fundamental mystery of plant cell biology is the occurrence of "stromules," stroma-filled tubular extensions from plastids (such as chloroplasts) that are universally observed in plants but whose functions are, in effect, completely unknown. One prevalent hypothesis is that stromules exchange signals or metabolites between plastids and other subcellular compartments, and that stromules are induced during stress. Until now, no signaling mechanisms originating within the plastid have been identified that regulate stromule activity, a critical missing link in this hypothesis. Using confocal and superresolution 3D microscopy, we have shown that stromules form in response to light-sensitive redox signals within the chloroplast. Stromule frequency increased during the day or after treatment with chemicals that produce reactive oxygen species specifically in the chloroplast. Silencing expression of the chloroplast NADPH-dependent thioredoxin reductase, a central hub in chloroplast redox signaling pathways, increased chloroplast stromule frequency, whereas silencing expression of nuclear genes related to plastid genome expression and tetrapyrrole biosynthesis had no impact on stromules. Leucoplasts, which are not photosynthetic, also made more stromules in the daytime. Leucoplasts did not respond to the same redox signaling pathway but instead increased stromule formation when exposed to sucrose, a major product of photosynthesis, although sucrose has no impact on chloroplast stromule frequency. Thus, different types of plastids make stromules in response to distinct signals. Finally, isolated chloroplasts could make stromules independently after extraction from the cytoplasm, suggesting that chloroplast-associated factors are sufficient to generate stromules. These discoveries demonstrate that chloroplasts are remarkably autonomous organelles that alter their stromule frequency in reaction to internal signal transduction pathways.