Impacts of high ATP supply from chloroplasts and mitochondria on the leaf metabolism of Arabidopsis thaliana.

Impacts of high ATP supply from chloroplasts and mitochondria on the leaf metabolism of Arabidopsis thaliana.
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叶绿体和线粒体高度ATP供应对拟南芥叶片代谢的影响。

DOI:
10.3389/fpls.2015.00922
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发表时间:
2015
影响因子:
5.6
通讯作者:
Lim BL
Lim BL
中科院分区:
生物学2区
文献类型:
--
作者:
Liang C;Zhang Y;Cheng S;Osorio S;Sun Y;Fernie AR;Cheung CY;Lim BL

文献摘要

被引文献

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叶绿体和线粒体是植物叶片中产生ATP的主要细胞器。拟南芥紫色酸性磷酸酶2 (AtPAP2)是一种双重靶向两种细胞器外膜的磷酸酶,它在选择核编码蛋白进入这两种细胞器的过程中起作用。AtPAP2在拟南芥中的过表达(OE)加速植物生长,促进开花、种子产量和成熟时的生物量。在夜间和光照16/8 h后的1 h和8 h,测定20日龄OE和野生型(WT)株系叶片中ADP/ATP/NADP+/NADPH含量,结果表明OE株系叶片中ATP水平和ATP/NADPH比值在三个时间点均显著升高。因此,AtPAP2 OE系是研究高能量对拟南芥整体分子状态影响的一个很好的模型。本研究检测了高ATP转基因品系的转录组、蛋白质组和代谢组谱,并与野生型植物进行了比较。在夜晚结束时,OE和WT的比较为线粒体更高的ATP输出对植物生理的影响提供了有价值的信息,因为线粒体呼吸是叶片黑暗中ATP的主要来源。同样,光照后OE和WT的比较将提供叶绿体高能量输出对植物生理影响的信息。发现AtPAP2的OE显著影响两个细胞器基因组编码基因的转录和蛋白质丰度。例如,在光照和黑暗条件下,AtPAP2 OE系叶绿体基因组编码的许多核糖体蛋白的蛋白质丰度都较高,而光合复合物的多个组分的蛋白质丰度则较低。RNA-seq数据还表明,线粒体基因组的转录受到能量可用性的极大影响。这些数据反映了细胞器基因组的转录和翻译与能量状态紧密耦合。该研究为高ATP水平对植物生理的影响提供了全面的信息,从细胞器生物学到初级和次级代谢。
Chloroplasts and mitochondria are the major ATP producing organelles in plant leaves. Arabidopsis thaliana purple acid phosphatase 2 (AtPAP2) is a phosphatase dually targeted to the outer membranes of both organelles and it plays a role in the import of selected nuclear-encoded proteins into these two organelles. Overexpression (OE) of AtPAP2 in A. thaliana accelerates plant growth and promotes flowering, seed yield, and biomass at maturity. Measurement of ADP/ATP/NADP+/NADPH contents in the leaves of 20-day-old OE and wild-type (WT) lines at the end of night and at 1 and 8 h following illumination in a 16/8 h photoperiod revealed that the ATP levels and ATP/NADPH ratios were significantly increased in the OE line at all three time points. The AtPAP2 OE line is therefore a good model to investigate the impact of high energy on the global molecular status of Arabidopsis. In this study, transcriptome, proteome, and metabolome profiles of the high ATP transgenic line were examined and compared with those of WT plants. A comparison of OE and WT at the end of the night provide valuable information on the impact of higher ATP output from mitochondria on plant physiology, as mitochondrial respiration is the major source of ATP in the dark in leaves. Similarly, comparison of OE and WT following illumination will provide information on the impact of higher energy output from chloroplasts on plant physiology. OE of AtPAP2 was found to significantly affect the transcript and protein abundances of genes encoded by the two organellar genomes. For example, the protein abundances of many ribosomal proteins encoded by the chloroplast genome were higher in the AtPAP2 OE line under both light and dark conditions, while the protein abundances of multiple components of the photosynthetic complexes were lower. RNA-seq data also showed that the transcription of the mitochondrial genome is greatly affected by the availability of energy. These data reflect that the transcription and translation of organellar genomes are tightly coupled with the energy status. This study thus provides comprehensive information on the impact of high ATP level on plant physiology, from organellar biology to primary and secondary metabolism.