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

TitleImpacts of high ATP supply from chloroplasts and mitochondria on the leaf metabolism of Arabidopsis thaliana
Authors
Issue Date2015
PublisherFrontiers Research Foundation. The Journal's web site is located at http://www.frontiersin.org/plant_science/
Citation
Frontiers in Plant Science, 2015, v. 6, p. article no. 922 How to Cite?
AbstractChloroplasts 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.
Persistent Identifierhttp://hdl.handle.net/10722/232836
ISSN
2015 Impact Factor: 4.495
2015 SCImago Journal Rankings: 2.067
PubMed Central ID

 

DC FieldValueLanguage
dc.contributor.authorLiang, C-
dc.contributor.authorZhang, Y-
dc.contributor.authorCheng, S-
dc.contributor.authorOsorio, S-
dc.contributor.authorSun, Y-
dc.contributor.authorFernie, AR-
dc.contributor.authorCheung, CY-
dc.contributor.authorLim, BL-
dc.date.accessioned2016-09-20T05:32:47Z-
dc.date.available2016-09-20T05:32:47Z-
dc.date.issued2015-
dc.identifier.citationFrontiers in Plant Science, 2015, v. 6, p. article no. 922-
dc.identifier.issn1664-462X-
dc.identifier.urihttp://hdl.handle.net/10722/232836-
dc.description.abstractChloroplasts 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.-
dc.languageeng-
dc.publisherFrontiers Research Foundation. The Journal's web site is located at http://www.frontiersin.org/plant_science/-
dc.relation.ispartofFrontiers in Plant Science-
dc.rightsThis Document is Protected by copyright and was first published by Frontiers. All rights reserved. It is reproduced with permission.-
dc.rightsCreative Commons: Attribution 3.0 Hong Kong License-
dc.titleImpacts of high ATP supply from chloroplasts and mitochondria on the leaf metabolism of Arabidopsis thaliana-
dc.typeArticle-
dc.identifier.emailLim, BL: bllim@hkucc.hku.hk-
dc.identifier.authorityLim, BL=rp00744-
dc.description.naturepublished_or_final_version-
dc.identifier.doi10.3389/fpls.2015.00922-
dc.identifier.pmcidPMC4623399-
dc.identifier.hkuros263362-
dc.identifier.volume6-
dc.identifier.spagearticle no. 922-
dc.identifier.epagearticle no. 922-
dc.publisher.placeSwitzerland-

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