Specificity of DNA import into isolated mitochondria from plants and mammals

Aim. Investigation of different features of DNA import into plant and human mitochondria, for a better understanding of mitochondrial genetics and generation of biotechnological tools. Methods. DNA up-take experiments with isolated plant mitochondria, using as substrates various sequences associated...

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Дата:	2014
Автори:	Koulintchenko, M.V., Ibrahim, N., Klimenko, E.S., Konstantinov, Yu.M., Weber-Lotfi, F., Dietrich, A.
Формат:	Стаття
Мова:	English
Опубліковано:	Інститут молекулярної біології і генетики НАН України 2014
Назва видання:	Вiopolymers and Cell
Теми:	Short Communications
Онлайн доступ:	http://dspace.nbuv.gov.ua/handle/123456789/153719
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Назва журналу:	Digital Library of Periodicals of National Academy of Sciences of Ukraine
Цитувати:	Specificity of DNA import into isolated mitochondria from plants and mammals / M.V. Koulintchenko, N. Ibrahim, E.S. Klimenko, Yu.M. Konstantinov, F. Weber-Lotfi, A. Dietrich // Вiopolymers and Cell. — 2014. — Т. 30, № 1. — С. 68-70. — Бібліогр.: 8 назв. — англ.

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Digital Library of Periodicals of National Academy of Sciences of Ukraine

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spelling	irk-123456789-1537192019-06-15T01:31:09Z Specificity of DNA import into isolated mitochondria from plants and mammals Koulintchenko, M.V. Ibrahim, N. Klimenko, E.S. Konstantinov, Yu.M. Weber-Lotfi, F. Dietrich, A. Short Communications Aim. Investigation of different features of DNA import into plant and human mitochondria, for a better understanding of mitochondrial genetics and generation of biotechnological tools. Methods. DNA up-take experiments with isolated plant mitochondria, using as substrates various sequences associated or not with the specific terminal inverted repeats (TIRs) present at each end of the plant mitochondrial linear plasmids. Results. It was established that the DNA import efficiency has a non-linear dependence on DNA size. It was shown that import into plant mitochondria of DNA molecules of «medium» sizes, i. e. between 4 and 7 kb, barely has any sequence specificity: neither TIRs from the 11.6 kb Brassica plasmid, nor TIRs from the Zea mays S-plasmids influenced DNA import into Solanum tuberosum mitochondria. Conclusions. The data obtained support the hypothesis about species-specific import mechanism operating under the mitochondrial linear plasmids transfer into plant mitochondria. Мета. Вивчення відмінностей в імпорті ДНК у мітохондрії рослин і людини для кращого розуміння генетики мітохондрій та розробки біотехнологічних підходів до її дослідження. Методи. Експерименти з імпорту ДНК в ізольоовані мітохондрії рослин з використанням як субстратів послідовностей, які містять або не містять специфічних кінцевих інвертованих повторів (КІП), характерних для лінійних плазмід рослинних мітохондрій. Результати. Встановлено, що ефективність імпорту ДНК у мітохондрії нелінійно залежить від розміру ДНК. Показано, що імпорт у рослинні мітохондрії молекул ДНК «середніх» розімрів (4–7 тис. п. н.) має незначну структурну специфічність: ані КІП плазміди 11,6 тис. п. н. з Brassica napus, ані КІП S-плазмід із Zea mays не чинять впливу на імпорт ДНК у мітохондрії Solanum tuberosum. Висновки. Отримані дані свідчать на користь гіпотези існування видоспецифічного механізму перенесення мітохондріальних лінійних плазмід у рослинні мітохондрії. Цель. Изучение различных свойств импорта ДНК в митохондрии растений и человека для лучшего понимания генетики митохондрий и разработки биотехнологических подходов для ее исследования. Методы. Эксперименты по импорту ДНК в изолированные митохондрии растений с использованием в качестве субстратов последовательностей, содержащих или не содержащих специфических концевых инвертированных повторов (КИП), характерных для линейных плазмид растительных митохондрий. Результаты. Установлено, что эффективность импорта ДНК в митохондрии имеет нелинейную зависимость от размера ДНК. Показано, что импорт в растительные митохондрии молекул ДНК «средних» размеров (4–7 тыс. п. н.) имеет незначительную структурную специфичность: ни КИП плазмиды 11,6 тыс. п. н. из Brassica napus, ни КИП S-плазмиды из Zea mays не оказывают влияния на импорт ДНК в митохондрии Solanum tuberosum. Выводы. Полученные данные свидетельствуют в пользу гипотезы существования видоспецифического механизма переноса митохондриальных линейных плазмид в растительные митохондрии. 2014 Article Specificity of DNA import into isolated mitochondria from plants and mammals / M.V. Koulintchenko, N. Ibrahim, E.S. Klimenko, Yu.M. Konstantinov, F. Weber-Lotfi, A. Dietrich // Вiopolymers and Cell. — 2014. — Т. 30, № 1. — С. 68-70. — Бібліогр.: 8 назв. — англ. 0233-7657 DOI: http://dx.doi.org/10.7124/bc.000880 http://dspace.nbuv.gov.ua/handle/123456789/153719 577.113 + 123.5 en Вiopolymers and Cell Інститут молекулярної біології і генетики НАН України
institution	Digital Library of Periodicals of National Academy of Sciences of Ukraine
collection	DSpace DC
language	English
topic	Short Communications Short Communications
spellingShingle	Short Communications Short Communications Koulintchenko, M.V. Ibrahim, N. Klimenko, E.S. Konstantinov, Yu.M. Weber-Lotfi, F. Dietrich, A. Specificity of DNA import into isolated mitochondria from plants and mammals Вiopolymers and Cell
description	Aim. Investigation of different features of DNA import into plant and human mitochondria, for a better understanding of mitochondrial genetics and generation of biotechnological tools. Methods. DNA up-take experiments with isolated plant mitochondria, using as substrates various sequences associated or not with the specific terminal inverted repeats (TIRs) present at each end of the plant mitochondrial linear plasmids. Results. It was established that the DNA import efficiency has a non-linear dependence on DNA size. It was shown that import into plant mitochondria of DNA molecules of «medium» sizes, i. e. between 4 and 7 kb, barely has any sequence specificity: neither TIRs from the 11.6 kb Brassica plasmid, nor TIRs from the Zea mays S-plasmids influenced DNA import into Solanum tuberosum mitochondria. Conclusions. The data obtained support the hypothesis about species-specific import mechanism operating under the mitochondrial linear plasmids transfer into plant mitochondria.
format	Article
author	Koulintchenko, M.V. Ibrahim, N. Klimenko, E.S. Konstantinov, Yu.M. Weber-Lotfi, F. Dietrich, A.
author_facet	Koulintchenko, M.V. Ibrahim, N. Klimenko, E.S. Konstantinov, Yu.M. Weber-Lotfi, F. Dietrich, A.
author_sort	Koulintchenko, M.V.
title	Specificity of DNA import into isolated mitochondria from plants and mammals
title_short	Specificity of DNA import into isolated mitochondria from plants and mammals
title_full	Specificity of DNA import into isolated mitochondria from plants and mammals
title_fullStr	Specificity of DNA import into isolated mitochondria from plants and mammals
title_full_unstemmed	Specificity of DNA import into isolated mitochondria from plants and mammals
title_sort	specificity of dna import into isolated mitochondria from plants and mammals
publisher	Інститут молекулярної біології і генетики НАН України
publishDate	2014
topic_facet	Short Communications
url	http://dspace.nbuv.gov.ua/handle/123456789/153719
citation_txt	Specificity of DNA import into isolated mitochondria from plants and mammals / M.V. Koulintchenko, N. Ibrahim, E.S. Klimenko, Yu.M. Konstantinov, F. Weber-Lotfi, A. Dietrich // Вiopolymers and Cell. — 2014. — Т. 30, № 1. — С. 68-70. — Бібліогр.: 8 назв. — англ.
series	Вiopolymers and Cell
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fulltext	SHORT COMMUNICATIONS UDC 577.113 + 123.5 Specificity of DNA import into isolated mitochondria from plants and mammals M. V. Koulintchenko1, 2, N. Ibrahim2, E. S. Klimenko1, Yu. M. Konstantinov1, F. Weber-Lotfi2, A. Dietrich2 1Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch of the Russian Academy of Sciences, 132, Lermontova Str., Irkutsk, Russian Federation, 664033 2CNRS Institute of Plant Molecular Biology, University of Strasbourg, 12 ,General Zimmer Str., Strasbourg, France, 67084 mk100171@yahoo.com Aim. Investigation of different features of DNA import into plant and human mitochondria, for a better under- standing of mitochondrial genetics and generation of biotechnological tools. Methods. DNA up-take experi- ments with isolated plant mitochondria, using as substrates various sequences associated or not with the specific terminal inverted repeats (TIRs) present at each end of the plant mitochondrial linear plasmids. Results. It was established that the DNA import efficiency has a non-linear dependence on DNA size. It was shown that import in- to plant mitochondria of DNA molecules of «medium» sizes, i. e. between 4 and 7 kb, barely has any sequence spe- cificity: neither TIRs from the 11.6 kb Brassica plasmid, nor TIRs from the Zea mays S-plasmids influenced DNA import into Solanum tuberosum mitochondria. Conclusions. The data obtained support the hypothesis about species-specific import mechanism operating under the mitochondrial linear plasmids transfer into plant mi- tochondria. Keywords: mitochondrial DNA import, plant mitochondrial linear plasmids, mitochondrial genome. Introduction. It is well known that horizontal gene trans- fer (HGT) is one of the substantial factors, mainly in the evolution of bacteria. Recent studies indicate that plant mi- tochondria are unusually active in HGT, relative to all other organelles of multicellular eukaryotes [1]. The dis- tinctive feature of plant mitochondria is the size of their ge- nomes, which are much larger than those of other eukaryo- tes. Moreover, in addition to a large and complex main mi- tochondrial genome, plant mitochondria contain small circular and linear DNAs regarded as extrachromosomal replicons or plasmids [2]. The linear mitochondrial plas- mids are present in many fungi and in some plant species, but they seem to be absent in most animal cells. They usually have in common an «invertron» structure that is characterized by the presence of terminal inverted repeats (TIRs) and proteins covalently attached to their 5' termini [3]. The Brassica 11.6 kb plasmid, one of the linear mi- tochondrial plasmids in plants, shows a non-maternal in- heritance, in contrast to mitochondrial genomes [4]. The origin of these plasmids is unknown, but indirect eviden- ce indicates the possibility of horizontal transfer from fun- gal mitochondria. These pecularities suggest that plant mi- tochondria might possess a mechanism of natural compe- tence to take up foreign DNA, resembling that of the pro- cess in the bacterial cells [5]. The aim of the project is to study different features of DNA import into plant mito- chondria and into human mitochondria, for a better under- standing of mitochondrial genetics and generation of bio- technological tools. Materials and methods. We developed DNA up- take experiments with isolated plant mitochondria, using as substrates various sequences associated or not with the specific TIRs present at each end of the 11.6 kb linear plasmid from rapeseed (Brassica napus L.) [4]. 68 ISSN 0233–7657. Biopolymers and Cell. 2014. vol. 30. N 1. P. 68–70 doi: http://dx.doi.org/10.7124/bc.000880 Ó Institute of Molecular Biology and Genetics, NAS of Ukraine, 2014 Further substrates for mitochondrial import were the S1 and S2 linear plasmids from maize (Zea mays) [6, 7]. Organization of these plasmids is shown in Fig. 1. Iso- lation of mitochondria and uptake assays were perfor- med as described earlier [5, 8]. Results and discussion. It has been shown previous- ly [8] that (i) the efficiency of the import of large DNA molecules into plant mitochondria depends on the sequen- ce and (ii) the specificity of DNA import can be mediated by the presence of certain elements in their sequence, es- pecially TIRs at the ends of the molecules. Conversely, the efficiency of DNA import into mammalian mitochon- dria seemed to depend neither on the DNA sequence, nor on its size. Until now the role of the sequence and struc- ture (in particular of the TIRs, which are different in linear plasmids from mitochondria of various plant species) in both mitochondrial DNA translocation and mitochondrial genetic processes (autonomous replication, integration in- to the genome, etc.) is unknown. We addressed the possible universal role of the TIRs of mitochondrial linear plasmids from Z. mays and Bras- sica in the mechanism of DNA import into plant mito- chondria. Using a vector containing the TIRs (327 bp) from the 11.6 kb B. napus plasmid [4], we obtained se- veral DNA constructs and tested the importance of the size and DNA structure in the efficiency of the import in- 69 SPECIFICITY OF DNA IMPORT INTO ISOLATED MITOCHONDRIA FROM PLANTS AND MAMMALS 11.6 kb Brassica napus orf5 S1, 6.4 kb Zea mays dpo TIR orf2orf4 homology S2, 5.4 kb Z. mays orf6 orf3 orf1 TIR rpo TIR homology TIR TIR TIR orf2 orf1 orf2 orf3 orf4 rpodpo Fig. 1. Organization of the mitochond- rial linear plasmids used in the stu- dies: Brassica napus 11.6 kb and Zea mays 6.4 kb S1 and 5.4 kb S2 plas- mids; dpo: DNA polymerase, rpo: RNA polymerase; the region of per- fect sequence homology between the S1 and S2 plasmids is designated by pink color TIR 4.2/4.7 5.9/6.6 7.0/7.7kb S2 pl S1 pl 5.0/5.4 6.0/6.4 Solanum tuberosum mitochondria B. rapa mtDNA Import assays DNA (+TIR) DNA (!TIR) A B DNA (+TIR) DNA (!TIR) DNA substrates for import & + ! + & + ! + & + Sequences from Brassica rapa mitochondrial DNA multiclonal site 7-kb 6-kb 4-kb TIR TIR TIR TIR TIR 11.6 kb TIR 11.6 kb S1 or S2 mtDNA B. rapa Fig. 2. Import of «medium» size DNA into Solanum tuberosum mitochondria does not depend on the presence of TIRs from mitochondrial linear plasmids: A – different sequences from the Brasica rapa mitochondrial genome were cloned between the TIRs from the B. napus 11.6 kb plasmid (the Zea mays S1 and S2 plasmids were cloned in parallel; all sequences were subsequently amplified by PCR with or without the TIRs); B – the amplified PCR products were radioactively labeled and used as substrates for import into isolated S. tuberosum mitochondria. Nucleic acids sub- sequently recovered in the mitochondrial fraction were analyzed by agarose gel electrophoresis, Southern blotting and autoradiography to plant mitochondria (Fig. 2, A). The DNA sequences of Z. mays linear plasmids, S1 [6] and S2 [7] with or wi- thout TIRS (208 bp) were also cloned and used as subst- rates for import assays (Fig. 2, B). Using radioactively labeled DNA subst rates and the in organello potato (S. tuberosum) mitochondrial import system [5], it was es- tablished that the import efficiency has a non-linear de- pendence on DNA size: DNA fragments of 6–7 kb in si- ze can be imported into S. tuberosum mitochondria mo- re effectively than molecules with a 4 kb size. It was also shown (Fig. 2) that import into plant mitochondria of DNA molecules of «medium» sizes, i. e. between 4 and 7 kb, barely has any sequence specificity: neither TIRs from the 11.6 kb Brassica plasmid, nor TIRs from the Z. mays S-plasmids influenced DNA import into S. tu- berosum mitochondria. Conversely, the role of the TIRs from the 11.6 kb linear plasmid in the import of large DNA molecules was established earlier for the B. rapa mitochondria [8]. Conclusions. The data obtained support a species- specific import mechanism of the mitochondrial linear plasmids, and more generally of large DNA molecules, into plant mitochondria, which needs further investi- gation. Funding. The work was supported by the Russian Fund for Basic Research (12-04-01400 and 12-04-01027) and the French Ministry for Research (Investis sements d’Avenir/Laboratoire d’Excellence MitoCross). The equipment of the Baikal Analytical Center (BAC) at the Presidium of ISC SB RAS was used for this work. Ñïå öèô³êà ³ìïîð òó ÄÍÊ â ³çîëü î âà íèõ ì³òî õîíäð³ÿõ ç ðîñ ëèí ³ ññàâö³â Ì. Â. Êóë³í÷åí êî, Í. ²áðàõ³ì, Ê. Ñ. Êë³ìåí êî, Þ. Ì. Êîí ñòàí òè íîâ, Ô. Âå áåð-Ëîòô³, À. Äèò ðèø Ðå çþ ìå Ìåòà. Âèâ ÷åí íÿ â³äì³ííîñ òåé â ³ìïîðò³ ÄÍÊ ó ì³òî õîíäð³¿ ðîñ - ëèí ³ ëþäèíè äëÿ êðà ùî ãî ðî çóì³ííÿ ãå íå òè êè ì³òî õîíäð³é òà ðîç- ðîáêè á³îò åõ íî ëîã³÷íèõ ï³äõîä³â äî ¿¿ äîñë³äæåí íÿ. Ìå òî äè. Åêñ- ïå ðè ìåí òè ç ³ìïîð òó ÄÍÊ â ³çîëü î î âàí³ ì³òî õîíäð³¿ ðîñ ëèí ç âè - êî ðèñ òàí íÿì ÿê ñóá ñòðàò³â ïîñë³äîâ íîñ òåé, ÿê³ ì³ñòÿòü àáî íå ì³ñòÿòü ñïå öèô³÷íèõ ê³íöå âèõ ³íâåð òî âà íèõ ïî âòîð³â (Ê²Ï), õà - ðàê òåð íèõ äëÿ ë³í³éíèõ ïëàçì³ä ðîñ ëèí íèõ ì³òî õîíäð³é. Ðå çóëü - òà òè. Âñòà íîâ ëå íî, ùî åôåê òèâí³ñòü ³ìïîð òó ÄÍÊ ó ì³òî õîíä- ð³¿ íåë³í³éíî çà ëå æèòü â³ä ðîçì³ðó ÄÍÊ. Ïî êà çà íî, ùî ³ìïîðò ó ðîñëèíí³ ì³òî õîíäð³¿ ìî ëå êóë ÄÍÊ «ñå ðåäí³õ» ðîç³ìð³â (4–7 òèñ. ï. í.) ìàº íå çíà÷ íó ñòðóê òóð íó ñïå öèô³÷í³ñòü: àí³ Ê²Ï ïëàçì³äè 11,6 òèñ. ï. í. ç Brassica napus, àí³ Ê²Ï S-ïëàçì³ä ³ç Zea mays íå ÷è- íÿòü âïëè âó íà ³ìïîðò ÄÍÊ ó ì³òî õîíäð³¿ Solanum tuberosum. Âèñ- íîâ êè. Îòðè ìàí³ äàí³ ñâ³ä÷àòü íà êî ðèñòü ã³ïî òå çè ³ñíó âàí íÿ âè- äîñïå öèô³÷íî ãî ìå õàí³çìó ïå ðåíå ñåí íÿ ì³òî õîíäð³àëü íèõ ë³í³éíèõ ïëàçì³ä ó ðîñ ëèíí³ ì³òî õîíäð³¿. Êëþ ÷îâ³ ñëî âà: ³ìïîðò ÄÍÊ ó ì³òî õîíäð³¿, ì³òî õîíäð³àëüí³ ë³í³éí³ ïëàçì³äè ðîñ ëèí, ì³òî õîíäð³àëüíèé ãå íîì. Ñïå öè ôè êà èì ïîð òà ÄÍÊ â èçî ëè ðî âàí íûõ ìè òî õîí äðè ÿõ ðàñ òå íèé è ìëå êî ïè òà þ ùèõ Ì. Â. Êó ëèí ÷åí êî, Í. Èáðà ãèì, Å. Ñ. Êëè ìåí êî, Þ. Ì. Êîí ñòàí òè íîâ, Ô. Âå áåð-Ëîò ôè, À. Äèò ðèø Ðå çþ ìå Öåëü. Èçó ÷å íèå ðàç ëè÷ íûõ ñâîéñòâ èì ïîð òà ÄÍÊ â ìè òî õîí äðèè ðàñ òå íèé è ÷å ëî âå êà äëÿ ëó÷ øå ãî ïî íè ìà íèÿ ãå íå òè êè ìè òî õîíä- ðèé è ðàç ðà áîò êè áè î òåõ íî ëî ãè ÷åñ êèõ ïîä õî äîâ äëÿ åå èñ ñëå äî âà - íèÿ. Ìå òî äû. Ýêñïå ðè ìåí òû ïî èì ïîð òó ÄÍÊ â èçî ëè ðî âàí íûå ìè òî õîí äðèè ðàñ òå íèé ñ èñ ïîëü çî âà íè åì â êà ÷åñ òâå ñóá ñòðà òîâ ïîñëå äî âà òåëü íîñ òåé, ñî äåð æà ùèõ èëè íå ñî äåð æà ùèõ ñïå öèôè- ÷åñ êèõ êîí öå âûõ èí âåð òè ðî âàí íûõ ïî âòî ðîâ (ÊÈÏ), õà ðàê òåð íûõ äëÿ ëè íåé íûõ ïëàç ìèä ðàñ òè òåëü íûõ ìè òî õîí äðèé. Ðå çóëü òà òû. Óñòà íîâ ëå íî, ÷òî ýô ôåê òèâ íîñòü èì ïîð òà ÄÍÊ â ìè òî õîí äðèè èìå åò íå ëè íåé íóþ çà âè ñè ìîñòü îò ðàç ìå ðà ÄÍÊ. Ïî êà çà íî, ÷òî èì ïîðò â ðàñ òè òåëü íûå ìè òî õîí äðèè ìî ëå êóë ÄÍÊ «ñðåä íèõ» ðàç ìå ðîâ (4–7 òûñ. ï. í.) èìå åò íå çíà ÷è òåëü íóþ ñòðóê òóð íóþ ñïå öè ôè÷ íîñòü: íè ÊÈÏ ïëàç ìè äû 11,6 òûñ. ï. í. èç Brassica na- pus, íè ÊÈÏ S-ïëàç ìè äû èç Zea mays íå îêà çû âà þò âëè ÿ íèÿ íà èì - ïîðò ÄÍÊ â ìè òî õîí äðèè Solanum tuberosum. Âû âî äû. Ïî ëó ÷åí - íûå äàí íûå ñâè äå ò åëüñòâó þò â ïî ëüçó ãè ïî òå çû ñó ùåñ òâî âà íèÿ âè äîñ ïå öè ôè ÷åñ êî ãî ìå õà íèç ìà ïå ðå íî ñà ìè òî õîí äðè àëü íûõ ëè - íåé íûõ ïëàç ìèä â ðàñ òè òåëü íûå ìè òî õîí äðèè. Êëþ ÷å âûå ñëî âà: èì ïîðò ÄÍÊ â ìè òî õîí äðèè, ìè òî õîí äðè- àëü íûå ëè íåé íûå ïëàç ìè äû ðàñ òå íèé, ìè òî õîí äðè àëü íûé ãå íîì. REFERENCES. 1. Mower JP, Jain K, Hepburn NJ. The role of horizontal transfer in shaping the plant mitochondrial genome. Adv Bot Res. 2012; 63:41–69. 2. Handa H. Linear plasmids in plant mitochondria: peaceful coexistence or malicious invasions? Mitochondrion. 2008; 8 (1):15–25. 3. Sakaguchi K. Invertrons, a class of structurally and functionally related genetic elements that includes linear DNA plasmids, transposable elements, and genomes of adeno-type viruses. Microbiol Rev. 1990; 54(1):66–74. 4. Handa H, Itani K, Sato H. Structural features and expression analysis of a linear mitochondrial plasmid in rapeseed (Brassica napus L.). Mol Genet Genomics. 2002; 267(6):797–805. 5. Koulintchenko M, Konstantinov Y, Dietrich A. Plant mitochond- ria actively import DNA via the permeability transition pore complex. EMBO J. 2003; 22(6):1245–1254. 6. Paillard M, Sederoff RR, Levings CS. Nucleotide sequence of the S-1 mitochondrial DNA from the S cytoplasm of maize. EMBO J. 1985; 4(5):1125–8. 7. Levings CS, Sederoff RR. Nucleotide sequence of the S-2 mi- tochondrial DNA from the S cytoplasm of maize. Proc Natl Acad Sci USA. 1983; 80(13):4055–9. 8. Ibrahim N, Handa H, Cosset A, Koulintchenko M, Konstantinov Y, Lightowlers RN, Dietrich A, Weber-Lotfi F. DNA delivery to mitochondria: sequence specifity and energy enhancement. Pharm Res. 2011; 28(11):2871–82. Recieved 01.09.13 70 KOULINTCHENKO M. V. ET AL.

Specificity of DNA import into isolated mitochondria from plants and mammals

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