A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development
Abstract Background The initial stage of the biosynthesis of steroid hormones in animals occurs in the mitochondria of steroidogenic tissues, where cytochrome P450SCC (CYP11A1) encoded by the CYP11A1 gene catalyzes the conversion of cholesterol into pregnenolone – the general precursor of all the st...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2017-11-01
|
| Series: | BMC Plant Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12870-017-1123-2 |
| _version_ | 1819175707010400256 |
|---|---|
| author | George V. Shpakovski Svetlana G. Spivak Irina N. Berdichevets Olga G. Babak Svetlana V. Kubrak Alexander V. Kilchevsky Andrey V. Aralov Ivan Yu. Slovokhotov Dmitry G. Shpakovski Ekaterina N. Baranova Marat R. Khaliluev Elena K. Shematorova |
| author_facet | George V. Shpakovski Svetlana G. Spivak Irina N. Berdichevets Olga G. Babak Svetlana V. Kubrak Alexander V. Kilchevsky Andrey V. Aralov Ivan Yu. Slovokhotov Dmitry G. Shpakovski Ekaterina N. Baranova Marat R. Khaliluev Elena K. Shematorova |
| author_sort | George V. Shpakovski |
| collection | DOAJ |
| description | Abstract Background The initial stage of the biosynthesis of steroid hormones in animals occurs in the mitochondria of steroidogenic tissues, where cytochrome P450SCC (CYP11A1) encoded by the CYP11A1 gene catalyzes the conversion of cholesterol into pregnenolone – the general precursor of all the steroid hormones, starting with progesterone. This stage is missing in plants where mitochondrial cytochromes P450 (the mito CYP clan) have not been found. Generating transgenic plants with a mitochondrial type P450 from animals would offer an interesting option to verify whether plant mitochondria could serve as another site of P450 monooxygenase reaction for the steroid hormones biosynthesis. Results For a more detailed comparison of steroidogenic systems of Plantae and Animalia, we have created and studied transgenic tobacco and tomato plants efficiently expressing mammalian CYP11A1 cDNA. The detailed phenotypic characterization of plants obtained has shown that through four generations studied, the transgenic tobacco plants have reduced a period of vegetative development (early flowering and maturation of bolls), enlarged biomass and increased productivity (quantity and quality of seeds) as compared to the only empty-vector containing or wild type plants. Moreover, the CYP11A1 transgenic plants show resistance to such fungal pathogen as Botrytis cinerea. Similar valuable phenotypes (the accelerated course of ontogenesis and/or stress resistance) are also visible in two clearly distinct transgenic tomato lines expressing CYP11A1 cDNA: one line (No. 4) has an accelerated rate of vegetative development, while the other (No. 7) has enhanced immunity to abiotic and biotic stresses. The progesterone level in transgenic tobacco and tomato leaves is 3–5 times higher than in the control plants of the wild type. Conclusions For the first time, we could show the compatibility in vivo of even the most specific components of the systems of biosynthesis of steroid hormones in Plantae and Animalia. The hypothesis is proposed and substantiated that the formation of the above-noted special phenotypes of transgenic plants expressing mammalian CYP11A1 cDNA is due to the increased biosynthesis of progesterone that can be considered as a very ancient bioregulator of plant cells and the first real hormone common to plants and animals. |
| first_indexed | 2024-12-22T20:59:08Z |
| format | Article |
| id | doaj.art-eab927c9ce47453da599401a1a263815 |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-12-22T20:59:08Z |
| publishDate | 2017-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-eab927c9ce47453da599401a1a2638152022-12-21T18:12:52ZengBMCBMC Plant Biology1471-22292017-11-0117S111310.1186/s12870-017-1123-2A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and developmentGeorge V. Shpakovski0Svetlana G. Spivak1Irina N. Berdichevets2Olga G. Babak3Svetlana V. Kubrak4Alexander V. Kilchevsky5Andrey V. Aralov6Ivan Yu. Slovokhotov7Dmitry G. Shpakovski8Ekaterina N. Baranova9Marat R. Khaliluev10Elena K. Shematorova11Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesInstitute of Genetics and Cytology, National Academy of Sciences of BelarusInstitute of Genetics and Cytology, National Academy of Sciences of BelarusInstitute of Genetics and Cytology, National Academy of Sciences of BelarusInstitute of Genetics and Cytology, National Academy of Sciences of BelarusInstitute of Genetics and Cytology, National Academy of Sciences of BelarusShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesAll-Russia Research Institute of Agricultural BiotechnologyAll-Russia Research Institute of Agricultural BiotechnologyShemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesAbstract Background The initial stage of the biosynthesis of steroid hormones in animals occurs in the mitochondria of steroidogenic tissues, where cytochrome P450SCC (CYP11A1) encoded by the CYP11A1 gene catalyzes the conversion of cholesterol into pregnenolone – the general precursor of all the steroid hormones, starting with progesterone. This stage is missing in plants where mitochondrial cytochromes P450 (the mito CYP clan) have not been found. Generating transgenic plants with a mitochondrial type P450 from animals would offer an interesting option to verify whether plant mitochondria could serve as another site of P450 monooxygenase reaction for the steroid hormones biosynthesis. Results For a more detailed comparison of steroidogenic systems of Plantae and Animalia, we have created and studied transgenic tobacco and tomato plants efficiently expressing mammalian CYP11A1 cDNA. The detailed phenotypic characterization of plants obtained has shown that through four generations studied, the transgenic tobacco plants have reduced a period of vegetative development (early flowering and maturation of bolls), enlarged biomass and increased productivity (quantity and quality of seeds) as compared to the only empty-vector containing or wild type plants. Moreover, the CYP11A1 transgenic plants show resistance to such fungal pathogen as Botrytis cinerea. Similar valuable phenotypes (the accelerated course of ontogenesis and/or stress resistance) are also visible in two clearly distinct transgenic tomato lines expressing CYP11A1 cDNA: one line (No. 4) has an accelerated rate of vegetative development, while the other (No. 7) has enhanced immunity to abiotic and biotic stresses. The progesterone level in transgenic tobacco and tomato leaves is 3–5 times higher than in the control plants of the wild type. Conclusions For the first time, we could show the compatibility in vivo of even the most specific components of the systems of biosynthesis of steroid hormones in Plantae and Animalia. The hypothesis is proposed and substantiated that the formation of the above-noted special phenotypes of transgenic plants expressing mammalian CYP11A1 cDNA is due to the increased biosynthesis of progesterone that can be considered as a very ancient bioregulator of plant cells and the first real hormone common to plants and animals.http://link.springer.com/article/10.1186/s12870-017-1123-2Transgenic plantsCytochrome P450scc (CYP11A1)TobaccoBotrytis cinereaProgesteroneMitochondria |
| spellingShingle | George V. Shpakovski Svetlana G. Spivak Irina N. Berdichevets Olga G. Babak Svetlana V. Kubrak Alexander V. Kilchevsky Andrey V. Aralov Ivan Yu. Slovokhotov Dmitry G. Shpakovski Ekaterina N. Baranova Marat R. Khaliluev Elena K. Shematorova A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development BMC Plant Biology Transgenic plants Cytochrome P450scc (CYP11A1) Tobacco Botrytis cinerea Progesterone Mitochondria |
| title | A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development |
| title_full | A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development |
| title_fullStr | A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development |
| title_full_unstemmed | A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development |
| title_short | A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development |
| title_sort | key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development |
| topic | Transgenic plants Cytochrome P450scc (CYP11A1) Tobacco Botrytis cinerea Progesterone Mitochondria |
| url | http://link.springer.com/article/10.1186/s12870-017-1123-2 |
| work_keys_str_mv | AT georgevshpakovski akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT svetlanagspivak akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT irinanberdichevets akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT olgagbabak akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT svetlanavkubrak akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT alexandervkilchevsky akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT andreyvaralov akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT ivanyuslovokhotov akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT dmitrygshpakovski akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT ekaterinanbaranova akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT maratrkhaliluev akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT elenakshematorova akeyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT georgevshpakovski keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT svetlanagspivak keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT irinanberdichevets keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT olgagbabak keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT svetlanavkubrak keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT alexandervkilchevsky keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT andreyvaralov keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT ivanyuslovokhotov keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT dmitrygshpakovski keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT ekaterinanbaranova keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT maratrkhaliluev keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment AT elenakshematorova keyenzymeofanimalsteroidogenesiscanfunctioninplantsenhancingtheirimmunityandacceleratingtheprocessesofgrowthanddevelopment |