<?xml version="1.0" encoding="UTF-8"?>
<!DOCTYPE root>
<article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xmlns:ali="http://www.niso.org/schemas/ali/1.0/" article-type="research-article" dtd-version="1.2" xml:lang="en"><front><journal-meta><journal-id journal-id-type="publisher-id">Ecological genetics</journal-id><journal-title-group><journal-title xml:lang="en">Ecological genetics</journal-title><trans-title-group xml:lang="ru"><trans-title>Экологическая генетика</trans-title></trans-title-group></journal-title-group><issn publication-format="print">1811-0932</issn><issn publication-format="electronic">2411-9202</issn><publisher><publisher-name xml:lang="en">Eco-Vector</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="publisher-id">12532</article-id><article-id pub-id-type="doi">10.17816/ecogen1745-14</article-id><article-categories><subj-group subj-group-type="toc-heading" xml:lang="en"><subject>Genetic basis of ecosystems evolution</subject></subj-group><subj-group subj-group-type="toc-heading" xml:lang="ru"><subject>Генетические основы эволюции экосистем</subject></subj-group><subj-group subj-group-type="article-type"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title xml:lang="en">Organization of the endoplasmic reticulum in cells of effective and ineffective pea nodules (Pisum sativum L.)</article-title><trans-title-group xml:lang="ru"><trans-title>Организация эндоплазматического ретикулума в клетках эффективных и неэффективных клубеньков гороха (Pisum sativum L.)</trans-title></trans-title-group></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0003-3505-4298</contrib-id><contrib-id contrib-id-type="spin">9149-5662</contrib-id><name-alternatives><name xml:lang="en"><surname>Tsyganova</surname><given-names>Anna V.</given-names></name><name xml:lang="ru"><surname>Цыганова</surname><given-names>Анна Викторовна</given-names></name></name-alternatives><address><country country="RU">Russian Federation</country></address><bio xml:lang="en"><p>Candidate of Biological Sciences, Leading Scientist of the Laboratory of Molecular and Cellular Biology</p></bio><bio xml:lang="ru"><p>Кандидат биологических наук, ведущий научный сотрудник лаборатории молекулярной и клеточной биологии</p></bio><email>isaakij@mail.ru</email><uri>http://arriam.ru/departments/laboratoriya-molekulyarnoj-i-kletochnoj-biologii/</uri><xref ref-type="aff" rid="aff1"/></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0003-3105-8689</contrib-id><contrib-id contrib-id-type="spin">6532-1332</contrib-id><name-alternatives><name xml:lang="en"><surname>Tsyganov</surname><given-names>Viktor E.</given-names></name><name xml:lang="ru"><surname>Цыганов</surname><given-names>Виктор Евгеньевич</given-names></name></name-alternatives><address><country country="RU">Russian Federation</country></address><bio xml:lang="en"><p>Doctor of Biological Sciences, Head of the Laboratory of Molecular and Cellular Biology, Department of Biotechnology; Senior Scientist of Saint Petersburg Scientific Center RAS</p></bio><bio xml:lang="ru"><p>Доктор биологических наук, заведующий лабораторией молекулярной и клеточной биологии; старший научный сотрудник Санкт-Петербургского научного центра РАН</p></bio><email>tsyganov@arriam.spb.ru</email><uri>http://arriam.ru/departments/laboratoriya-molekulyarnoj-i-kletochnoj-biologii/</uri><xref ref-type="aff" rid="aff1"/><xref ref-type="aff" rid="aff2"/></contrib></contrib-group><aff-alternatives id="aff1"><aff><institution xml:lang="en">All-Russia Research Institute for Agricultural Microbiology</institution></aff><aff><institution xml:lang="ru">ФГБНУ «Всероссийский научно-исследовательский институт сельскохозяйственной микробиологии»</institution></aff></aff-alternatives><aff-alternatives id="aff2"><aff><institution xml:lang="en">Saint Petersburg Scientific Center RAS</institution></aff><aff><institution xml:lang="ru">Санкт-Петербургский научный центр РАН</institution></aff></aff-alternatives><pub-date date-type="preprint" iso-8601-date="2019-09-14" publication-format="electronic"><day>14</day><month>09</month><year>2019</year></pub-date><pub-date date-type="pub" iso-8601-date="2019-12-15" publication-format="electronic"><day>15</day><month>12</month><year>2019</year></pub-date><volume>17</volume><issue>4</issue><issue-title xml:lang="en"/><issue-title xml:lang="ru"/><fpage>5</fpage><lpage>14</lpage><history><date date-type="received" iso-8601-date="2019-05-04"><day>04</day><month>05</month><year>2019</year></date><date date-type="accepted" iso-8601-date="2019-09-14"><day>14</day><month>09</month><year>2019</year></date></history><permissions><copyright-statement xml:lang="en">Copyright ©; 2019, Tsyganova A., Tsyganov V.</copyright-statement><copyright-statement xml:lang="ru">Copyright ©; 2019, Цыганова А.В., Цыганов В.Е.</copyright-statement><copyright-year>2019</copyright-year><copyright-holder xml:lang="en">Tsyganova A., Tsyganov V.</copyright-holder><copyright-holder xml:lang="ru">Цыганова А.В., Цыганов В.Е.</copyright-holder><ali:free_to_read xmlns:ali="http://www.niso.org/schemas/ali/1.0/"/><license><ali:license_ref xmlns:ali="http://www.niso.org/schemas/ali/1.0/">http://creativecommons.org/licenses/by/4.0</ali:license_ref></license></permissions><self-uri xlink:href="https://journals.eco-vector.com/ecolgenet/article/view/12532">https://journals.eco-vector.com/ecolgenet/article/view/12532</self-uri><abstract xml:lang="en"><p><bold>Background. </bold>The endoplasmic reticulum (ER) is the largest membrane-bound organelle, which plays an important role in the functioning of a plant cell and participates in its differentiation.</p> <p><bold>Materials and methods.</bold> Using the methods of transmission electron microscopy, the morphological features and dynamics of structural changes in the ER in symbiotic nodules of pea (<italic>Pisum sativum</italic> L.) wild-type and mutants blocked at different stages of nodule development were studied.</p> <p><bold>Results.</bold> ER developed from a network of individual tubules in meristematic cells, to a developed network of cisterns around the nucleus and plasmalemma, and a network of granular and smooth tubules accompanying infection structures in colonized and infected cells and symbiosomes in infected cells.</p> <p><bold>Conclusions.</bold> A correlation was found between the level of development of the ER network and the degree of bacteroid differentiation.</p></abstract><trans-abstract xml:lang="ru"><p>Эндоплазматический ретикулум (ЭПР) является самой большой, окруженной мембраной органеллой, которая выполняет важную роль в функционировании растительной клетки и участвует в ее дифференцировке. С помощью методов просвечивающей электронной микроскопии были исследованы морфологические особенности и динамика структурных изменений ЭПР в симбиотических клубеньках гороха (<italic>Pisum sativum</italic> L.) дикого типа и мутантов, блокированных на различных стадиях развития клубенька. ЭПР развивался от сети отдельных канальцев в меристематических клетках, к развитой сети цистерн вокруг ядра и плазмалеммы и сети гранулярных и гладких канальцев, сопровождающих инфекционные структуры в колонизированных и инфицированных клетках и симбиосомы в инфицированных клетках. Была выявлена корреляция между уровнем развития сети ЭПР и степенью дифференцировки бактероидов.</p></trans-abstract><kwd-group xml:lang="en"><kwd>legume-rhizobial symbiosis</kwd><kwd>symbiotic nodule</kwd><kwd>ineffective mutants</kwd><kwd>cell organelles</kwd><kwd>Pisum sativum L.</kwd></kwd-group><kwd-group xml:lang="ru"><kwd>бобово-ризобиальный симбиоз</kwd><kwd>симбиотический клубенек</kwd><kwd>неэффективные мутанты</kwd><kwd>клеточные органеллы</kwd><kwd>Pisum sativum L.</kwd></kwd-group><funding-group><award-group><funding-source><institution-wrap><institution xml:lang="en">Russian Science Foundation</institution></institution-wrap><institution-wrap><institution xml:lang="ru">Российский научный фонд</institution></institution-wrap></funding-source><award-id></award-id></award-group><funding-statement xml:lang="en">This work was funded by a grant from the Russian Science Foundation (16-16-10035). This work was carried out using the equipment of the Resource Center “Development of Molecular and Cellular Technologies” of the Federal State Budget Educational Institution of Higher Education at St. Petersburg State University.</funding-statement><funding-statement xml:lang="ru">Данная работа была финансирована грантом Российского научного фонда (16-16-10035). Работа выполнена с использованием оборудования Ресурсного центра «Развитие молекулярных и клеточных технологий» ФГБОУ ВО СПбГУ.</funding-statement></funding-group></article-meta></front><body></body><back><ref-list><ref id="B1"><label>1.</label><mixed-citation>Wada M, Suetsugu N. Plant organelle positioning. Curr Opin Plant Biol. 2004;7(6):626-631. https://doi.org/10.1016/j.pbi.2004.09.005.</mixed-citation></ref><ref id="B2"><label>2.</label><mixed-citation>Agrawal GK, Bourguignon J, Rolland N, et al. Plant organelle proteomics: collaborating for optimal cell function. Mass Spectrom Rev. 2011;30(5):772-853. https://doi.org/10.1002/mas.20301.</mixed-citation></ref><ref id="B3"><label>3.</label><mixed-citation>Shibata Y, Shemesh T, Prinz WA, et al. Mechanisms determining the morphology of the peripheral ER. Cell. 2010;143(5):774-788. https://doi.org/10.1016/j.cell.2010.11.007.</mixed-citation></ref><ref id="B4"><label>4.</label><mixed-citation>Chen J, Doyle C, Qi X, Zheng H. The endoplasmic reticulum: a social network in plant cells. J Integr Plant Biol. 2012;54(11):840-850. https://doi.org/10.1111/j.1744-7909.2012.01176.x.</mixed-citation></ref><ref id="B5"><label>5.</label><mixed-citation>Griffing LR, Lin C, Perico C, et al. Plant ER geometry and dynamics: biophysical and cytoskeletal control during growth and biotic response. Protoplasma. 2017;254(1):43-56. https://doi.org/10.1007/s00709-016-0945-3.</mixed-citation></ref><ref id="B6"><label>6.</label><mixed-citation>Perrine-Walker FM, Kouchi H, Ridge RW. Endoplasmic reticulum-targeted GFP reveals ER remodeling in Mesorhizobium-treated Lotus japonicus root hairs during root hair curling and infection thread formation. Protoplasma. 2014;251(4):817-826. https://doi.org/10.1007/s00709-013-0584-x.</mixed-citation></ref><ref id="B7"><label>7.</label><mixed-citation>Newcomb W. A correlated light and electron microscopic study of symbiotic growth and differentiation in Pisum sativum root nodules. Can J Bot. 1976;54(18):2163-2186. https://doi.org/10.1139/b76-233.</mixed-citation></ref><ref id="B8"><label>8.</label><mixed-citation>Fournier J, Teillet A, Chabaud M, et al. Remodeling of the infection chamber before infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair. Plant Physiol. 2015;167(4):1233-1242. https://doi.org/10.1104/pp.114.253302.</mixed-citation></ref><ref id="B9"><label>9.</label><mixed-citation>MacKenzie CR, Jordan DC. Ultrastructure of root nodules formed by ineffective strains of Rhizobium meliloti. Can J Microbiol. 1974;20(5):755-758. https://doi.org/10.1139/m74-115.</mixed-citation></ref><ref id="B10"><label>10.</label><mixed-citation>Hirsch AM, Bang M, Ausubel FM. Ultrastructural analysis of ineffective alfalfa nodules formed by nif::Tn5 mutants of Rhizobium meliloti. J Bacteriol. 1983;155(1):367-380.</mixed-citation></ref><ref id="B11"><label>11.</label><mixed-citation>Hirsch AM, Smith CA. Effects of Rhizobium meliloti nif and fix mutants on alfalfa root nodule development. J Bacteriol. 1987;169(3):1137-1146. https://doi.org/10.1128/jb.169.3.1137-1146.1987.</mixed-citation></ref><ref id="B12"><label>12.</label><mixed-citation>Gardiol AE, Truchet GL, Dazzo FB. Requirement of succinate dehydrogenase activity for symbiotic bacteroid differentiation of Rhizobium meliloti in alfalfa nodules. Appl Environ Microbiol. 1987;53(8): 1947-1950.</mixed-citation></ref><ref id="B13"><label>13.</label><mixed-citation>Newcomb W, Syono K, Torrey JG. Development of an ineffective pea root nodule: morphogenesis, fine structure, and cytokinin biosynthesis. Can J Bot. 1977;55(14): 1891-1907. https://doi.org/10.1139/b77-217.</mixed-citation></ref><ref id="B14"><label>14.</label><mixed-citation>Wang TL, Wood EA, Brewin NJ. Growth regulators, Rhizobium and nodulation in peas. Planta. 1982;155(4): 350-355. https://doi.org/10.1007/bf00429464.</mixed-citation></ref><ref id="B15"><label>15.</label><mixed-citation>Tsyganov VE, Borisov AY, Rozov SM, Tikhonovich IA. New symbiotic mutants of pea obtained after mutagenesis of laboratory line SGE. Pisum Genetics. 1994;26:36-37.</mixed-citation></ref><ref id="B16"><label>16.</label><mixed-citation>Kosterin OE, Rozov SM. Mapping of the new mutation blb and the problem of integrity of linkage group I. Pisum Genetics. 1993;25:27-31.</mixed-citation></ref><ref id="B17"><label>17.</label><mixed-citation>Tsyganov VE, Morzhina EV, Stefanov SY, et al. The pea (Pisum sativum L.) genes sym33 and sym40 control infection thread formation and root nodule function. Mol Gen Genet. 1998;259(5):491-503. https://doi.org/10.1007/s004380050840.</mixed-citation></ref><ref id="B18"><label>18.</label><mixed-citation>Voroshilova VA, Boesten B, Tsyganov VE, et al. Effect of mutations in Pisum sativum L. genes blocking different stages of nodule development on the expression of late symbiotic genes in Rhizobium leguminosarum bv. viciae. Mol Plant Microbe Interact. 2001;14(4):471-476. https://doi.org/10.1094/MPMI.2001.14.4.471.</mixed-citation></ref><ref id="B19"><label>19.</label><mixed-citation>Serova TA, Tsyganova AV, Tsyganov VE. Early nodule senescence is activated in symbiotic mutants of pea (Pisum sativum L.) forming ineffective nodules blocked at different nodule developmental stages. Protoplasma. 2018;255(5):1443-1459. https://doi.org/10.1007/s00709-018-1246-9.</mixed-citation></ref><ref id="B20"><label>20.</label><mixed-citation>Borisov AY, Rozov SM, Tsyganov VE, et al. Identification of symbiotic genes in pea (Pisum sativum L.) by means of experimental mutagenesis. Soviet Genetics. 1994;30(1):1484-1494.</mixed-citation></ref><ref id="B21"><label>21.</label><mixed-citation>Неманкин Т.А. Анализ генетической системы гороха (Pisum sativum L.), контролирующей развитие арбускулярной микоризы и азотфиксирующего симбиоза: Автореф. дис. … канд. биол. наук. – СПб., 2011. – 19 с. [Nemankin TA. Analiz geneticheskoi sistemy gorokha (Pisum sativum L.), kontrolirujushei razvitie arbuskulyarnoi mikorizy i azotfiksireujushego simbioza. [dissertation abstract] Saint Petersburg; 2011. 19 p. (In Russ.)]. Доступно по: http://earthpapers.net/analiz-geneticheskoy-sistemy-goroha-pisum-sativum-l-kontroliruyuschey-razvitie-arbuskulyarnoy-mikorizy-i-azotfiksiruyusch. Ссылка активна на 14.08.2019.</mixed-citation></ref><ref id="B22"><label>22.</label><mixed-citation>Ovchinnikova E, Journet EP, Chabaud M, et al. IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago spp. Mol Plant Microbe Interact. 2011;24(11):1333-1344. https://doi.org/10.1094/MPMI-01-11-0013.</mixed-citation></ref><ref id="B23"><label>23.</label><mixed-citation>Ivanova KA, Tsyganova AV, Brewin NJ, et al. Induction of host defences by Rhizobium during ineffective nodulation of pea (Pisum sativum L.) carrying symbiotically defective mutations sym40 (PsEFD), sym33 (PsIPD3/PsCYCLOPS) and sym42. Protoplasma. 2015;252(6):505-517. https://doi.org/10.1007/s00709-015-0780-y.</mixed-citation></ref><ref id="B24"><label>24.</label><mixed-citation>Fahraeus G. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol. 1957;16(2):374-381. https://doi.org/10.1099/00221287-16-2-374.</mixed-citation></ref><ref id="B25"><label>25.</label><mixed-citation>Kijne JW, Pluvque K. Ultrastructural study of the endomembrane system in infected cells of pea and soybean root nodules. Physiol Plant Pathol. 1979;14(3):339-345. https://doi.org/10.1016/0048-4059(79)90053-5.</mixed-citation></ref><ref id="B26"><label>26.</label><mixed-citation>Wang D, Griffitts J, Starker C, et al. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science. 2010;327(5969):1126-1129. https://doi.org/10.1126/science.1184096.</mixed-citation></ref><ref id="B27"><label>27.</label><mixed-citation>Kitaeva AB, Demchenko KN, Tikhonovich IA, et al. Comparative analysis of the tubulin cytoskeleton organization in nodules of Medicago truncatula and Pisum sativum: bacterial release and bacteroid positioning correlate with characteristic microtubule rearrangements. New Phytol. 2016;210(1):168-183. https://doi.org/ 10.1111/nph.13792.</mixed-citation></ref><ref id="B28"><label>28.</label><mixed-citation>Newcomb W, Wood SM. Fine structure of nitrogen-fixing leguminous root nodules from the Canadian Arctic. Nord J Bot. 1986;6(5):609-626. https://doi.org/10.1111/j.1756-1051.1986.tb00461.x.</mixed-citation></ref><ref id="B29"><label>29.</label><mixed-citation>Safronova V, Belimov A, Sazanova A, et al. Two broad host range rhizobial strains isolated from relict legumes have various complementary effects on symbiotic parameters of co-inoculated plants. Front Microbiol. 2019;10:514. https://doi.org/10.3389/fmicb. 2019.00514.</mixed-citation></ref></ref-list></back></article>
