References

vavilov

Вавиловский журнал генетики и селекции

Vavilov Journal of Genetics and Breeding

2500-3259

Institute of Cytology and Genetics of Siberian Branch of the RAS

10.18699/VJ19.509

vavilov-2131

Research Article

ГЕНЕТИЧЕСКИЕ РЕСУРСЫ И БИОКОЛЛЕКЦИИ

PLANT GENETICS

Факторы транскрипции MhyFIL1 и MhyFIL3 (Monotropa hypopitys) определяют асимметричное развитие боковых органов надземной части растения

Transcription factors MhyFIL1 and MhyFIL3 (Monotropa hypopitys) determine the asymmetric development of above-ground lateral organs in plants

https://orcid.org/0000-0003-4692-3727

Щенникова

А. В.

Shchennikova

A. V.

shchennikova@yandex.ru

https://orcid.org/0000-0001-9815-9578

Камионская

А. М.

Kamionskaya

A. M.

https://orcid.org/0000-0003-4175-3175

Нежданова

А. В.

Nezhdanova

A. V.

https://orcid.org/0000-0001-8207-3622

Гаврилова

К. С.

Gavrilova

K. S.

https://orcid.org/0000-0003-3668-7601

Филюшин

М. А.

Filyushin

M. A.

https://orcid.org/0000-0002-6091-0765

Кочиева

Е. З.

Kochieva

E. Z.

https://orcid.org/0000-0001-6642-4410

Скрябин

К. Г.

Skryabin

K. G.

Федеральный исследовательский центр «Фундаментальные основы биотехнологии» Российской академии наук, Институт биоинженерииРоссияFederal Research Centre “Fundamentals of Biotechnology”, RAS, Institute of BioengineeringRussian Federation

2019

07072019

234405411

2019

Щенникова А.В., Камионская А.М., Нежданова А.В., Гаврилова К.С., Филюшин М.А., Кочиева Е.З., Скрябин К.Г.

Shchennikova A.V., Kamionskaya A.M., Nezhdanova A.V., Gavrilova K.S., Filyushin M.A., Kochieva E.Z., Skryabin K.G.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://vavilov.elpub.ru/jour/article/view/2131

Считается, что полный микогетеротроф, подъельник Monotropa hypopitys, адаптивно эволюционировал из фотосинтезирующего микоризного предшественника, потеряв при этом аппарат фотосинтеза и вегетативные органы (стебель и листья). Надземная часть растения представляет собой цветонос со стерильными прицветниками и соцветием с каноническим для высших растений типом цветка. У растений происхождение плоского листа и других листоподобных латеральных органов связывают с эволюцией генов YABBY, которые, в зависимости от профиля экспрессии, разделяются на «вегетативные» и эволюционно более поздние «репродуктивные» гены. Изучение «вегетативных» генов YABBY подъельника позволит выяснить, сохранились ли их функции (определение идентичности клеток абаксиальной поверхности латеральных органов) у растения без листьев. В настоящем исследовании проведен структурно-филогенетический анализ генов подъельника MhyFIL1 и MhyFIL3, охарактеризованы основные консервативные домены и мотивы кодируемых ими белков и подтверждена принадлежность генов к «вегетативной» кладе YABBY3/FIL. Проведена оценка влияния гетерологичной эктопической экспрессии генов MhyFIL1 и MhyFIL3 на фенотип трансгенных растений табака Nicotiana tabacum. Показано, что оба типа растений, 35S::MhyFIL1 и 35S::MhyFIL3, формируют листья более узкие, чем в норме, и скрученные за счет измененной идентичности клеток адаксиальной поверхности. Выявлены также изменения архитектуры надземной части и корневой системы растений, включая аберрантный филлотаксис и подавление развития апикальных меристем побега и корня. Часть растений 35S::MhyFIL1 и 35S::MhyFIL3 погибала еще на стадии формирования первых листьев, часть не цвела, остальные имели сильно увеличенный период вегетации и при цветении формировали меньше цветков, чем в норме. Цветки не имели видимых отличий от контроля, за исключением ломких цветоножек. Таким образом, отсутствие изменений в строении цветка подъельника в сравнении с автотрофными видами, а также особенности влияния гетерологичной экспрессии генов MhyFIL1/3 на развитие растений табака говорят о сохранении генами подъельника MhyFIL1/3 функции «вегетативных» генов YABBY. При этом у M. hypopitys активность YABBY-факторов транскрипции группы FIL напрямую не связана с потерей способности формировать листья при эволюционном переходе подъельника от аутотрофного питания к гетеротрофии.

It is believed that the complete mycoheterotroph pinesap Monotropa hypopitys adaptively evolved from a photosynthetic mycorrhizal ancestor, which had lost its photosynthetic apparatus and vegetative organs (stem and leaves). The aerial part of the plant is a reproductive axis with sterile bracts and inflorescence with a flower type canonical for higher plants. The origin of leaves and leaf-like lateral organs is associated, among other factors, with the evolution of the YABBY genes, which are divided into“vegetative” and evolutionarily recent“reproductive” genes, with regard to their expression profiles. The study of the vegetative YABBY genes in pinesap will determine whether their functions (identification of cell identity on the abaxial surface of the lateral organs) are preserved in the leafless plant. In this study, the structural and phylogenetic analysis of the pinesap vegetative genes MhyFIL1 and MhyFIL3 is performed, the main conserved domains and motifs of the encoded proteins are characterized, and it is confirmed that the genes belong to the vegetative clade YABBY3/FIL. The effect of heterologous ectopic expression of the MhyFIL1 and MhyFIL3 genes on the phenotype of transgenic tobacco Nicotiana tabacum is evaluated. The leaves formed by both types of plants, 35S::MhyFIL1 and 35S::MhyFIL3, were narrower than in control plants and were twisted due to the changed identity of adaxial surface cells. Also, changes in the architecture of the aerial part and the root system of transgenic plants, including aberrant phyllotaxis and arrest of the shoot and root apical meristem development, were noted. Some of the 35S::MhyFIL1 and 35S::MhyFIL3 plants died as early as the stage of the formation of the first leaves, others did not bloom, and still others had a greatly prolonged vegetation period and formed fewer flowers than normal ones. The flowers had no visible differences from the control except for fragile pedicles. Thus, the absence of structural changes from the M. hypopitys flower in comparison to autotrophic species and the effect of MhyFIL1/3 heterologous expression on the development of tobacco plants indicate the preservation of the functions of the vegetative YABBY genes by the MhyFIL1/3 genes in pinesap. Moreover, the activity of YABBY transcription factors of the FIL clade in M. hypopitys is not directly related to the loss of the ability of pinesap to form leaves during the evolutionary transition from autotrophic nutrition to heterotrophy.

Monotropa hypopitysмикогетеротрофгетерологичная экспрессия генаабаксиальноадаксиальная асимметриятранскрипционные факторы YABBY«вегетативные» YABBYFILAMENTOUS FLOWER

Monotropa hypopitysmycoheterotrophheterologous gene expressionabaxial-adaxial asymmetrytranscription factorsYABBY“vegetative”YABBYsFILAMENTOUS FLOWER

This work was financially supported by the Russian Science Foundation, project No. 14-24-00175, and the Ministry of Science and Higher Education of the Russian Federation (A.V. Nezhdanova, K.S. Gavrilova), and was performed using the experimental climate control facility in the Institute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences.

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The authors declare that there are no conflicts of interest present.