Low temperature-induced chloroplast relocation in mesophyll cells of Pinus sylvestris (Pinaceae): SBF SEM 3D reconstruction

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Abstract

Evergreen species of temperate zone acclimate to seasonal climates by reorganizations of mesophyll cell structure including chloroplast movement as a photoprotective reaction. However the exact factor inducing structural changes is still unexplored. To reveal the specific pattern of chloroplast arrangement during the annual cycle and the effect of temperature on their movement, the mesophyll cell structure in Pinus sylvestris grown out- and indoors was studied. The serial block-face scanning electron microscopy (SBF SEM) was used for the 3D imaging of mesophyll cells to show the spatial position and shape modification of chloroplasts. It has been shown that during the growing season, chloroplasts have a well-developed thylakoid system, they are located along the cell wall and occupy predominantly the part of the cell wall faced the intercellular airspace. Chloroplast movement starts in October-November, and during the winter they aggregate in the cell lobes clumping together. At that time, the thylakoid system is reorganised and consists mainly of long doubled thylakoids and small grana. The 3D reconstruction shows that the chloroplasts are irregularly oriented, swollen, and develop multiple protrusions filled by stroma that can be recognized as stromules. In indoor plants, seasonal reorganization of the mesophyll ultrastructure does not occur suggesting low temperatures but not photoperiod and light quality induce seasonal chloroplast movement in P. sylvestris mesophyll. Finally, we indicate 3D reconstruction is a powerful tool in study of low temperature-induced change of chloroplast positioning.

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About the authors

N. K. Koteyeva

Komarov Botanical Institute RAS

Author for correspondence.
Email: nkoteyeva@binran.ru
Russian Federation, 197022, St. Petersburg, Prof. Popova Str., 2

A. N. Ivanova

Komarov Botanical Institute RAS; St. Petersburg State University

Email: nkoteyeva@binran.ru
Russian Federation, 197022, St. Petersburg, Prof. Popova Str., 2; 199034, St. Petersburg, Universitetskaya Emb., 7–9

T. A. Borisenko

Komarov Botanical Institute RAS; St. Petersburg State University

Email: nkoteyeva@binran.ru
Russian Federation, 197022, St. Petersburg, Prof. Popova Str., 2; 199034, St. Petersburg, Universitetskaya Emb., 7–9

M. S. Tarasova

Komarov Botanical Institute RAS; St. Petersburg State University

Email: nkoteyeva@binran.ru
Russian Federation, 197022, St. Petersburg, Prof. Popova Str., 2; 199034, St. Petersburg, Universitetskaya Emb., 7–9

O. E. Mirgorodskaya

Komarov Botanical Institute RAS

Email: nkoteyeva@binran.ru
Russian Federation, 197022, St. Petersburg, Prof. Popova Str., 2

E. V. Voznesenskaya

Komarov Botanical Institute RAS

Email: nkoteyeva@binran.ru
Russian Federation, 197022, St. Petersburg, Prof. Popova Str., 2

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2. Fig. 1. General anatomy of Pinus sylvestris needles on cross (A) and longitudinal (B) sections, August. En – endodermis; Ep – epidermis; H – hypodermis; IAS – intercellular airspace; M – mesophyll; St – stomata; VB – vascular bundle. Scales: A, B, 150 µm.

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3. Fig. 2. Serial cross sections through mesophyll of Pinus sylvestris showing mesophyll cell extended from hypodermis to endodermis (labelled by red asterisk). The total number of sections is 351. The serial number of individual section is in the right corner of the image. En – endodermis; H – hypodermis; IAS – intercellular airspace; M – mesophyll cell; St – stomata. Scale: 50 µm.

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4. Fig. 3. Transmission electron microscopy of mesophyll cells in outdoor- (A–C, F) and indoor-grown (D, E) Pinus sylvestris. A, B, D. Cross sections in the midplane of a mesophyll cell in July (A) and February (B, D). C, E, F. Cross sections of chloroplasts in July (C) and February (E, F). Ch – chloroplasts; CW – cell wall; DT – doubled thylakoids; G – grana; N – nucleus; T – tannins; V – vacuole. Scales: A, B, D, 10 µm; C, E, 1 µm; F, 0.5 µm.

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5. Fig. 4. 3D reconstruction of mesophyll cells of Pinus sylvestris during vegetation (May–October) period. A. Cross section in the midplane of the cell. B–D. 3D reconstruction of chloroplasts located along the cell wall showing “summer” positioning (cell wall is not presented on the reconstruction), view from the lateral side of the cell (B) and view from the hypodermis (C) showing absence of chloroplasts along the adjacent cell walls (arrows) (D). Ch – chloroplasts; CW – cell wall; N – nucleus; V – vacuole. Scales: A–D, 10 µm.

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6. Fig. 5. 3D reconstruction of chloroplasts in mesophyll cells of Pinus sylvestris during winter (November–April). A. Cross section in the midplane of the cell. B, C. 3D reconstruction of chloroplasts grouped in one of the mesophyll cell lobe (cell wall is not presented on the reconstruction), view from the lateral side of the cell (B) and view from the hypodermis (С). D. 3D reconstruction of a single chloroplast viewed from different sides showing irregular shape and several protrusions. Ch – chloroplasts; CW – cell wall; N – nucleus; V – vacuole. Scales: A–C, 10 µm; D, 5 µm.

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