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Lamelloplasts and minichloroplasts in Begoniaceae: iridescence and photosynthetic functioning

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Abstract

Iridoplasts (modified plastids in adaxial epidermal cells) reported from Begonia were originally hypothesized to cause iridescence, which was broadly accepted for decades. However, several species of Begonia with iridoplasts are not iridescent causing confusion. Here chloroplast ultrastructure was observed in 40 taxa of Begoniaceae to explore the phenomenon of iridescence. However, 22 Begonias and Hillebrandia were found to have iridoplasts, but only nine display visually iridescent blue to blue-green leaves. Unexpectedly, a new type of plastid, a ‘minichloroplast,’ was found in the abaxial epidermal cells of all taxa, but was present in adaxial epidermal cells only if iridoplasts were absent. Comparative ultrastructural study of iridoplasts and a shading experiment of selected taxa show that a taxon with iridoplasts does not inevitably have visual iridescence, but iridescence is greatly affected by the spacing between thylakoid lamellae (stoma spacing). Thus, we propose instead the name ‘lamelloplast’ for plastids filled entirely with regular lamellae to avoid prejudging their function. To evaluate photosynthetic performance, chlorophyll fluorescence (Fv/Fm) was measured separately from the chloroplasts in the adaxial epidermis and lower leaf tissues by using leaf dermal peels. Lamelloplasts and minichloroplasts have much lower photosynthetic efficiency than mesophyll chloroplasts. Nevertheless, photosynthetic proteins (psbA protein of PSII, RuBisCo and ATPase) were detected in both plastids as well as mesophyll chloroplasts in an immunogold labeling. Spectrometry revealed additional blue to blue-green peaks in visually iridescent leaves. Micro-spectrometry detected a blue peak from single blue spots in adaxial epidermal cells confirming that the color is derived from lamelloplasts. Presence of lamelloplasts or minichloroplasts is species specific and exclusive. High prevalence of lamelloplasts in Begoniaceae, including the basal clade Hillebrandia, highlights a unique evolutionary development. These new findings clarify the association between iridescence and lamelloplasts, and with implications for new directions in the study of plastid morphogenesis.

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Acknowledgements

The authors thank the editor and three anonymous reviewers for valuable comments and suggestions. This article is dedicated to the memory of the late Dr. C. C. Tsai who did much to promote the study of plant phylogeny and structure. The authors thank Dr. W. H. Hu (The National Museum of Natural Science, Taichung) for providing the material of Hillebrandia, Miss P. C. Chaw (National Chung Hsing University) for assistance in TEM operation, and Mr. Lin (Meijia Company) for assistance in CSLM operation. This study was partially supported by the Ministry of Science and Technology [MOST-101-2621-B-005-002-MY3; MOST 104-2621-B-005-002-MY3], Taiwan.

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Authors and Affiliations

  1. Department of Life Sciences and Center of Global Change Biology, National Chung Hsing University, 145 Xingda Rd., South Dist., Taichung, 402, Taiwan

    Shang-Hung Pao, Ping-Yun Tsai, Peter Chesson & Chiou-Rong Sheue

  2. Biodiversity Research Center, Academia Sinica, 128, Sec. 2, Academia Rd., Taipei, 115, Taiwan

    Ching-I Peng

  3. Department of Entomology, National Taiwan University, 1, Sec. 4, Roosevelt Rd., Taipei, 106, Taiwan

    Pei-Ju Chen & En-Cheng Yang

  4. Department of Evolutionary Studies of Biosystems, SOKENDAI (The Graduate University for Advanced Studies), Shonan Village, Hayama, Kanagawa, 240-0193, Japan

    Pei-Ju Chen

  5. Kaohsiung District Agricultural Research and Extension Station, 2-6 Dehe Rd., Changjhih, 908, Pingtung County, Taiwan

    Chi-Chu Tsai

  6. Department of Physics, National Chung Hsing University, 145 Xingda Rd., South Dist., Taichung, 402, Taiwan

    Ming-Chih Shih & Jiannyeu Chen

  7. Research Center for Sustainable Energy and Nanotechnology, National Chung Hsing University, 145 Xingda Rd., South Dist., Taichung, 402, Taiwan

    Ming-Chih Shih & Jiannyeu Chen

  8. Institute of Biochemistry, National Chung Hsing University, 145 Xingda Rd., South Dist., Taichung, 402, Taiwan

    Jun-Yi Yang

  9. Department of Ecology and Evolutionary Biology, The University of Arizona, Tucson, AZ, 85721, USA

    Peter Chesson & Chiou-Rong Sheue

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  1. Shang-Hung Pao
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  2. Ping-Yun Tsai
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  3. Ching-I Peng
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  4. Pei-Ju Chen
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  5. Chi-Chu Tsai
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  7. Ming-Chih Shih
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  8. Jiannyeu Chen
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  9. Jun-Yi Yang
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  10. Peter Chesson
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  11. Chiou-Rong Sheue
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Corresponding author

Correspondence to Chiou-Rong Sheue.

Additional information

Deceased: Chi-Chu Tsai, Ching-I Peng.

Dr. Ching-I Peng named 93 new species of Begonia, and is widely acknowledged for his contributions to Begonia research.

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Pao, SH., Tsai, PY., Peng, CI. et al. Lamelloplasts and minichloroplasts in Begoniaceae: iridescence and photosynthetic functioning. J Plant Res 131, 655–670 (2018). https://doi.org/10.1007/s10265-018-1020-2

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