Lamelloplasts and minichloroplasts in Begoniaceae: iridescence and photosynthetic functioning
- 416 Downloads
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 (F v /F m ) 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.
KeywordsBegonia Chlorophyll fluorescence Chloroplast Epidermal plastid Fv/Fm Hillebrandia Lamellar structure Reflectance spectrum Shade plant
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.
- de Wilde JJFE (2011) Begoniaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol 2. Springer, Berlin, pp 56–71Google Scholar
- Doorenbos JM, Sosef SM, de Wilde JJFE (1998) The sections of Begonia, including descriptions, keys and species lists (studies in Begoniaceae VI). Wageningen Agricultural University, WageningenGoogle Scholar
- Gu C, Peng CI, Turland NJ (2007) Begoniaceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol 13. Science Press, Beijing, Missouri Botanical Garden, St. Louis, pp 153–207Google Scholar
- Jacobs M, Lopez-Garcia M, Phrathep OP et al (2016) Photonic multilayer structure of Begonia chloroplasts enhances photosynthetic efficiency. Nat Plants 2:161162Google Scholar
- Jangoux J (2002) Begonia venosa in the Chapada Diamantina, Bahia, Brazil. Begonian 69. http://www.begonias.org/Articles/Vol69/Begonia_venosa.htm. Accessed 28 Feb 2017
- Kiew R (2005) Begonias of Peninsular Malaysia. National History Publications, Kota Kinabalu (Borneo)Google Scholar
- Lai KS (2008) Taiwan’s native begonias and environmental needs. Nat Conserv Q 63:24–30Google Scholar
- Pao SH (2012) A study on leaf structure, mechanism of foliar variegation and novel chloroplasts in Begoniaceae. Master thesis, National Chiayi University, ChiayiGoogle Scholar
- Sheue CR, Sarafis V, Liu HY et al (2004) Structural study on leaves of super shade plants. In: Proceedings of the 24th R. O. C. symposium on microscopy, 17th January. National Defense Medical Center, TaipeiGoogle Scholar
- Shui YM, Peng CI, Wu CY (2002) Synopsis of the Chinese species of Begonia (Begoniaceae), with a reappraisal of sectional delimitation. Bot Stud 43:313–327Google Scholar
- Wu YH (2012) Chloroplast diversity, bizonoplast development and immunogold labeling of photosynthetic protein of Selaginella erythropus. Master thesis, National Chiayi University, ChiayiGoogle Scholar