Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-26T03:42:42.798Z Has data issue: false hasContentIssue false
  • English
  • Français

Development of C-lignin with G/S-lignin and lipids in orchid seed coats – an unexpected diversity exposed by ATR-FT-IR spectroscopy

Published online by Cambridge University Press:  09 January 2018

S.T. Barsberg ,
Y.-I. Lee  and
H.N. Rasmussen
S.T. Barsberg*
Affiliation:
Department of Geosciences and Nature Resource Management, University of Copenhagen, Rolighedsvej 23, 1958 Frederiksberg C, Copenhagen, Denmark
Y.-I. Lee
Affiliation:
Biology Department, National Museum of Natural Science, No 1, Kuan-Chien Road, Taichung, Taiwan Department of Life Sciences, National Chung Hsing University, Taichung 40227, Taiwan
H.N. Rasmussen
Affiliation:
Department of Geosciences and Nature Resource Management, University of Copenhagen, Rolighedsvej 23, 1958 Frederiksberg C, Copenhagen, Denmark
*
Author for correspondence: S.T. Barsberg, Email: sbar@ign.ku.dk
Get access Rights & Permissions [Opens in a new window]

Abstract

Members of the orchid family occupy many germination niches, in terrestrial, epiphytic and epilithic environments. How orchid seeds attach to their substrate and survive after dispersal is largely unknown. C-lignin is a recently discovered specialized lignin, found in seed coats of some plants, including orchid species, but its functional and biological significance is obscure. We studied seed coat ontogenesis in three species (Neuwiedia veratrifolia, Cypripedium formosanum and Phalaenopsis aphrodite) that represent basal and advanced branches in orchid phylogeny and divergent life forms. From each species, controlled pollination yielded several stages of seed development, from which seed coats (testa) were isolated and analysed by ATR-FT-IR spectroscopy. The use of the ATR set-up ensured that the chemical information originated only from the integral outer seed surface layers. The FT-IR bands of C-lignin are presented here for the first time, and distinguished from bands of G/S-lignin. In the seed coats, C-lignin developed after G/S-lignin in N. veratrifolia and C. formosanum, while only G/S-lignin developed in P. aphrodite. We discuss C-lignin properties and possible function in relation to seed coat properties. The species differed with respect to sequence and amounts of deposition, not only of lignins but also lipids, resulting in differences in mature seed coat compositions. Thus we revealed an unexpected and marked diversity among orchids with respect to seed surface chemistry, with possible implications for seed and germination ecology.

Keywords

Cypripedium formosanumNeuwiedia veratrifoliaPhalaenopsis aphroditeOrchidaceaeseed coat ontogenesisdust seedsinfrared spectroscopysurface chemistry
Type
Research Papers
Information
Seed Science Research , Volume 28 , Issue 1 , March 2018 , pp. 41 - 51
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barsberg, S (2010) Prediction of vibrational spectra of polysaccharides – simulated IR spectrum of cellulose based on Density Functional Theory (DFT). Journal of Physical Chemistry B 114, 11703–11708.CrossRefGoogle ScholarPubMed
Barsberg, S, Rasmussen, HN and Kodahl, N (2013) Composition of Cypripedium calceolus (Orchidaceae) seeds analyzed by attenuated total reflectance IR spectroscopy: in search of understanding longevity in the ground. American Journal of Botany 100, 2066–2073.CrossRefGoogle ScholarPubMed
Barthlott, W, Große-Veldmann, B and Korotkova, N (2014) Orchid seed diversity: a scanning electron microscopy survey. Berlin: Botanic Garden and Botanical Museum Berlin-Dahlem. Englera 32.Google Scholar
Barthlott, W and Ziegler, B (1980) Über ausziehbare helicale Zellwandverdickungen als Haf-apparat der Samenschalen von Chiloschista lunifera (Orchidaceae). Berichten der Deutsche Botanische Gesellschaft 93, 391–403.CrossRefGoogle Scholar
Berstis, L, Elder, T, Crowley, M and Beckham, GT (2016) Radical nature of C-lignin. ACS Sustainable Chemistry and Engineering 4, 5327–5335.CrossRefGoogle Scholar
Brundrett, MC, Kendrick, B and Peterson, CA (1991) Efficient lipid staining in plant material with Sudan red 7B or fluoral yellow 088 in polyethylene glycol-glycerol. Biotechnic and Histochemistry 66, 111–116.Google Scholar
Cameron, KM (2011) Vanilla phylogeny and classification, pp. 243–255 in Havkin-Frenkel, D and Belanger, FC (eds), Handbook of Vanilla Science and Technology. New York: Wiley-Blackwell.Google Scholar
Cameron, KM and Chase, MW (1998) Seed morphology of Vanillioid orchids (Vanillioideae: Orchidaceae). Lindleyana 13, 148–169.Google Scholar
Carlson, MS (1940) Formation of the seed of Cypripedium parviflorum . Botanical Gazette 102, 295‒300.CrossRefGoogle Scholar
Chase, MW, Cameron, KM, Barrett, RI and Freudenstein, JV (2003) DNA data and Orchidaceae systematics: a new phylogenetic classification, pp. 69–89 in Dixon, KM, Kell, SP, Barrett, RI and Cribb, PJ (eds), Orchid Conservation. Kota Kinabalu, Natural History Publishers.Google Scholar
Chen, F, Tobimatsu, Y, Havkin-Frenkeld, D, Dixona, RA and Ralph, J (2012) A polymer of caffeyl alcohol in plant seeds. Proceedings of the National Academy of Sciences of the USA 109, 1772–1777.CrossRefGoogle ScholarPubMed
Chen, F, Tobimatsu, Y, Jackson, L, Nakashima, J and Ralph, J (2013) Novel seed coat lignins in the Cactaceae: structure, distribution and implications for the evolution of lignin diversity. Plant Journal 73, 201–211.Google Scholar
Clements, MA and Molvray, M (1999) Seed morphology, pp. 59–66 in Pridgeon, AM, Cribb, PJ, Chase, MW and Rasmussen, FN (eds), Genera Orchidacearum vol. 1: General Introduction, Apostasioideae, Cypripedioideae. Oxford: Oxford University Press.Google Scholar
Constant, S, Wienk, HLJ and Frissen, AE (2016) New insights into the structure and composition of technical lignins: a comparative characterisation study. Green Chemistry 18, 2651–2665.Google Scholar
Dence, CW and Lin, SY (1992) Methods in Lignin Chemistry. Heidelberg: Springer Verlag.Google Scholar
Faix, O (1991) Classification of lignins from different botanical origins by FT-IR spectroscopy. Holzforschung 45 (S), 21–27.Google Scholar
Fatihah, NHN, Fay, MF and Maxted, N (2011) Molecular phylogenetics of Cypripedium L. (Cypripedioideae: Orchidaceae) based on plastid and nuclear DNA sequences. Journal of Agrobiotechnology 2, 35–51.Google Scholar
Fowler, SD and Greenspan, P (1985) Application of Nile red, a fluorescent hydrophobic probe, for the detection of neutral lipid deposits in tissue sections: comparison with oil red O. Journal of Histochemistry and Cytochemistry 33, 833–836.CrossRefGoogle ScholarPubMed
Guillén, MD and Cabo, N (1997) Infrared spectroscopy in the study of edible oils and fats. Journal of the Science of Food and Agriculture 75, 1–11.Google Scholar
Harrick, NJ (1967) Internal reflection spectroscopy. New York, Wiley.Google Scholar
Harvais, G (1980) Scientific notes on a Cypripedium reginae of northwestern Ontario, Canada. American Orchid Society Bulletin 49, 237–244.Google Scholar
Hergert, H (1998) Developments in organosolv pulping – an overview, pp. 5–67 in Young, RA and Akhtar, M (eds), Environmentally Friendly Technologies for the Pulp and Paper Industry. New York: Wiley.Google Scholar
Hergert, HL (1971) Infrared spectra, pp. 267–297 in Sarkanen, KV and Ludwig, CH (eds), Lignins – Occurrence, Formation, Structure and Reactions. New York: Wiley.Google Scholar
Kačuráková, M, Capek, P, Sasinková, V, Wellner, N and Ebringerová, A (2000) FT-IR study of plant cell wall model compounds: pectic polysaccharides and hemicelluloses. Carbohydrate Polymers 43, 195–203.Google Scholar
Kodahl, N, Johansen, BB and Rasmussen, FN (2015) The embryo sac of Vanilla imperialis (Orchidaceae) is six-nucleate, and double fertilization and formation of endosperm are not observed. Botanical Journal of the Linnaean Society 177, 202–213.Google Scholar
Kurzweil, H (1993) Seed morphology in Southern African Orchidoideae (Orchidaceae). Plant Systematics and Evolution 185, 229–247.CrossRefGoogle Scholar
Larsen, KL and Barsberg, S (2010) Theoretical and Raman spectroscopic studies of phenolic lignin model monomers. Journal of Physical Chemistry B 114, 8009–8021.CrossRefGoogle ScholarPubMed
Lee, YI (2003) Growth periodicity, changes of endogenous abscisic acid during embryogenesis, and in vitro propagation of Cypripedium formosanum Hay . PhD dissertation, National Taiwan University, Taipei, Taiwan.Google Scholar
Lee, YI, Lee, N, Yeung, EC and Chung, MC (2005) Embryo development of Cypripedium formosanum in relation to seed germination in vitro . Journal of the American Society for Horticultural Science 130, 747–753.Google Scholar
Lee, YI, Yeung, EC, Lee, N and Chung, MC (2008) Embryology of Phalaenopsis amabilis var. formosa: embryo development. Botanical Studies 49, 139–146.Google Scholar
Lee, YI, Chung, MC, Yeung, EC and Lee, N (2015) Dynamic distribution and the role of abscisic acid during seed development of a lady's slipper orchid, Cypripedium formosanum . Annals of Botany 116, 403–411.CrossRefGoogle ScholarPubMed
Li, JH, Liu, ZJ, Salazar, GA, Bernhardt, P, Perner, H, Yukawa, T, Jin, XH, Chung, SW and Luo, YB (2011) Molecular phylogeny of Cypripedium (Orchidaceae: Cypripedioideae) inferred from multiple nuclear and chloroplast regions. Molecular Phylogenetics and Evolution 61, 308–320.Google Scholar
Nishimura, G and Yukawa, T (2010) Dark material accumulation and sclerotization during seed coat formation in Vanilla planifolia Jacks: Ex Andrews (Orchidaceae). Bulletin of the American Museum of Natural History Ser B 36, 33–37.Google Scholar
Prutsch, J, Schardt, A and Schill, R (2000) Adaptations of an orchid seed to water uptake and –storage. Plant Systematics and Evolution 220, 69–75.Google Scholar
Rasmussen, HN and Pedersen, HÆ (2011) Cypripedium calceolus germination in situ: Seed longevity, and dormancy breakage by long incubation and cold winters. European Journal of Environmental Science 1, 69–70.Google Scholar
Rasmussen, HN and Rasmussen, FN (2014) Seedling mycorrhiza: a discussion of origin and evolution in Orchidaceae. Botanical Journal of the Linnean Society 175, 313–327.Google Scholar
Rauh, W, Barthlott, W and Ehler, N (1975) Morphologie und Funktion der Testa staubförmiger Flugsamen. Botaniche Jahrbücher für Systematik 96, 353–374.Google Scholar
Rodolphe, G, Severine, B, Michel, G and Pascale, B (2011) Biodiversity and evolution in the Vanilla genus, pp. 1–27 in Grillo, O and Venora, G (eds), The Dynamical Processes of Biodiversity – Case Studies of Evolution and Spatial Distribution (online). http://www.intechopen.com/books.Google Scholar
Ruzin, SE (1999) Plant Microtechnique and Microscopy. New York: Oxford University Press.Google Scholar
Sletvold, N, Øien, D-I and Moen, A (2010) Long-term influence of moving on population dynamics in the rare orchid Dactylorhiza lapponica: the importance of recruitment and seed production. Biological Conservation 143, 747–755.Google Scholar
Suetsugu, K, Kawakita, A and Makoto Kato, M (2015) Avian seed dispersal in a mycoheterotrophic orchid Cyrtosia septentrionalis . Nature Plants 1, 15052. doi: 10.1038/nplants.2015.52.Google Scholar
Thompson, DT, Edwards, TJ and Van Staden, J (2001) In vitro germination of several South African summer rainfall Disa (Orchidaceae) species – is seed structure a function of habitat and determinant of germinability? Systematics and Geography of Plants 71, 597–606.Google Scholar
Tobimatsu, Y, Chen, F, Nakashima, J, Escamilla-Treviño, LL, Jackson, L, Dixon, R and Ralph, J (2013) Coexistence but independent biosynthesis of catechyl and guaiacyl/syringyl lignin polymers in seed coats. Plant Cell 25, 2587–2600.Google Scholar
Tsutsumi, C, Yukawa, T, Lee, NS, Lee, CS and Kato, M (2007) Phylogeny and comparative seed morphology of epiphytic and terrestrial species of Liparis (Orchidaceae). Japanese Journal of Plant Research 120, 405–412.Google Scholar
Vázquez, G, Antorrena, G, González, J and Freire, S (1997) FTIR, 1H and 13C NMR characterization of Acetosolv-solubilized pine and eucalyptus lignins. Holzforschung 51, 158–166.Google Scholar
Verma, J, Kranti Thakur, K, Sembi, JK and Vij, SP (2012) Study of seed morphometry or seven threatened Himalayan orchids exhibiting varied life modes. Acta Botanica Gallica 159, 443–449.Google Scholar
Yang, CK and Lee, YI (2014) The seed development of a mycoheterotrophic orchid, Cyrtosia javanica Blume. Botanical Studies 55, 44.Google Scholar
Yeung, EC, Zee, SY and Ye, XL (1996) Embryology of Cymbidium sinense: embryo development. Annals of Botany 78, 105–110.Google Scholar
Zeng, S, Zhang, Y, Teixeira da Silva, JA, Wu, KI, Zhang, J and Duan, J (2014) Seed biology and in vitro seed germination of Cypripedium . Critical reviews in biotechnology 34, 358–371.Google Scholar
Supplementary material: File

Barsberg et al. supplementary material

Barsberg et al. supplementary material 1

Download Barsberg et al. supplementary material(File)
File 121.7 KB