Carotenoid composition and its chemotaxonomic significance in leaves of ten species of the genus Ceratozamia (Cycads)
Introduction
There has recently been intensified development of research on cycads. Cycads are a relict group of ancient and morphologically primitive gymnosperms now conventionally considered as “living fossil plants”. Their maximum diffusion was in the Mesozoic era (150×106 years ago) when they represented 20–25% of terrestrial vegetation. They still exist today, but mostly in restricted tropical areas. The genus Ceratozamia is one of 11 genera still surviving and it is present today only in Mexico.
Until the 1980s there was no information available on carotenoid pigments in the photosynthetic tissues of these plants. Limited data on ripe seed coat carotenoids indicated a simple mixture of classic carotenoids occurring in the chromoplasts of seeds of some cycads (Bouchez et al., 1970; Baumann and Yokoyama, 1976; Whatley, 1985).
As recently as 1981 (Ida, 1981), the first data appeared on some classic carotenoids in Cycas revolute, which contained α- and β-carotene, violaxanthin, and lutein in green leaves, while rodoxanthin was also found in senescing leaves. Subsequently, a red keto seco-carotenoid, isolated for the first time from young leaflets of Ceratozamia fuscoviridis (Cardini, 1984), was fully identified as the very rare semi-β-carotenone in leaflets of two cycads: C. fuscoviridis and C. kuesteriana Regel (Cardini et al., 1987; quoted by Enzell and Back, 1995).
The C. fuscoviridis described by Moore (1878) and considered by Schuster (1932) as one of the forms of C. mexicana Brongn. has been renamed C. mexicana Brongniart var. latifolia “forma fuscoviridis” Moore ex Schuster (Stevenson and Sabato, 1986) while C. kuesteriana Regel is a true, attributed species rediscovered in Mexico (Moretti et al., 1982).
The leaflets of C. fuscoviridis Moore and of C.mexicana Brongn. have been particularly of interest because they are easily available: several specimens of cycad genera belonging to the collection of the National Botanical Garden Glasnevin in Dublin were given to the Botanical Garden of the University of Florence in 1907 where the original label, C. fuscoviridis, has been maintained. In the present text this binomial will be used.
In these two cycads, in addition to the very rare semi-β-carotenone, three other red keto-carotenoids have subsequently been isolated and fully identified: the very rare triphasiaxanthin (Cardini et al., 1990), the β-carotenone (Selva et al., 1994), and the novel ceratoxanthin (Cardini et al., 1989; quoted by Hull and Pfander, 1995). Three other novel red keto seco-carotenoids have only been partially characterized (ceratozamiaxanthin, kuesteriaxanthin, and ceratoxanthone, Selva et al., 2003), and traces of a remaining unknown epiphasic keto-carotenoid are also present. All eight of these compounds constitute a complex red keto-mixture that in the first stages of leaflet development represents a high percentage of the total carotenoids (more than 70% in C. fuscoviridis).
In sonicated and isolated chloroplasts, as evidenced by co-chromatography on silica gel layers employing as standards natural keto-carotenoids obtained in our laboratory, these keto-carotenoids appeared in an unusual location. They were not in the thylakoidal membranes but in very electron-dense plastoglobules (PGLs) of the stroma, which, in the case of leaflets of C. fuscoviridis, are found closely packed around the prolamellar body. Therefore, the very young leaflets of the pinnate leaf show a transitory dark red brown coloration that is evidently correlated with the presence of these peculiar plastoglobules because both of them progressively disappear while the development of the thylakoidal system proceeds at the same rate of leaflet expansion (Morassi Bonzi et al., 1992, Morassi Bonzi et al., 1996).
It is known that chloroplasts of developing tissues generally do not contain or contain only few plastoglobules that increase in size and in number when the thylakoids are degrading during leaf senescence (Lichtenthaler, 1969a, Lichtenthaler, 1969b), and consequently become a pool of various lipids, secondary carotenoids, and protein.
On the contrary, the presence of plastoglobules could be involved in the progressive formation of thylakoids and the relative organization of photosynthetic apparatus. In fact, while the thylakoids are developing in parallel with the growth pattern, the neoformed leaflets tend to expand, becoming green up to a final stage of full ripeness. Moreover, during these processes the stroma plastoglobules, which contain exclusively the pool of red keto-carotenoids, decrease in size and number and tend progressively to disappear. A possible role as passive “sunscreen” in protecting the photosynthetic apparatus during its organization has also been proposed (Morassi Bonzi et al., 1992, Morassi Bonzi et al., 1996; Bar et al., 1995).
After having concentrated our study on the two mentioned species (C. fuscoviridis and C. kuesteriana), we gradually extended the research of this pool of keto carotenoids present in stroma plastoglobules to seven other species of genus Ceratozamia. In addition, we characterized the thylakoidal carotenoids in all the species considered in this investigation.
Section snippets
Plant materials
Variable amounts of fresh green leaflets of C. mexicana Brongn. and red-brown or also green leaflets of C. fuscoviridis were obtained from the collection of the Botanical Garden of the University of Florence.
Red-brown or green leaflets of the other eight species of Ceratozamia (C. kuesteriana, C. robusta, C. hildae, C. matudae, C. spinosa, C. microstrobila, C. zaragozae, and C. latifolia) were obtained from the collection of the Botanical Garden of the University of Naples.
Procedures
Limbs of the ten
Results
The studies were carried out on ten species of the genus Ceratozamia, including those divided into fully attributed species and those of still uncertain attribution, and on coloration of the newly formed leaflets of the pinnate leaf (Table 1). Note that only C. mexicana Brongn. leaflets are always green during the span of development.
For this investigation, the moment of complete development of the thylakoidal apparatus was selected as the first stage for both qualitative and quantitative
Discussion
The qualitative composition and localization of carotenoids in leaflets of ten species of the genus Ceratozamia (Cycads) have been investigated. It is admitted that, among the ten species considered, only the leaflets of C. mexicana Brongn. are always green, both samples from the wild in Mexico and in samples cultivated in collections of several botanical gardens in Europe (Stevenson, personal communication). On the contrary, the leaflets of the other nine species, before they have been
Acknowledgments
We thank Prof. F. Fabbri and Dr. G. Cellai Ciuffi (Botanical Garden of the University of Florence) for the supply of C. mexicana Brongn. and the “forma fuscoviridis”. We also thank Prof. A. Moretti and particularly Prof. G. De Luca (Botanical Garden the University of Naples) for the supply of the other eight species of genus Ceratozamia.
A particular thanks to Mr. S. Fioretti of the Botanical Garden of Naples for his expert support in sampling the various species of Cycads investigated.
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