Photosynthesis in a Vanda sp orchid with Photosynthetic Roots
Introduction
Crassulacean acid metabolism (CAM) involves a reversal of normal stomatal function such that plants open their stomates at night and temporarily fix CO2 as C4 organic acids before closing their stomates in daylight, decarboxylating the C4 acids accumulated in the plant values and refixing the CO2 via the Calvin cycle. Classic examples of obligate or constitutive CAM plants are many orchids and bromeliads (Ritchie and Bunthawin, 2010a,b) but some orchids exhibit little or no CAM (Goh et al., 1983; Oncidium ‘aloha’: Rodriques et al., 2013). Many CAM plants are obligate CAM, in other words they perform CAM physiology regardless of their water status whereas some plants only perform CAM physiology when under water stress (Mesembryanthemum crystallinum: Ślesak et al., 2003; Broetto et al., 2007). Other examples of obligate CAM plants are Kalanchoe daigremontiana and K. pinnata (Von Caemmerer and Griffiths, 2009). Clusia species cover the entire spectrum from obligate CAM, facultative CAM and C3-CAM intermediates (Lüttge, 1999) and there are many other examples of facultative CAM (Winter and Holtum, 2014) and variants such as CAM-cycling (Kerbauy et al., 2012). All part of the CAM continuum (Silvera et al., 2010).
Some CAM plants are not only capable of CAM physiology but may be highly resistant to desiccation of the plant cells but rapidly recover when watered (Kerbauy et al., 2012). Such plants are called resurrection plants (Lüttge, 2004, 2010; Kessler and Siorak, 2007). There are two types of resurrection plant: in some the cytoplasm and chloroplasts are strongly resistant to desiccation but recover in only a matter of minutes to rehydrate (homiochlorophyllous), the other type need to resynthesize their chloroplasts and can take hours or days to fully recover (poikiloochlorophyllous) (Kessler and Siorak, 2007). The epiphytic orchid Dimerandra emarginata behaves like a poikiloochlorophyllous species because it takes a few days to recover from severe water stress (Zotz et al., 2001). In a previous study we found that the epiphytic fern Davallia angustata (Wall, ex Hook. and Grev.) was a homiochlorophyllous resurrection plant but was not a CAM plant (Quinnell et al., 2017). CAM has evolved several times and there is a continuum of some species from obligate CAM, facultative CAM to no discernible CAM activity at all (Silvera et al., 2010; Winter and Holtum, 2014).
Many epiphytic orchids have green-coloured roots that contain chlorophyll but have varying levels of photosynthetic activity (Goh et al., 1983; Zotz and Winkler, 2013; Rodriques et al., 2013; Kerbauy et al., 2012) and so the question arises how important is the photosynthesis of such roots? In Phalaenopsis species the aerial roots typically appear dry and inactive and are covered by a dull green parchment-like epidermis called the velamen radicum (Zotz and Winkler, 2013; Kerbauy et al., 2012). The aerial roots are thought to be active in nutrient acquisition when wet from dewfall and rainfall. The photosynthetic activity of aerial roots do not appear to have been frequently investigated (Goh et al., 1983) but an example of a leafless orchid that has CAM is Campylocentrum tryyidion which has very succulent roots which would be expected to be found in any tissue capable of CAM (Winter et al., 1985). Goh et al. (1983) found that the aerial roots of two epiphytic orchids (Arachnis Maggi Oei & Aranda Deborah) exhibited very little photosynthesis but the aerial roots showed no CAM acid accumulation (Fig. 2 in Goh et al., 1983). The CAM accumulation of acids in roots was very small compared to leaves. On the other hand, gas exchange and pulse amplitude modulation (PAM) fluorometry on the ground orchid Corallorhiza trifida showed that it fixes very little carbon photosynthetically (Cameron et al., 2009). Velamen radicum covered orchid roots generally have poor photosynthetic activity (rarely measured experimentally) and marginal or absent CAM physiology (Kerbauy et al., 2012).
Vanda sp (Gaud ex Pfitzers, Vandeae) (about 80 species and hybrids) are common epiphytic orchids used as ornamental orchids in much of SE-Asia. Ornamentals are heavily hybridised and so a species name might be misleading. It was found growing as an ornamental epiphyte on tree trunks on the campus of Prince of Songkla University Phuket, Thailand (lat. 7°53, long 98°24E). The species had inert-looking aerial roots covered in a parchment like layer (velamen radicum). The aerial roots were not succulent as found in Campylocentrum tryyidion (Winter et al., 1985). The study was made in October-November 2019 which is in the wet season of Phuket (Thailand). The roots were found to be opportunistically homiochlorophyllous with no apparent CAM. The leaves had a limited capacity for CAM and fixed organic acids in early morning daylight rather than at night (CAM-cycling, Silvera et al., 2010; Kerbauy et al., 2012).
Section snippets
PAM fluorometry
Pulse Amplitude Modulation Fluorometry (PAM) is a method to directly measure the light reactions of PSII in photosynthesis (Ralph and Gademann, 2005; Brestic and Zivcak, 2013). A Junior PAM portable chlorophyll fluorometer (Gademann Instruments, Würzburg, Germany) was used in the study. The PAM parameters (Y, rETR, qN, NPQ) were automatically calculated using the WINCONTROL software (v2.08 and v2.13; Heinz Walz Gmbh, Effeltrich, Germany) using the standard default settings for rapid light
Results and discussion
Fig. 1 shows the yield and rapid light curves for orchid leaves measured at 12 a.m. over an irradiance range up to 850 μmol photon m−2 s−1(PPFD), n = 6, ±95% confidence limits. Yield: Ymax = 0.617 ± 0.262, Y½ = 128 ± 12.4 μmol photon m−2 s−1, r = 0.9831. ETR: Eopt = 369 ± 23.3 μmol photon m−2 s−1, ETR (surface areas basis) = 26.0 ± 1.00 μmol e− m−2 s−1, ETR (Chl a basis) = 97.6 ± 3.76 μmol e− g−1 Chl a s−1, r = 0.9607. NPQ plotted against irradiance showed a simple exponential saturation curve:
Conclusion
Overall, it can be concluded that the Vanda orchid exhibited a very limited CAM physiology in its leaves and no apparent CAM in its roots. In particular, no apparent accumulation of C4 acid occurred during nightime (Table 1) but there was measureable acid accumulation in the leaves in the first few hours of daylight which disappeared during the course of the day, behaviour consistent with CAM-cycling metabolism (Silvera et al., 2010; Kerbauy et al., 2012). This difference in timing of acid
CRediT authorship contribution statement
Suhailar Sma-Air: Writing - review & editing. Raymond J. Ritchie: Conceptualization, Methodology, Software, Writing - original draft, Writing - review & editing.
Declaration of Competing Interest
Suhailar Sma-air was employed to assist in the project by Raymond J. Ritchie; otherwise there are no conflicts of interest.
Acknowledgements
This paper is based upon a study of orchid physiology partially funded by Prince of Songkla University-Phuket, Faculty of Technology and Environment. The authors wish to thank the university for access to their facilities. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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