Fv/Fm, a measure of leaf’s efficiency in converting absorb light energy to photochemical activity (Bjorkman 1981) and a sensitive indicator of stress (Kooten and Snel 1990, Maxwell and Johnson 2000) was high (approximately 0.8) and did not differ significantly in A. rufescens, regardless of leaf halves (upper or lower), light level (high or low), or water treatment (well-watered and drought). This finding indicates that the plants in this study were not under high levels of stress. In addition, mean anthocyanin concentrations were not different among water treatment (well-water and drought) or leaf halves (abaxial and adaxial).
In contrast, the amount of anthocyanin in whole leaves was positively correlated with Fv’/Fm’, which reflects the efficiency of utilization of light absorbed by the chlorophyll in the leaves. Thus, when leaf anthocyanin concentrations were low, the leaves did not efficiently utilize the light they absorbed by the chlorophyll. The qP and qN results indicate that this inefficiency was likely the result of temporary problems in the photochemical apparatus and a lack of thermal dissipation qN of the absorbed energy.
The above finding applied to data combined for both light treatments.
However, if the data from the high light and low light treatments were analyzed separately, anthocyanin concentrations correlated positively with fluorescence parameters only in the high light treatment. This finding is consistent with the results discussed above; plants in the high light treatment were more likely to
suffer problems such as photodamage. The lack of an apparent photoprotective role of anthocyanin in the low light-grown plants in this study may simply reflect the low probability of photodamage as a result of the low irradiances under which these plants were grown.
Drought treatment
Many studies have provided strong evidence that anthocyanin is an important pigment directly or indirectly attenuating drought stress (Chalker-Scott 1999, Sperdouli and Moustakas 2012). In many species, drought stress induced or enhanced the accumulation of anthocyanin (Sherwin and Farrant 1998, Sperdouli and Moustakas 2012, Osório et al. 2013). In contrast, leaf anthocyanin concentrations were unaffected by drought stress in plants of A.
rufescens. The results of this study imply that the photoprotective role of
anthocyanin in this species is more important than a direct role in reducing the effects of drought stress.
Fv/Fm values of plants in the low light treatment were significantly lower after the drought; however, the difference between values before and after drought was so small that the biological significance of this difference is questionable. On the other hand, a decrease in Fv/Fm values following drought stress is a common finding in many other plants (Efeoğlu et al. 2009, Sperdouli and Moustakas 2012, Osório et al. 2013). Although, Fv/Fm values in the high
light treatment did not significantly decrease after drought, the apparent decrease in Fv/Fm in the high light plants was similar in magnitude to the decrease in Fv/Fm observedin the low light plants.
The light-adapted efficiency of light utilization (Fv’/Fm’) decreased after drought in the high light treatment, but did not significantly change in plants grown at low light. These findings indicate that the combination of drought stress and high light temporarily decreased the plants’ ability to efficiently utilize the light energy absorbed by the chlorophyll, but only in the high light treatment. Furthermore, nonphotochemical dissipation of absorbed light energy (qN) decreased with drought in the plants grown under high light, while
photochemical activity (qP) did not change. Therefore, the decline in the
efficiency of light energy utilization after its absorption by the chlorophyll can be ascribed, at least in part, to the loss of absorbed energy by
nonphotochemical, thermal dissipation.
Although the difference in Fv’/Fm’ before and after drought was not statistically significant in the low light treatment, qP decreased significantly, indicating that the rate of the light reactions (photochemical activity) declined with the drought treatment. The latter two results appear contradictory and indeed are, considering many past studies of stress effects on the manner in which absorbed light is utilized in the photochemical apparatus in plants under stress (Demmig-Adams and Adams 1992). Perhaps a greater sample size would result in similar declines in these two measures (Fv’/Fm’ and qP) in these plants grown under low light and drought-stressed.
It is clear that the manner in which light energy was utilized by the A.
rufescens plants was different according to their growth light level. This may
prove to be important to plants in situ as a result of microclimatic differences associated with the microhabitats in which these plants are found, e.g., shading by surrounding plants, stones, etc. vs. full exposure.
Conclusions
Leaf anthocyanin appears to play an important role in photoprotection in the South African succulent A. rufescens, which is likely important for survival under exposed conditions in an arid environment. For example, leaves with higher concentrations of anthocyanin exhibited less evidence of photoinhibition.
Anthocyanin was found in both the adaxial and abaxial halves of the leaves, which should prevent damage due to high levels of irradiance from above the plants in exposed environments and from below the leaves due to reflection from rock surfaces in the plant environment. The photosynthetic (i.e.,
fluorescence) responses of plants under drought stress were variable and depended on the light level at which the plants were grown.
Overall, anthocyanin in the leaves of this succulent from arid region in South Africa appears to be important for optimal ecophysiological function in a highly stressful habitat. This study is the first to explore the ecophysiological functions of anthocyanin in a South African succulent with a bifacial
distribution of this pigment in the leaves of this xerophyte. It is also one of very few studies examining the potential importance of this photoprotective pigment on abaxial and adaxial leaf halves of a heliophyte.
, I would like to thank the two advisors for tolerance my poor English.
Reference
Alexieva, V., I. Sergiev, S. Mapelli, and E. Karanov. 2001. The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat.
Plant, Cell and Environment 24:1337-1344.
Bahler, B. D., K. L. Steffen, and M. D. Orzolek. 1991. Morphological and biochemical comparison of a purple-leafed and a green-leafed pepper cultivar. HortScience 26:736.
Bjorkman, O. 1981. Responses to different quantum flux densities. Pages. 57-107 in OL Lange, PS Nobel, CB Osmond, H Ziegler, editors.
Physiological Plant Ecology, Vol. I. Responses to the physical environment. Springer, Berlin.
Björkman, O. and S. Powles. 1984. Inhibition of photosynthetic reactions under water stress: interaction with light level. Planta 161:490-504.
Boardman, N. K. 1977. Comparative photosynthesis of sun and shade plants.
Annual Review of Plant Physiology 28: 355-377.
Bowler, C., G. Neuhaus, H. Yamagata, and N.-H. Chua. 1994. Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77:73-81.
Burger, J. and G. E. Edwards. 1996. Photosynthetic efficiency, and
photodamage by uv and visible radiation, in red versus green leaf coleus varieties. Plant and Cell Physiology 37:395-399.
Caldwell, M. M., S. D. Flint, and P. S. Searles. 1994. Spectral balance and UV-B sensitivity of soybean: a field experiment. Plant, Cell and Environment
17:267-276.
Chalker-Scott, L. 1999. Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology 70:1-9.
Close, D. and C. Beadle. 2003. The ecophysiology of foliar anthocyanin. The Botanical Review 69:149-161.
Constable, G. A. and H. M. Rawson. 1980. Effect of leaf position, expansion, and age on photosynthesis, transpiration, and water use efficiency of cotton. Australian Journal of Plant Physiology 7:89-100.
Curtis, J. D., N. R. Lersten, and G. P. Lewis. 1996. Leaf anatomy, emphasizing unusual ‘concertina’ mesophyll cells, of two east African legumes
(caesalpinieae, caesalpinioideae, leguminosae). Annals of Botany 78:55-59.
DeLucia, E. H., T. A. Day, and T. C. Vogelman. 1992. Ultraviolet-B and visible light penetration into needles of two species of subalpine conifers during foliar development. Plant, Cell and Environment 15:921-929.
Demmig-Adams, B., W. W. Adams Iii, D. H. Barker, B. A. Logan, D. R.
Bowling, and A. S. Verhoeven. 1996. Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum 98:253-264.
Demmig-Adams, B. and W. W. Adams. 1992. Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43:599-626.
Drumm-Herrel, H. and H. Mohr. 1982. Effect of blue/UV light on anthocyanin
synthesis in tomato seedlings in the absonce of bulk carotenoids.
Photochem. Photobiol. 36:229-233.
Efeoğlu, B., Y. Ekmekçi, and N. Çiçek. 2009. Physiological responses of three maize cultivars to drought stress and recovery. South African Journal of Botany 75:34-42.
Feild, T. S., D. W. Lee, and N. M. Holbrook. 2001. Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiology 127:566-574.
Furuta, K. 1986. Host preference and population-dynamics in an autumnal population of the maple aphid, periphyllus-californiensis shinji
(homoptera, aphididae). Journal of Applied Entomology-Zeitschrift Fur Angewandte Entomologie 102:93-100.
Giusti, M. M., L. E. Rodríguez-Saona, and R. E. Wrolstad. 1999. Molar absorptivity and color characteristics of acylated and non-acylated pelargonidin-based anthocyanins. Journal of Agricultural and Food Chemistry 47:4631-4637.
Gould, K. S. 2004. Swiss army knife: the diverse protective roles of anthocyanins in leaves. Journal of Biomedicine and Biotechnology 2004:314-320.
Gould, K. S., K. R. Markham, R. H. Smith, and J. J. Goris. 2000. Functional role of anthocyanins in the leaves of Quintinia Serrata A. Cunn. Journal of Experimental Botany 51:1107-1115.
Gould, K. S., J. McKelvie, and K. R. Markham. 2002. Do anthocyanins
function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury. Plant, Cell and Environment 25:1261-1269.
Hsiao, T. C. 1973. Plant responses to water stress. Annual Review of Plant Physiology and Plant Molecular Biology 24:519-570
Hamilton, W. D. and S. P. Brown. 2001. Autumn tree colours as a handicap signal. Proceedings of the Royal Society of London. Series B: Biological Sciences 268:1489-1493.
Harborne, J. B. 1965. Flavonoids: distribution and contribution to flower colour.
Pages 247–278 in T. W. Goodwin, editor. Chemistry and Biochemistry of Plant Pigments. Academic Press, London.
Harborne, J. B. and C. A. Williams. 2001. Anthocyanins and other flavonoids.
Natural Product Reports 18:310-333.
Hipskind, J., K. Wood, and R. L. Nicholson. 1996. Localized stimulation of anthocyanin accumulation and delineation of pathogen ingress in maize genetically resistant to Bipolaris maydis race O. Physiological and Molecular Plant Pathology 49:247-256.
Kooten, O. and J. H. Snel. 1990. The use of chlorophyll fluorescence
nomenclature in plant stress physiology. Photosynthesis Research 25:147-150.
Krol, M., G. R. Gray, N. P. A. Huner, V. M. Hurry, G. Ö quist, and L. Malek.
1995. Low-temperature stress and photoperiod affect an increased tolerance to photoinhibition in Pinus banksiana seedlings. Canadian
Journal of Botany 73:1119-1127.
Lee, D. W. 2001. Phylogenetic and ontogenetic influences on the distribution of anthocyanins and betacyanins in leaves of tropical plants. International journal of plant sciences 162:1141.
Lee, D. W. 2002. Anthocyanins in leaves: distribution, phylogeny and development. Advances in Botanical Research 37:37-53.
Leng, P., H. Itamura, and H. Yamamura. 1993. Freezing tolerance of several diospyros species and kaki cultivars as related to anthocyanin formation.
Journal of the Japanese Society for Horticultural Science 61:795-804.
Li, J., T. M. Ou-Lee, R. Raba, R. G. Amundson, and R. L. Last. 1993.
Arabidopsis flavonoid mutants are hypersensitive to uv-b irradiation. The Plant Cell Online 5:171-179.
Long, S. P., S. Humphries, and P. G. Falkowski. 1994. Photoinhibition of photosynthesis in nature. Annual Review of Plant Physiology and Plant Molecular Biology 45:633-662.
Manetas, Y. 2006. Why some leaves are anthocyanic and why most anthocyanic leaves are red? Flora - Morphology, Distribution, Functional Ecology of Plants 201:163-177.
Martin, C., R. C. Hsu, and T.-C. Lin. 2010. Sun/shade adaptations of the
photosynthetic apparatus of Hoya carnosa, an epiphytic CAM vine, in a subtropical rain forest in northeastern Taiwan. Acta Physiologiae
Plantarum 32:575-581.
Maxwell, K. and G. N. Johnson. 2000. Chlorophyll fluorescence—a practical
guide. Journal of Experimental Botany 51:659-668.
Moran, R. 1982. Formulae for determination of chlorophyllous pigments
extracted with N,N-Dimethylformamide. Plant Physiology 69:1376-1381.
Neill, S. and K. S. Gould. 2000. Optical properties of leaves in relation to anthocyanin concentration and distribution. Canadian Journal of Botany 77:1777-1782.
Neill, S. O. and K. S. Gould. 2003. Anthocyanins in leaves: light attenuators or antioxidants? Functional Plant Biology 30:865-873.
Osório, M. L., J. Osório, and A. Romano. 2013. Photosynthesis, energy partitioning, and metabolic adjustments of the endangered Cistaceae species Tuberaria major under high temperature and drought.
Photosynthetica 51:75-84.
Page, J. and N. Towers. 2002. Anthocyanins protect light-sensitive thiarubrine phototoxins. Planta 215:478-484.
Pietrini, F. and A. Massacci. 1998. Leaf anthocyanin content changes in Zea mays L. grown at low temperature: Significance for the relationship
between the quantum yield of PS II and the apparent quantum yield of CO2 assimilation. Photosynthesis Research 58:213-219.
Sherwin, H. and J. Farrant. 1998. Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa.
Plant Growth Regulation 24:203-210.
Smillie, R. M. and S. E. Hetherington. 1999. Photoabatement by anthocyanin shields photosynthetic systems from light stress. Photosynthetica
36:451-463.
Solovchenko, A. 2010. photoprotection in plants : optical screening-based mechanisms. Springer, Berlin.
Sperdouli, I. and M. Moustakas. 2012. Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. Journal of Plant Physiology 169:577-585.
Stapleton, A. E. and V. Walbot. 1994. Flavonoids can protect maize dna from the induction of ultraviolet radiation damage. Plant Physiology 105:881-889.
Steyn, W. J., S. J. E. Wand, D. M. Holcroft, and G. Jacobs. 2002. Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytologist 155:349-361.
Takahashi, A., K. Takeda, and T. Ohnishi. 1991. Light-induced anthocyanin reduces the extent of damage to DNA in uv-irradiated centaurea cyanus cells in culture. Plant and Cell Physiology 32:541-547.
Woodall, G. S. and G. R. Stewart. 1998. Do anthocyanins play a role in UV protection of the red juvenile leaves of Syzygium? Journal of
Experimental Botany 49:1447-1450.