Anthocyanins have become sought-after natural products due to potential for medicinal and industrial uses. These metabolites have a number of health-promoting properties; increasing demand for nutraceuticals, fruits, and vegetables containing anthocyanins (Deroles, 2009; He and Giusti, 2010; Wrolstad and Culver, 2012). Production of textiles, cosmetics, and solar panels are examples of industrial applications where anthocyanins are also being increasingly used to replace synthetic dyes (Hao et al., 2006; Mansour et al., 2013; Wongcharee et al., 2007).
The use of anthocyanin extracts for the above applications is limited by the small number plant sources of anthocyanins as well as the cultural limitations of these species: annual life cycle, slow growth, limited harvest, high input, etc. (Deroles, 2009). The use of plant tissue culture has been proposed as a means of large-scale anthocyanin production; however, to date, these techniques have not been able to produce anthocyanins at levels sufficient to meet current industrial needs (Delgado-Vargas, 2000; Vogelien et al., 1990; Yamamoto and Mizuguchi, 1982). One way to meet the increasing demand for anthocyanins is to employ nonconventional plant species, such as poaceous grasses. The anatomy and perennial nature of turfgrasses make them attractive anthocyanin production systems.
Turfgrasses accumulate anthocyanins in leaves that originate from meristematic tissues that sit at or below the soil surface (Christians, 2011). Leaf tissue can therefore be harvested while keeping meristematic tissues intact, allowing for year-round production from the same stand of plants. Cool-season turfgrasses (C3 photosynthetic) devote greater than 60% of photosynthate toward leaf and sheath growth, and the potential yield of anthocyanin-containing tissue could be upwards of 3 Mg·ha−1 after a single harvest (Krans and Beard, 1980; Landschoot and Waddington, 1987; Younger, 1969). Relative to fruit crops, currently the most used anthocyanin source, turfgrasses provide numerous advantages. For example, turfgrasses could be harvested for anthocyanins within weeks of seeding, and leaf tissue could be harvested at least once per month. Further, since turfgrasses do not undergo secondary growth, a greater proportion of photosynthate could be devoted toward anthocyanin synthesis.
Rough bluegrass (P. trivialis L.) is known to constitutively produce the anthocyanins cyanidin-3-glucoside and cyanidin-3-malonylglucoside in the leaf sheath (Fossen et al., 2002; Hurley, 2010). This turfgrass is a fast-growing perennial under field conditions, and high tissue yield could therefore be expected (Atkin et al., 1996). Still, to employ this species as an industrial crop, it would be necessary to increase anthocyanin production in rough bluegrass to levels greater than those currently observed in the field. Environmental stress, light in particular, is one factor that is known to increase anthocyanin synthesis (Boldt et al., 2014).
Transient anthocyanin accumulation occurs with changes in light quantity and/or quality, and has been documented in a variety of plants including: tomato, Arabidopsis, maize, sorghum, rye, red cabbage, and mustard (Chalker-Scott, 1999; Mancinelli, 1985; Mol et al., 1996). Light is a requirement for anthocyanin synthesis, and anthocyanin production is photoregulated (Downs and Siegelman, 1963; Lange et al., 1971; Mancinelli, 1985; Rabino et al., 1977; Vyas et al., 2014). Photomanipulation could therefore be used to increase anthocyanin content in rough bluegrass.
Phytochrome has been shown to regulate anthocyanin synthesis through the absorption of red or far-red (FR) light (Kerckhoffs and Kendrick, 1997; Mancinelli, 1985; Neff and Chory, 1998; Oh et al., 2014; Wade et al., 2001). However, blue light also regulates anthocyanin synthesis, although this is accomplished through the activity of multiple photoreceptors, including both cryptochromes and phototropins (Galvão and Frankhauser, 2015). Cryptochromes are well known to regulate anthocyanin synthesis, whereas phototropins have only been recently implicated in anthocyanin regulation (Folta and Carvalho, 2015; Fox et al., 2012; Hong et al., 2009; Kadomura-Ishikawa et al., 2013; Poppe et al., 1998; Vandenbussche et al., 2007).
Treatment with red and blue light may also increase anthocyanin synthesis through photoreceptor coaction. In other words, red light may be noninductive on its own, but when applied with blue light, anthocyanin synthesis may be increased compared with blue light alone (Drumm and Mohr, 1978; Mancinelli, 1985; Mohr and Drumm-Herrel, 1983; Wade et al., 2001). In addition, anthocyanin synthesis has also been shown to be regulated through photosynthesis and increased under high-intensity light (Kumar Das et al., 2011; Mancinelli et al., 1976; Mancinelli and Rabino, 1978; Mancinelli, 1985; Schneider and Stimson, 1971; Weiss and Halevy, 1991). Therefore, anthocyanin content may increase through a combination of photosynthetic and photoreceptor-mediated regulation when blue, red, and/or combinations of blue and red light are applied.
Given the previously established regulation of anthocyanin synthesis in several monocot crops (i.e., sorghum and maize), we hypothesized that anthocyanin production in rough bluegrass could be manipulated through exposure to specific light regimes. The objectives of this research were to determine conditions that favor anthocyanin synthesis in rough bluegrass by first evaluating whether treatment with high-intensity light could increase anthocyanin content. Second, the wavelength(s) of light capable of upregulating anthocyanin synthesis was determined to optimize light conditions. Finally, the role of photosynthesis on anthocyanin production in rough bluegrass was evaluated.
Atkin, O.K., Botman, B. & Lambers, H. 1996 The causes of inherently slow growth in alpine plants: An analysis based on the underlying carbon economies of alpine and lowland Poa species Funct. Ecol. 10 6 698 707
Boldt, J.K. 2013 Foliar anthocyanins in coleus and ornamental grasses: Accumulation, localization, and function. Univ. of Minnesota, Minneapolis, MN, PhD. Diss
Boldt, J.K., Meyer, M.H. & Erwin, J.E. 2014 Foliar anthocyanins: A horticultural review, p. 209–251. In: J. Janick (ed.). Hort. Rev. Wiley, New York, NY
Christians, N.E. 2011 Chapter 2: Introduction to the grasses, p. 9–31. In: N.E. Christians (ed.). Fundamentals of turfgrass management. 4th ed. Wiley, New York, NY
Delgado-Vargas, F., Jiménez, A.R. & Paredes-López, O. 2000 Natural pigments: Carotenoids, anthocyanins, and betalains: Characteristics, biosynthesis, processing, and stability Crit. Rev. Food Sci. Nutr. 40 3 173 289
Del Pozo-Insfran, D., Brenes, C.H. & Taloctt, S.T. 2004 Phytochemical composition and pigment stability of acai (Euterpe oleracea Mart.) J. Agr. Food Chem. 52 1539 1545
de Pascual-Teresa, S., Santos-Buelga, C. & Rivas-Gonzalo, J.C. 2002 LC-MS analysis of anthocyanins from purple corn cob J. Sci. Food Agr. 82 1003 1006
Deroles, S. 2009 Anthocyanin biosynthesis in plant cell cultures: A potential source of natural colourants, p. 107–168. In: K. Gould, K. Davies, and C. Winfield (eds.). Anthocyanins: Biosynthesis, functions, and applications. Springer-Verlag, New York, NY
Drumm, H. & Mohr, H. 1978 The mode of interaction between blue (UV) light photoreceptor and phytochrome in anthocyanin formation of the Sorghum seedling Photochem. Photobiol. 27 241 248
Fox, A.R., Soto, G.C., Jones, A.M., Casal, J.J., Muschietti, J.P. & Mazzella, M.A. 2012 Cry1 and GPA1 signaling genetically interact in hook opening and anthocyanin synthesis in Arabidopsis Plant Mol. Biol. 20 315 324
Galvão, V.C. & Frankhauser, C. 2015 Sensing the light environment in plants: Photoreceptors and early signaling steps Curr. Opin. Neurobiol. 34 46 53
Giusti, M. & Wrolstad, R.E. 2001 Characterization and measurement of anthocyanins by UV-visible spectroscopy Curr. Protoc. Food Anal. Chem. 2 1 13
Hong, G., Hu, W., Li, J., Chen, Z. & Wang, L. 2009 Increased accumulation of artemisinin and anthocyanins in Artemisia annua expressing Arabidopsis blue light receptor CRY1 Plant Mol. Biol. Rpt. 27 334 341
Hughes, N.M., Morley, C.B. & Smith, W.K. 2007 Coordination of anthocyanin decline and photosynthetic maturation in juvenile leaves of three deciduous tree species New Phytol. 175 675 685
Hughes, N.M., Carpenter, K.L. & Cannon, J.G. 2013 Estimating contribution of anthocyanin pigments to osmotic adjustment during leaf reddening J. Plant Physiol. 170 230 233
Hurley, R. 2010 Rough bluegrass (Poa trivialis L.), p. 67–73. In: M.D. Casler and R.R. Duncan (eds.). Turfgrass biology, genetics, and breeding. Wiley, New York, NY
Jeong, S., Kumar Das, P., Jeoung, S.C., Song, J., Lee, H.K., Kim, Y., Kim, W.J., Park, Y.I., Yoo, S., Choi, S., Choi, G. & Park, Y. 2010 Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis Plant Physiol. 154 1514 1531
Kadomura-Isikawa, Y., Miyawaki, K., Noji, S. & Takahashi, A. 2013 Phototropin 2 is involved in blue light-induced anthocyanin accumulation in Fragaria x ananassa fruits J. Plant Res. 126 847 857
Krans, J.V. & Beard, J.B. 1980 The effects of stage of seedling development on selected physiological and morphology parameters in Kentucky bluegrass and red fescue, p. 89–95. Proc. of the Third Intl. Turfgrass Res. Conf. Amer. Soc. of Agron., Crop Sci. Soc. of Amer., Soil Sci. Soc. of Amer., and the Intl. Turfgrass Soc
Kumar Das, P., Geul, B., Choi, S., Yoo, S. & Park, Y. 2011 Photosynthesis-dependent anthocyanin pigmentation in Arabidopsis Plant Signal. Behav. 6 1 23 25
Lin-Wang, K., Micheletti, D., Palmer, J., Voltz, R., Lozano, L., Espley, R., Hellens, R.P., Chagne, D., Rowan, D.D., Troggio, M.A., Iglesias, I. & Allan, A.C. 2011 High temperature reduces apple fruit color via modulation of the anthocyanin regulatory network Plant Cell Environ. 34 1176 1190
Mancinelli, A.L. 1985 Light-dependent anthocyanin synthesis: A model system for the study of plant photomorphogenesis Bot. Rev. 51 1 107 157
Mancinelli, A.L., Yang, C.H., Rabino, I. & Kuzmanoff, K.M. 1976 Photocontrol of anthocyanin synthesis: V. Further evidence against the involvement of photosynthesis in high irradiance reaction anthocyanin synthesis of young seedlings Plant Physiol. 58 241 217
Mansour, R., Ezzili, B. & Farouk, M. 2013 Dyeing properties of wool fabrics dyes with Vitis vinifera L. (Black Grenache) leaves extract Fibers Polym. 14 5 786 792
Merzylak, M.N., Chivkunova, O.B., Solovchenko, A.E. & Naqvi, K.R. 2008 Light absorption by anthocyanins in juvenile, stressed, and senescing leaves J. Expt. Bot. 59 14 3903 3911
Mohr, H. & Drumm-Herrel, H. 1983 Coaction between phytochrome and blue/UV light in anthocyanin synthesis in seedlings Physiol. Plant. 58 408 414
Mol, J., Jenkins, G., Schäfer, E., Weiss, D. & Walbot, V. 1996 Signal perception, transduction, and gene expression involved in anthocyanin biosynthesis. Crit. Rev. Plant Sci. 15(5–6):525–557
Nangle, E.J., Gardner, D.S., Metzger, J.D., Rodriquez-Saona, L., Giusti, M.M., Danneberger, T.K. & Petrella, D.P. 2015 Pigment changes in cool-season turfgrasses in response to ultraviolet-B light Agron. J. 107 1 41 50
Neff, M.M. & Chory, J. 1998 Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development Plant Physiol. 118 27 36
Oh, S., Warnasooriya, S.N. & Montgomery, B.L. 2014 Mesophyll-localized phytochromes gate stress- and light-inducible anthocyanin accumulation in Arabidopsis thaliana Plant Signal. Behav. 9 1 9
Poppe, C., Sweere, U., Drumm-Herrel, H. & Schäfer, E. 1998 The blue light receptor cryptochrome 1 can interact independently of phytochrome A and B in Arabidopsis thaliana Plant J. 16 4 466 471
Rabino, I., Mancinelli, A.L. & Kuzmanoff, K.M. 1977 Photocontrol of anthocyanin synthesis: VI. Spectral sensitivity, irradiance dependence, and reciprocity relationship Plant Physiol. 59 569 573
Schneider, M.J. & Stimson, W.R. 1971 Contribution of photosynthesis and phytochrome to the formation of anthocyanin in turnip seedlings Plant Physiol. 48 312 315
U.S. Department of Agriculture 2015 Noncitrus fruits and nuts 2014 summary. US. Dept. of Agr., Washington, DC
Vandenbussche, F., Habricot, Y., Condiff, A.S., Maldiney, R., Van Der Straeten, D. & Ahmad, M. 2007 HY5 is a point of convergence between cryptochrome and cytokinin signaling pathways in Arabidopsis thaliana The Plant J. 49 428 441
Vyas, P., Haque, I. & Kumar, M. 2014 Photocontrol of differential gene expression and alterations in foliar anthocyanin accumulation: A comparative study using red and green forma Ocimum tenuiflorum Acta Physiol. Plant. 36 2091 2102
Wade, H.K., Bibikova, T.N., Valentine, W.J. & Jenkins, G.I. 2001 Interactions within a network of phytochrome, cryptochrome and UV-B phototransduction pathways regulate chalcone synthase gene expression in Arabidopsis leaf tissue Plant J. 25 6 675 685
Weiss, D. & Halevy, A.H. 1991 The role of light reactions in the regulation of anthocyanin synthesis in Petunia corollas Physiol. Plant. 81 127 133
Wellburn, A.R. 1994 The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution J. Plant Physiol. 144 307 313
Wongcharee, K., Meeyoo, V. & Chavadej, S. 2007 Dye-sensitized solar cell using natural dyes extracted from rosella and blue pea flowers Sol. Energy Mater. Sol. Cells 91 566 571
Wu, X., Beecher, G.R., Holden, J.M., Hautowitz, D.B., Gebhardt, S.E. & Prior, R.L. 2006 Concentrations of anthocyanins in common foods consumed in the United States and estimation of normal consumption J. Agr. Food Chem. 54 4069 4075
Yamamoto, Y. & Mizuguchi, R. 1982 Selection of a high and stable pigment-producing strain in cultured Euphorbia millii cells Theor. Appl. Genet. 61 113 116
Yamane, T., Tae Jeong, S., Goto-Yamamoto, N., Koshita, Y. & Kobayashi, S. 2006 Effects of temperature on anthocyanin biosynthesis in grape berry skins Amer. J. Enol. Viticult. 57 1 54 59
Younger, V.B. 1969 Physiology of growth and development, p. 187–216. In: A.A. Hanson and F.V. Juska (eds.). Turfgrass Science. Amer. Soc. of Agron. Madison, WI