Light Emission in Betalains: From Fluorescent Flowers to Biotechnological Applications

Abstract

The discovery of visible fluorescence in the plant pigments betalains revealed the existence of fluorescent patterns in flowers of plants of the order Caryophyllales, where betalains substitute anthocyanins. The serendipitous initial discovery led to a systemized characterization of the role of different substructures on the photophysical phenomenon. Strong fluorescence is general to all members of the family of betaxanthins linked to the structural property that the betalamic acid moiety is connected to an amine group. This property has led to bioinspired tailor-made probes and to the development of novel biotechnological applications in screening techniques or microscopy labeling. Here, we comprehensively review the photophysics, photochemistry, and photobiology of betalain fluorescence and describe all current applications. BetalainsBetalains are nitrogenous plant pigments that are characteristic for plants belonging to the order Caryophyllales. These pigments are divided into the yellow betaxanthins and the violet betacyanins [1]. The presence of both types of pigments is required for the orange and red colors that coexist in nature with the pure yellow and violet colors. Betalains substitute anthocyanins and play their roles in the colored tissues of most plant families of the Caryophyllales. Both families of pigments are watersoluble and mutually exclusive [2,3]. Numerous studies were performed on the color properties of betalains since they were described as a novel family of pigments, different to 'nitrogenous anthocyanins' [4,5]. However, it was not until 2005 that their natural fluorescence was discovered [6]. In addition, it was demonstrated that under physiological conditions, light emission was exhibited in the plant tissues that contain them, including flowers [7,8].Among the Caryophyllales plants, red beet roots (Beta vulgaris) and the fruits of cacti belonging to the genus Opuntia are the best known sources of betalains, with betanin and indicaxanthin being, respectively, their main pigments [9,10]. Current research has described the betalain content of novel sources, such as the tubers from Ullucus tuberosus [11] or the betalain-containing berries of Rivina humilis [12]. Also, the multiple shades of quinoa grains (Chenopodium quinoa) have recently been reported to be based on betacyanins and betaxanthins [13]. In addition, betalains have in recent years been shown to have promising bioactive properties. Early investigations revealed a strong free radical scavenging capacity of betalains purified from beet root [14]. Subsequent research revealed the existence of an intrinsic activity, present in all betalains, that is modulated by structural factors [15,16]. Furthermore, studies with different human cancer cell lines have demonstrated the potential of betalains in the chemoprevention of cancer [17,18]. In vivo experiments have shown that very low concentrations of dietary pigments inhibit the formation of tumors in mice [19,20] and extend the lifespan of the model animal Caenorhabditis elegans [21...

Biological Properties and Applications of Betalains

“…A more pronounced hypsochromic effect is observed in neobetanin (CAS 71199-29-6 = 14,15-dehydrobetanin), which is orange and not violet [ 67 ]. The same effect is found in betaxanthins: a hypsochromic shift occurs upon decarboxylation of portulacaxanthin II (CAS 135545-98-1) and dopaxanthin [ 68 ].…”

“…The existence of intramolecular hydrogen bonds constrains the dynamics of the molecule, favorizing certain structures, as it occurs in miraxanthin I (CAS 5296-79-7). This phenomenon decreases the radiationless energy losses and contributes to the high fluorescence quantum yield of miraxanthin I molecule ( Table S4 ), recognized as the most fluorescent natural betaxanthin [ 68 ].…”

Virus-Mediated Transient Expression Techniques Enable Functional Genomics Studies and Modulations of Betalain Biosynthesis and Plant Height in Quinoa

“…Although betalains have attracted attention in recent years as plant pigments with promising health-promoting potential and visible fluorescence (Gandía-Herrero et al, 2016;Guerrero-Rubio et al, 2020), research on quinoa betalains has only recently begun. A previous mutant analysis indicated that CqCYP76AD1 functions in betalain accumulation during the hypocotyl pigmentation process in quinoa (Imamura et al, 2018).…”

“…The relative betacyanin contents were estimated spectrophotometrically based on absorbance at 536 nm (Imamura et al, 2019;Guerrero-Rubio et al, 2020). UV-Vis spectra were acquired using a DeNovix DS-11 (DeNovix, Wilmington DE, United States) spectrophotometer.…”

Elucidation of the Core Betalain Biosynthesis Pathway in Amaranthus tricolor

“…An increased understanding of the betalain biosynthesis pathway has facilitated the metabolic engineering of betalains, providing new sources for basic research studies and commercial applications 22,23 . For example, the uorescent betaxanthins produced by the expression of MjDODAa1 in yeast were used as chemical biosensors to reveal the tyrosine hydroxylase activity of BvCYP76AD1 15 .…”