Complex Pigment Evolution in the Caryophyllales

New Review Phytologist Research review Complex pigment evolution in the Caryophyllales Author for correspondence: Samuel F. Brockington1,2, Rachel H. Walker2, Beverley J. Glover2, Samuel F. Brockington 3 1 Tel: +44 07540460768 Pamela S. Soltis and Douglas E. Soltis Email: [email protected] 1Department of Biology, University of Florida, Gainesville, FL 32611, USA; 2Department of Plant 3 Received: 6 January 2011 Science, University of Cambridge, Cambridge, CB2 3EA, UK; Florida Museum of Natural History, Accepted: 2 February 2011 University of Florida, Gainesville, FL 32611, USA Summary New Phytologist (2011) 190: 854–864 Carotenoids and flavonoids including anthocyanins are the predominant pigments doi: 10.1111/j.1469-8137.2011.03687.x in flowering plants, where they play important roles in pollination, seed dispersal, protection against stress and signalling. In certain families within the Pentapetalae Key words: anthocyanins, betalains, order Caryophyllales, an unusual class of pigments, known as betalains, replaces Caryophyllales, chemotaxonomy, the more common anthocyanins. This isolated occurrence of betalains in the pigmentation. Caryophyllales has stimulated over half a century of debate and experimentation. Numerous hypotheses have been suggested to explain the phylogenetically restricted occurrence of betalains and their apparent mutual exclusion with anthocyanins. In this review, we evaluate these hypotheses in the face of a changing interpretation of Caryophyllales phylogeny and new comparative genetic data. Phylogenetic analyses expose substantial gaps in our knowledge of the early evolution of pigments in the Caryophyllales and suggest pigmentation to be much more labile than previously recognized. Reconstructions of character evolution imply multiple switches from betalain to anthocyanin pigmentation, but also allow for possible multiple origins of betalains. Comparative genetic studies propose possible mechanisms underlying switches between pigment types and suggest that tran- scriptional down-regulation of late-acting enzymes is responsible for a loss of anthocyanins. Given these insights from molecular phylogenetics and comparative genetics, we discuss outstanding questions and define key goals for future research. structurally and biosynthetically distinct from flavonoids and Introduction anthocyanins, and appear to have evolved at least twice: once Pigments perform critical roles in the biology of angio- within a fungal lineage – the Basidiomycetes; and once sperms, where they act as visible signals to attract fauna for within a flowering plant order – the core Caryophyllales pollination and seed dispersal, protect plants from light (Bischoff, 1876; Mabry, 1964) (see Fig. 1). The core damage, phytopathogens and heavy metals, and are involved Caryophyllales is a well-defined clade of eudicots comprising in internal signalling (reviewed by Koes et al., 2005). c. 29 families and c. 9000 species (APG, 2003). In betalain- Flavonoids, including anthocyanins, are widely distributed producing families within the core Caryophyllales, anthocya- across angiosperms, where they are responsible for the nins have never been detected (Bate-Smith, 1962; Mabry, colouration found in flowers, leaves, fruit and seeds (Tanaka 1964), indicating that betalain pigmentation substitutes for et al., 2008) (see Fig. 1). Betalains are pigments that are the otherwise ubiquitous anthocyanins. However, in two 854 New Phytologist (2011) 190: 854–864 Ó 2011 The Authors www.newphytologist.com New Phytologist Ó 2011 New Phytologist Trust New Phytologist Research review Review 855 (a) (b) before the radiation of major pollinator lineages. In this open, pollinator-deprived environment, wind pollination may have prevailed, and anthocyanin pigmentation was lost as there was no need to attract pollinators. Subsequently, following the radiation of pollinator lineages and the colo- nization of less marginal habitats, reversion to zoophily engendered a return to pigmentation in the form of betalains rather than anthocyanins (Ehrendorfer, 1976). This hypothesis is difficult to evaluate (Clement & Mabry, 1996) and the phylogenetic concept of Caryophyllales has Fig. 1 Similar hues, different pigments. (a) Anthocyanin changed considerably since Ehrendorfer (1976). Some pigmentation in Antirrhinum majus. (b) Betalain pigmentation in morphological features of extant Caryophyllales are consistent Mirabilis jalapa. with a wind-pollinated ancestor, including an ancestrally uniseriate undifferentiated flower (i.e. a perianth of one families in the core Caryophyllales, the Molluginaceae and organ type rather than differentiated sepals and petals); Caryophyllaceae, anthocyanins are produced instead of beta- however, several newly placed lineages (Rhabdodendron, lains, suggesting that anthocyanins and betalains are Asteropeia, Macarthuria) suggest that entomophily may be mutually exclusive pigment types (Mabry, 1964). the ancestral state (Brockington et al., 2009). Furthermore, The novel origin of betalains within the core Caryophyllales because anthocyanins and betalains accumulate and and their mutual exclusion with anthocyanins have stimu- function in both vegetative and reproductive tissues, it is lated over half a century of debate in the fields of taxonomy unreasonable to explain the evolutionary changes in and systematics, phytochemistry and evolutionary biology. pigmentation as a result of the absence or presence of In this article, we examine the scope and limitations of pollinators alone (reviewed in Whittall & Strauss, 2006). existing hypotheses that have been proposed to explain There are few competing explanations for the unique presence the complex patterns of pigment variation in the core of betalains in the core Caryophyllales; however, Stafford Caryophyllales. We review the state of knowledge regarding (1994) suggested possible horizontal transfer of genes from the biosynthesis and regulation of anthocyanin and betalain betalain-pigmented Basidiomycetes – an intriguing if pigmentation, review insights from recent studies that take improbable scenario that cannot yet be ruled out. a comparative genetic approach to betalain and anthocyanin synthesis, assess the impact of recent molecular phylogenetic The presence of both betalain and anthocyanin analyses on the reconstruction of pigment evolution and lineages identify key questions and hypotheses for future research. To explain the presence of both betalain and anthocyanin The scope and limitations of existing lineages, Clement & Mabry (1996) suggested that the two hypotheses compounds may have co-occurred in an ancestor to the core Caryophyllales. The two pigments might have been selectively Several hypotheses have been proposed to explain the evolu- maintained in ancestors of extant Caryophyllales, with the sub- tion of betalain pigmentation; however, explanations of sequent loss of one or other of the pigments in extant pigment evolution in the core Caryophyllales must be able lineages. Clement & Mabry (1996) did not identify the to account for the following three phenomena: (1) the nature of the selection maintaining this co-occurrence, or its unique derived origin of betalain pigmentation; (2) the loss, but betalains may have evolved as a result of their fungi- presence of both anthocyanin-pigmented and betalain- cidal properties (Mabry, 1980; Piatelli, 1981), rather than pigmented lineages in the core Caryophyllales; and (3) the pigmentation; thus, the two pigments could have co-existed mutual exclusivity of the two pigment types. As discussed as a result of the complementary pigmentation and anti- below, many of the hypotheses that have been advanced to fungal properties. The most significant objection to this date are not mutually exclusive, but none alone adequately hypothesis is that no taxon has been identified that contains explains these three phenomena. both anthocyanins and betalains, which is surprising if they are complementary in function. It remains possible that the two pigment types co-exist in unexplored taxa; however, the The unique origin of betalains maintenance of both pigments in a common ancestor does Ehrendorfer (1976) argued that the unique presence of not provide mechanisms for their ultimate mutual exclusion. betalains in Caryophyllales was the consequence of an Clement & Mabry (1996) referred to the ‘stochastic loss’ of unusual evolutionary history, in which the ancestor to one or other pigment in extant lineages, but did not provide Caryophyllales evolved in arid to semi-arid conditions specific mechanisms to explain the loss of a pigment. Ó 2011 The Authors New Phytologist (2011) 190: 854–864 New Phytologist Ó 2011 New Phytologist Trust www.newphytologist.com New 856 Review Research review Phytologist The mutual exclusion of anthocyanins and betalains Anthocyanins Additional hypotheses are needed to explain the mutual Phenylalanine Cinnamic acid p-coumaric acid exclusion of these pigment types and ⁄ or the replacement of PAL C4H 4CL one pigment type with another. Clement & Mabry (1996) explored the relative metabolic cost of betalain and anthocyanin synthesis, but reached no clear conclusions, in part 3 Malonyl-CoA p-coumaroyl-CoA because the full physiological roles of anthocyanins and CHS betalains are not thoroughly understood, and in part because true metabolic costs are not easily assessed. The relative effectiveness of the pigments has also been discussed Tetrahydroxychalcone in terms of molar absorptivity, with the suggestion that CHI much smaller amounts of

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