Pigment Evolution in the Caryophyllales: a Systematic Overview*

Abstract

While the apparent mutual exclusiveness of anthocyanins and betalains in the Caryophyllales has given rise to considerable taxonomic debate, historical factors affecting the present distribution of these compounds have rarely been discussed. An understanding of pigment evolution in the order is hindered by a number of unresolved systematic issues and a lack of knowledge of the importance of anthocyanins and betalains beyond their roles in pollination and seed dispersal. The hypothesis that betalains arose in an unpigmented ancestor of the Chenopodiinae in response to selection from pollinators cannot be rejected, but scant evidence exists in favor of it. Questions persist regarding whether the most recent ancestor to the Chenopodiinae presented a pigmented floral display and whether the appropriate pollinators were present at this time to select for floral pigmentation. In view of these ambiguities and the possible non-monophyly of the Chenopodiinae we consider some alternative scenarios and suggest potentially rewarding avenues for future research. We discuss roles for anthocyanins and betalains beyond their use as optical attractants, possible costs and benefits associated with producing each pigment type, and the possibility that they may have cooccurred in an ancestor for some period of time.

Phylogeny of the Caryophyllales Sensu Lato: Revisiting Hypotheses on Pollination Biology and Perianth Differentiation in the Core Caryophyllales

“…Consequently, he argued that anemophily was the ancestral condition because the early Caryophyllales had evolved in open, dry, marginal environments at a time when pollinators were scarce. These hypotheses are difficult to prove or disprove (Clement and Mabry 1996); however, our phylogeny confirms that the Amaranthaceae constitute a relatively derived lineage. If pollinators were scarce at the time of origin of the Caryophyllales, this might also apply as a general limitation to other lineages of eudicots diverging at that time, but in any case, the relative timing and location of diversification in eudicot lineages and their respective pollinator lineages are unclear at present.…”

“…Coding Physena as wind pollinated, however, does not alter the conclusion of the character mapping analyses, and thus there is little support for an anemophillous ancestry in the core Caryophyllales. Indeed, as noted by Clement and Mabry (1996), even if one accepts the highly reduced inconspicuous flowers of Amaranthaceae s.l. as archetypal, it is not necessary to invoke wind pollination because it has already been noted that many of the diminutive flowers in Amaranthaceae are probably entomophilous (Blackwell and Powell 1981;Kuhn 1993).…”

Characterization and Functional Identification of a Novel Plant 4,5-Extradiol Dioxygenase Involved in Betalain Pigment Biosynthesis in Portulaca grandiflora

“…Betalains are also present in some basidiomycete fungi belonging to the Amanita and Hygrocybe genera. Betalains provide a key taxonomic criterion in our understanding of Caryophyllales evolution (Cuenoud et al, 2002); the origin of the alternative pigment biosynthetic pathway is still unknown (Clement and Mabry, 1996), and the purpose of our work is to provide, through the characterization of a key biosynthetic enzyme, one element of the answer to this problem.Information on the biochemistry and genetics of the plant betalain pathway is scarce. Genetic analysis of the betalain biosynthetic pathway in the ornamental plant Portulaca grandiflora (Pg) indicates that four structural genes would be sufficient to account for the different color phenotypes observed in petals (Trezzini and Zrÿ d, 1990).…”

“…Betalains are also present in some basidiomycete fungi belonging to the Amanita and Hygrocybe genera. Betalains provide a key taxonomic criterion in our understanding of Caryophyllales evolution (Cuenoud et al, 2002); the origin of the alternative pigment biosynthetic pathway is still unknown (Clement and Mabry, 1996), and the purpose of our work is to provide, through the characterization of a key biosynthetic enzyme, one element of the answer to this problem.…”

Characterization of major betalain pigments -gomphrenin, betanin and isobetanin from Basella rubra L. fruit and evaluation of efficacy as a natural colourant in product (ice cream) development

“…Betalains and anthocyanins are the most important water soluble pigments in nature but never been found in the same plant (Stafford 1998). Betalains are nitrogen containing plant pigment which replaces anthocyanins in flowers and fruits of plants of family Caryophyllales (Clement and Mabry 1996). The other sources of betalains are beet root, Gomphrena globosa flowers, amaranth plant, Rivina humilis fruits and cactus fruits (Lin et al 2010;Khan et al 2012;Khan and Giridhar 2014a).…”