How to make a red flower: the combinatorial effect of pigments

Ng, Julienne; Smith, Stacey D.

doi:10.1093/aobpla/plw013

Cited by 36 publications

(31 citation statements)

References 91 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…2b). This chemical prole would likely result in red or pink oral coloration (Ng and Smith 2016a;Smith and Rausher 2011).…”

Section: Resultsmentioning

confidence: 99%

Computational modeling of anthocyanin pathway evolution

Wheeler

Smith²

2019

Preprint

Self Cite

View full text Add to dashboard Cite

Alteration of metabolic pathways is a common mechanism underlying the evolution of new phenotypes. Flower color is a striking example of the importance of metabolic evolution in a complex phenotype, wherein shifts in the activity of the underlying pathway lead to a wide range of pigments. Although experimental work has identied common classes of mutations responsible for transitions among colors, we lack a unifying model that relates pathway function and activity to the evolution of distinct pigment phenotypes. One challenge in creating such a model is the branching structure of pigment pathways, which may lead to evolutionary trade-os due to competition for shared substrates. In order to predict the eects of shifts in enzyme function and activity on pigment production, we created a simple kinetic model of a major plant pigmentation pathway:the anthocyanin pathway. This model describes the production of the three classes of blue, purple and red anthocyanin pigments, and accordingly, includes multiple branches and substrate competition. We rst studied the general behavior of this model using a naïve set of parameters. We then stochastically evolved the pathway toward a dened optimum and analyzed the patterns of xed mutations. This approach allowed us to quantify the probability density of trajectories through pathway state space and identify the types and number of changes. Finally, we examined whether our simulated results qualitatively align with experimental observations, i.e., the predominance of mutations which change color by altering the function of branching genes in the pathway. These analyses provide a theoretical framework that can be used to predict the consequences of new mutations in terms of both pigment phenotypes and pleiotropic eects.We thank members of the Smith lab for useful conversations regarding implementation and interpretation of our computational model. We thank Jacob Stanley and Rutendo Sigauke in the Dowell group at CU Boulder for helpful conversations regarding development of the simulation framework and appropriate implementation of the subsequent analyses. We also thank Boswell Wing, Sebastian Kopf, and the other members of the CU Boulder Geobiology Super Group for their helpful feedback.

show abstract

“…2b). This chemical prole would likely result in red or pink oral coloration (Ng and Smith 2016a;Smith and Rausher 2011).…”

Section: Resultsmentioning

confidence: 99%

Computational modeling of anthocyanin pathway evolution

Wheeler

Smith²

2019

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…In addition, comparative studies have shown that red‐coloured flowers can result from various combinations of pigments (e.g. purple anthocyanins plus orange carotenoids; Ng & Smith, ,b), providing multiple pathways for evolutionary transitions among colours.…”

Section: Discussionmentioning

confidence: 99%

“…These independent origins of red flowers have involved at least three different developmental mechanisms and two distinct pigment pathways (Ng & Smith, 2016a). Specifically, red flower coloration can be due to the presence of anthocyanin pigments, carotenoid pigments or the production of both (Ng & Smith, 2016b). The potential for producing red flowers via multiple types of genetic and biochemical changes may help to explain the evolutionary lability of this trait, with many gains and losses (Perret et al, 2003;Tripp & Manos, 2008), as well as the widespread convergence on this colour across angiosperms (Cronk & Ojeda, 2008).…”

Section: Introductionmentioning

confidence: 99%

Why are red flowers so rare? Testing the macroevolutionary causes of tippiness

Smith

2018

J of Evolutionary Biology

Self Cite

View full text Add to dashboard Cite

Traits that have arisen multiple times yet still remain rare present a curious paradox. A number of these rare traits show a distinct tippy pattern, where they appear widely dispersed across a phylogeny, are associated with short branches and differ between recently diverged sister species. This phylogenetic pattern has classically been attributed to the trait being an evolutionary dead end, where the trait arises due to some short‐term evolutionary advantage, but it ultimately leads species to extinction. While the higher extinction rate associated with a dead end trait could produce such a tippy pattern, a similar pattern could appear if lineages with the trait speciated slower than other lineages, or if the trait was lost more often that it was gained. In this study, we quantify the degree of tippiness of red flowers in the tomato family, Solanaceae, and investigate the macroevolutionary processes that could explain the sparse phylogenetic distribution of this trait. Using a suite of metrics, we confirm that red‐flowered lineages are significantly overdispersed across the tree and form smaller clades than expected under a null model. Next, we fit 22 alternative models using HiSSE (Hidden State Speciation and Extinction), which accommodates asymmetries in speciation, extinction and transition rates that depend on observed and unobserved (hidden) character states. Results of the model fitting indicated significant variation in diversification rates across the family, which is best explained by the inclusion of hidden states. Our best fitting model differs between the maximum clade credibility tree and when incorporating phylogenetic uncertainty, suggesting that the extreme tippiness and rarity of red Solanaceae flowers makes it difficult to distinguish among different underlying processes. However, both of the best models strongly support a bias towards the loss of red flowers. The best fitting HiSSE model when incorporating phylogenetic uncertainty lends some support to the hypothesis that lineages with red flowers exhibit reduced diversification rates due to elevated extinction rates. Future studies employing simulations or targeting population‐level processes may allow us to determine whether red flowers in Solanaceae or other angiosperms clades are rare and tippy due to a combination of processes, or asymmetrical transitions alone.

show abstract

“…(). Given that flower color is preserved in herbarium specimens, we also sampled flowers from several collections () as in Ng and Smith (). In addition, we conducted a comprehensive literature search to collect previously published data on floral anthocyanin composition in Solanaceae ().…”

Section: Methodsmentioning

confidence: 99%

“…). Among the three types, those derived from delphinidin appear to be the most commonly produced in floral tissue, followed by cyanidin and pelargonidin (Ng and Smith ). The wide phylogenetic distribution of taxa with similar pigment profiles suggests that shifts in anthocyanin production have occurred multiple times in the family, providing the foundation for modeling evolutionary transitions.…”

mentioning

confidence: 99%

Stepwise evolution of floral pigmentation predicted by biochemical pathway structure

Freitas

Smith

2018

Evolution

Self Cite

View full text Add to dashboard Cite

Developmental pathways play a major role in influencing the distribution of naturally occurring phenotypes. For example, pathway structure and regulation could make some phenotypes inaccessible or restrict the routes through which phenotypes evolve. In this study, we examine floral anthocyanin pigments across the Solanaceae family and test whether patterns of phenotypic variation are consistent with predicted constraints based on the structure of the flavonoid biosynthetic pathway. We find that anthocyanin evolution occurs in a stepwise manner whereby transitions between the production of red mono hydroxylated pelargonidin pigments and blue trihydroxylated delphinidin pigments first passes through an intermediate step of producing purple dihydroxylated cyanidin pigments. Although the transitions between these three pigment types differ in frequency, we infer that these shifts are often reversible, suggesting that the functionality of the underlying biochemical pathway is generally conserved. Furthermore, our study finds that some pigment combinations are never observed, pointing to additional constraints on naturally occurring phenotypes. Overall, our findings provide insights into how the structure of an angiosperm-wide biochemical pathway has shaped macroevolutionary variation in floral pigmentation.

show abstract

How to make a red flower: the combinatorial effect of pigments

Cited by 36 publications

References 91 publications

Computational modeling of anthocyanin pathway evolution

Computational modeling of anthocyanin pathway evolution

Why are red flowers so rare? Testing the macroevolutionary causes of tippiness

Stepwise evolution of floral pigmentation predicted by biochemical pathway structure

Contact Info

Product

Resources

About