Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species

Abstract

Flower color patterns have long served as a model for developmental genetics because pigment phenotypes are visually striking, yet generally not required for plant viability, facilitating the genetic analysis of color and pattern mutants. The evolution of novel flower colors and patterns has played a key role in the adaptive radiation of flowering plants via their specialized interactions with different pollinator guilds (e.g., bees, butterflies, birds), motivating the search for allelic differences affecting flower color pattern in closely related plant species with different pollinators. We have identified LIGHT AREAS1 (LAR1), encoding an R2R3-MYB transcription factor, as the causal gene underlying the spatial pattern variation of floral anthocyanin pigmentation between two sister species of monkeyflower: the bumblebee-pollinated Mimulus lewisii and the hummingbirdpollinated Mimulus cardinalis. We demonstrated that LAR1 positively regulates FLAVONOL SYNTHASE (FLS), essentially eliminating anthocyanin biosynthesis in the white region (i.e., light areas) around the corolla throat of M. lewisii flowers by diverting dihydroflavonol into flavonol biosynthesis from the anthocyanin pigment pathway. FLS is preferentially expressed in the light areas of the M. lewisii flower, thus prepatterning the corolla. LAR1 expression in M. cardinalis flowers is much lower than in M. lewisii, explaining the unpatterned phenotype and recessive inheritance of the M. cardinalis allele. Furthermore, our gene-expression analysis and genetic mapping results suggest that cis-regulatory change at the LAR1 gene played a critical role in the evolution of different pigmentation patterns between the two species.flower color pattern | Mimulus | anthocyanins | flavonols | R2R3-MYB M any flowers display interesting color patterns (e.g., spots, stripes, picotees, bull's-eyes) that are precisely programmed during development. Numerous studies have shown that these color patterns are critically important for plant-pollinator interactions (1-8). Among the most captivating examples are deceptive orchids that display floral pigment patterns remarkably similar to female bees or wasps to lure male counterparts for pseudocopulation, thereby achieving pollination (9-11). Despite the obvious aesthetic and ecological significance of these flower color patterns, the molecular mechanisms of pigment pattern formation is not well understood, nor is the genetic basis underlying pattern variation between related species in nature.From a genetic and developmental viewpoint, the most extensively studied flower color pattern is venation. Studies in snapdragon (Antirrhinum majus) and petunia (Petunia hybrida) have revealed a conserved mechanism for the formation of vein-associated anthocyanin pigmentation pattern in petal epidermis. Pigments are only produced in the overlapping expression domains of the R2R3-MYB and bHLH coregulators of anthocyanin biosynthetic genes; the bHLH expression is confined to the petal epidermis and the R2R3-MYB expression is specific to ce...

Developmental control of convergent floral pigmentation across evolutionary timescales

“…The range of flavonol production was also broad (0.003 to 3.7 mg/g), with similar ranges between the pigmented (0.05‐3.7 mg/g) and white (0.003‐1.05 mg/g) species. We did not find a significant negative correlation between anthocyanidins and flavonols (Figure ) although this pattern has been observed in experimental systems …”

“…We did not find a significant negative correlation between anthocyanidins and flavonols ( Figure 3) although this pattern has been observed in experimental systems. [39][40][41] The flavonoid profiles of the white morphs of the pigmented species were similar to those of the white species, suggesting the phenotypic convergence is coupled with biochemical convergence. For two of the six polymorphic species (Table 1), the white morphs produced no detectable anthocyanidins ( Figure 2).…”

A dominant‐negative actin mutation alters corolla tube width and pollinator visitation in Mimulus lewisii

“…a,b). It should be noted that the same transformation vector, pEarleyGate 302 (Earley et al ., ), previously has been used to express pigment‐related transgenes in M. lewisii (Yuan et al ., , ), and none of the > 100 transgenic lines generated in previous studies showed a phenotype resembling the ML14257 mutant. Therefore, the current transgenic results clearly support the ‘dominant‐negative’ hypothesis.…”

“…Perhaps a more practical approach to investigate the developmental genetics of corolla tube elaboration is to employ a genetic model plant that has a corolla tube. The bumblebee‐pollinated monkeyflower species Mimulus lewisii is such a model; it has proven to be an excellent system for studying the developmental genetics of ecologically important floral traits, especially those that are difficult or infeasible to study using Arabidopsis (Yuan et al ., , , ; Sagawa et al ., ). As the first step of a systematic effort to elucidate the genetic network underlying corolla tube elaborations, we have generated several ethyl methanesulfonate (EMS) mutants of M. lewisii with altered corolla tube attributes.…”

Chemical analysis of color change and transcriptional profile in flavonoids biosynthesis during flower development of Tibouchina pulchra (Cham.) Cong.

“…Pursh (Scrophulariaceae, Lamiales), and M. cardinalis Douglas ex Benth. flowers (Chiu et al 2010, Pattanaik et al 2010, Yuan et al 2016. In Ipomea purpurea (L.) Roth (Convolvulaceae, Solanales) transposon-insertion double mutants for bHLH and MYB genes resulted in snow-white flowers where the expression of the late biosynthetic genes was completely abolished (Park et al 2007).…”