Different outcomes for the MYB floral symmetry genes DIVARICATA and RADIALIS during the evolution of derived actinomorphy in Plantago

Abstract

Summary The gene network that specifies flower shape in Antirrhinum majus (bilateral floral symmetry or zygomorphy) includes two MYB‐class genes – RADIALIS (RAD) and DIVARICATA (DIV). RAD is involved in establishing the dorsal identity program and its role is to regulate the domain of activity of DIV (the ventral identity program) by restricting it to ventral regions of the flower. Plantago is in the same family as Antirrhinum but has small, radially symmetrical (actinomorphic) flowers derived from a zygomorphic ancestral state. Here we investigate the MYB‐class floral symmetry genes and the role they have played in the evolution of derived actinomorphy in Plantago lanceolata. A DIV ortholog (PlDIV) but no RAD ortholog was identified in P. lanceolata. PlDIV is expressed across all petals and stamens later in flower development, which is consistent with the loss of RAD gene function. PlDIV expression in anther sporogenous tissue also suggests that PlDIV was co‐opted to regulate cell proliferation during the early stages of pollen development. These results indicate that evolution of derived actinomorphy in Plantago involved complete loss of dorsal gene function, resulting in expansion of the domain of expression of the ventral class of floral symmetry genes.

Evolution of RADIALIS and DIVARICATA gene lineages in flowering plants with an expanded sampling in non‐core eudicots

“…Furthermore, three Oryza sativa MYB‐related proteins (OsMYBS1–3) regulate expression of the α‐amylase gene in response to sugar accumulation and hormone signals (Feller et al., ; Lu, ). In addition to these roles, some MYB genes like RAD and DIV control the dorsiventral floral symmetry in Antirrhinum majus (Almeida et al., ; Corley et al., ; Galego and Almeida, ; Reardon et al., ). RAD expression is promoted by CYC2 , a CYCLOIDEA TCP transcription factor (Corley et al., ; Costa et al., ).…”

“…In bilateral Lamialean flowers such as Torenia fournieri (Scrophulariaceae), both TfCYC2 and TfRAD1 are also highly expressed in the floral dorsal region and coordinate petal shape and corolla pigmentation (Su et al., ). Conversely, radial symmetry in Lamialean flowers is likely due to the broader homogeneous expression of both CYC and RAD throughout the floral meristem (Reardon et al., ; Su et al., ; Zhong and Kellogg, , b). In bilateral flowers of Dipsacales, RAD paralogs are differentially expressed in the dorsal and ventral floral organs as well as in leaf tissues (Boyden et al., ).…”

“…Both CYC and DICH genes belong to the TCP gene family (abbreviation for TEOSINTE BRANCHED 1 [ TB1 ] from Zea mays , CYCLOIDEA [ CYC ] from Antirrhinum majus and PROLIFERATION CELL FACTOR 1 and 2 [ PCF1 and PCF2 ] from Oryza sativa ) and have been comprehensively studied in model and non‐model species (Boyden et al., ; Broholm, ; Damerval and Manuel, ; De Paolo et al., ; Fambrini and Pugliesi, ; Galego and Almeida, ; Hileman et al., ; Howarth and Donoghue, , ; Lei et al., ; Li et al., ; Lin et al., ; Luo et al., ; Madrigal et al., ; Reardon et al., ; Su et al., ; Wei et al., ; Zhong and Kellogg, ; Zhou et al., ). On the other hand, RAD and DIV belong to the MYB ( Myeloblastosis ) gene superfamily and have been less studied in comparison to the TCP genes (Corley et al., ; Costa et al., ; Galego and Almeida, ; Luo et al., ; MacHemer et al., ; Reardon et al., ; Su et al., ; Valoroso et al., ).…”

Control of Floret Symmetry by RAY3, SvDIV1B, and SvRAD in the Capitulum of Senecio vulgaris

“…While the importance of CYC genes in the evolution of floral zygomorphy has been studied extensively in many species, evidence of RAD and DIV involvement is very limited. Recently, it has been proposed that the reversion to actinomorphic flowers in Plantago lanceolata is due to a loss of RAD from the genome (Reardon et al, 2014). In Bournea leiophylla (Gesneriaceae), loss of dorsal expression of BlCYC and BlRAD during the later stages of flower development led to up-regulation of BlDIV in the entire flower, which in turn generated a final actinomorphic structure (Zhou et al, 2008).…”

Genome structure and evolution ofAntirrhnum majusL

“…Interestingly, the results indicated this syntenic block was retained from a whole genome duplication event taken place during the time span of the zygomorphic flower emergences (about 60 million years ago). Furthermore, downstream CYC/DICH , two genes ( DIV and DRIF ) in RAD / DIV module have homologous copies with similar Ks as CYC / DICH , while DRIF is located at a WGD derived syntenic block 19,20,21 . Those analyses showed that the master regulators of zygomorphic flower were retained from the recent whole genome duplication, revealing the evolutionary base for the zygomorphic flower maintenance in A. majus and perhaps other close relatives.…”