Similar Genetic Mechanisms Underlie the Parallel Evolution of Floral Phenotypes

The repeated origin of similar phenotypes is invaluable for studying the underlying genetics of adaptive traits; molecular evidence, however, is lacking for most examples of such similarity. The floral morphology of neotropical Malpighiaceae is distinctive and highly conserved, especially with regard to symmetry, and is thought to result from specialization on oil-bee pollinators. We recently demonstrated that CYCLOIDEA2–like genes (CYC2A and CYC2B) are associated with the development of the stereotypical floral zygomorphy that is critical to this plant–pollinator mutualism. Here, we build on this developmental framework to characterize floral symmetry in three clades of Malpighiaceae that have independently lost their oil bee association and experienced parallel shifts in their floral morphology, especially in regard to symmetry. We show that in each case these species exhibit a loss of CYC2B function, and a strikingly similar shift in the expression of CYC2A that is coincident with their shift in floral symmetry. These results indicate that similar floral phenotypes in this large angiosperm clade have evolved via parallel genetic changes from an otherwise highly conserved developmental program

Genetic Analysis of Floral Symmetry in Van Gogh's Sunflowers Reveals Independent Recruitment of CYCLOIDEA Genes in the Asteraceae

The genetic basis of floral symmetry is a topic of great interest because of its effect on pollinator behavior and, consequently, plant diversification. The Asteraceae, which is the largest family of flowering plants, is an ideal system in which to study this trait, as many species within the family exhibit a compound inflorescence containing both bilaterally symmetric (i.e., zygomorphic) and radially symmetric (i.e., actinomorphic) florets. In sunflower and related species, the inflorescence is composed of a single whorl of ray florets surrounding multiple whorls of disc florets. We show that in double-flowered (dbl) sunflower mutants (in which disc florets develop bilateral symmetry), such as those captured by Vincent van Gogh in his famous nineteenth-century sunflower paintings, an insertion into the promoter region of a CYCLOIDEA (CYC)-like gene (HaCYC2c) that is normally expressed specifically in WT rays is instead expressed throughout the inflorescence, presumably resulting in the observed loss of actinomorphy. This same gene is mutated in two independent tubular-rayed (tub) mutants, though these mutations involve apparently recent transposon insertions, resulting in little or no expression and radialization of the normally zygomorphic ray florets. Interestingly, a phylogenetic analysis of CYC-like genes from across the family suggests that different paralogs of this fascinating gene family have been independently recruited to specify zygomorphy in different species within the Asteraceae

A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus

In several eudicots, including members of the Asteraceae family, the CYCLOIDEA (CYC) genes, which belong to the TCP class of transcription factors, are key players for floral symmetry. The sunflower inflorescence is heterogamous (radiate capitulum) with sterile monosymmetric ray flowers located in the outermost whorl of the inflorescence and hermaphrodite polysymmetric disk flowers. In inflorescence of Heliantheae tribe, flower primordia development initiates from the marginal ray flowers while disk flowers develop later in an acropetal fashion in organized parastichies along a number found to be one of Fibonacci patterns. Mutants for inflorescence morphology can provide information on the role of CYC-like genes in radiate capitulum evolution. The tubular ray flower (turf) mutant of sunflower shows hermaphrodite ray flowers with a nearly polysymmetric tubular-like corolla. Here, we demonstrate that this mutation is caused by the insertion in the TCP motif of a sunflower CYC-like gene (HaCYC2c) of non-autonomous transposable element (TE), belonging to the CACTA superfamily of transposons. We named this element Transposable element of turf1 (Tetu1). The Tetu1 insertion changes the reading frame of turf-HaCYC2c for the encoded protein and leads to a premature stop codon. Although in Tetu1 a transposase gene is lacking, our results clearly suggest that it is an active TE. The excision of Tetu1 restores the wild type phenotype or generates stable mutants. Co-segregation and sequence analysis in progenies of F2 and self-fertilized plants derived from reversion of turf to wild type clearly identify HaCYC2c as a key regulator of ray flowers symmetry. Also, HaCYC2c loss-of-function promotes the developmental switch from sterile to hermaphrodite flowers, revealing a novel and unexpected role for a CYC-like gene in the repression of female organs