Implications of region-specific gene expression for development of the partially fused petunia corolla.

Angiosperm petal fusion (sympetaly) has evolved multiple times independently and is associated with increased specificity between plants and their pollinators. To uncover developmental genetic changes that might have led to the evolution of sympetaly in the asterid core eudicot genus Petunia (Solanaceae), we carried out global and fine-scale gene expression analyses in different regions of the corolla. We found that, despite several similarities with the choripetalous model species Arabidopsis thaliana in the proximal-distal transcriptome, the Petunia axillaris fused and proximal corolla tube expresses several genes that in A. thaliana are associated with the distal petal region. This difference aligns with variation in petal shape and fusion across ontogeny of the two species. Moreover, differential gene expression between the unfused lobes and fused tube of P. axillaris petals revealed three strong candidate genes for sympetaly based on functional annotation in organ boundary specification. Partial silencing of one of these, the HANABA TARANU (HAN)-like gene PhGATA19, resulted in reduced fusion of Petunia hybrida petals, with silencing of both PhGATA19 and its close paralog causing premature plant senescence. Finally, detailed expression analyses for the previously characterized organ boundary gene candidate NO APICAL MERISTEM (NAM) supports the hypothesis that it establishes boundaries between most P. axillaris floral organs, with the exception of boundaries between petals.

Bridging the gaps: evolution and development of perianth fusion.

One of the most striking innovations in flower development is the congenital or postgenital union of petals (sympetaly) which has enabled dramatic specialization in flower structure and possibly accelerated speciation rates. Sympetalous flowers exhibit extraordinary variation in development, including the degree and timing of fusion, and fusion with other floral organs. Different axes of corolla tube complexity can be disentangled at the developmental level, with most variation being explained by differences in coordinated growth between interconnected and lobed regions of neighboring petal primordia, and between lower and upper portions of the corolla tube, defined by the stamen insertion boundary. Genetically, inter- and intra-specific variation in the degree of petal fusion is controlled by various inputs from genes that affect organ boundary and lateral growth, signaling between different cell types, and production of the cuticle. It is thus hypothesized that the evolution and diversification of fused petals, at least within the megadiverse Asteridae clade of core eudicots, have occurred through the modification of a conserved genetic pathway previously involved in free petal development.