Evolution of Darwin’s Peloric Gloxinia (Sinningia speciosa) Is Caused by a Null Mutation in a Pleiotropic TCP Gene

Abstract

Unlike most crops, which were domesticated through long periods of selection by ancient humans, horticultural plants were primarily domesticated through intentional selection over short time periods. The molecular mechanisms underlying the origin and spread of novel traits in the domestication process have remained largely unexplored in horticultural plants. Gloxinia (Sinningia speciosa), whose attractive peloric flowers influenced the thoughts of Darwin, have been cultivated since the early 19th century, but its origin and genetic basis are currently unknown. By employing multiple experimental approaches including genetic analysis, genotype–phenotype associations, gene expression analysis, and functional interrogations, we showed that a single gene encoding a TCP protein, SsCYC, controls both floral orientation and zygomorphy in gloxinia. We revealed that a causal mutation responsible for the development of peloric gloxinia lies in a 10-bp deletion in the coding sequence of SsCYC. By combining genetic inference and literature searches, we have traced the putative ancestor and reconstructed the domestication path of the peloric gloxinia, in which a 10-bp deletion in SsCYC under selection triggered its evolution from the wild progenitor. The results presented here suggest that a simple genetic change in a pleiotropic gene can promote the elaboration of floral organs under intensive selection pressure.

Extensive phenotypic diversity in the cultivated Florist’s Gloxinia, Sinningia speciosa (Lodd.) Hiern, is derived from the domestication of a single founder population

“…As this mutation has probably occurred only once, all cultivated forms with actinomorphic flowers are likely descendants of Gloxinia “Fyfiana” (Citerne & Cronk, ; Dong et al, ). The identical mutation was confirmed in multiple cultivars by Dong et al () who identified a small deletion in the single CYCLOIDEA ‐like gene found in S. speciosa ( SsCYC ). The wild‐type allele of this and related genes are responsible for suppressing growth in the dorsal organs of wild zygomorphic flowers such as S. speciosa and Antirrhinum majus (snapdragon).…”

“…This particular cultivar occupies an important place in the history of S. speciosa , because most modern cultivars have inherited their distinctive flower shape from a single recessive mutation that was disseminated extensively during the early stages of domestication. As this mutation has probably occurred only once, all cultivated forms with actinomorphic flowers are likely descendants of Gloxinia “Fyfiana” (Citerne & Cronk, ; Dong et al, ). The identical mutation was confirmed in multiple cultivars by Dong et al () who identified a small deletion in the single CYCLOIDEA ‐like gene found in S. speciosa ( SsCYC ).…”

“…He associated seven domesticated cultivars with the wild forms “Avenida Niemeyer” and ‘São Conrado’, also collected along the coast in the city of Rio de Janeiro. Dong et al () however, obtained contrasting results. Their phylogenetic analysis was based on the SsCYC gene sequence and suggests that the actinomorphic allele, which is homozygous in most cultivated material, originated from the wild‐type “Cardoso Moreira”.…”

“…Their phylogenetic analysis was based on the SsCYC gene sequence and suggests that the actinomorphic allele, which is homozygous in most cultivated material, originated from the wild‐type “Cardoso Moreira”. The plant material used in the Dong et al () study traces to a population located 2–3 km from the town of the same name, located in the northern part of Rio de Janeiro state (more than 300 km distant from Rio de Janeiro city) ~50 km from the southern border of the state of Espírito Santo (Zaitlin, ). Both of our “Cardoso Moreira” samples (purple‐ and pink‐flowered forms) clustered together with "São Fidelis", an accession that was collected 30–40 km from the “Cardoso Moreira” population, validating its geographical origin.…”

“…These results are supported by our population structure analyses in conjunction with previous phenetic and phylogenetic analyses (Zaitlin, ) as well as by written records that disclose collection sites (Brackenridge, ; Hooker, ; Paxton, ). Second, the already narrow pool of alleles in cultivated material could have shrunken even further following the substantial selective sweep around the SsCYC gene (Dong et al, ) that has practically fixed the mutant actinomorphic allele in the modern cultivars.…”