Evolution and expression of the flowering integrator genes AGL24, SVP, and SOC1 in the endoholoparasitic Apodanthaceae

Abstract

ABSTRACT: Floral transition is crucial for successful plant reproduction. This is regulated by multiple genetic pathways activated by environmental and endogenous signals and unified by a limited number of integrators. While floral transitions have been extensively studied in autotrophic plants, less attention has been given to endoholoparasitic angiosperms, which lack stems and leaves; thus they cannot sense environmental signals to initiate the floral transition, yet they still manage to bloom. In this study, we explore how the Apodanthaceae (a family with 12 endoholoparasitic species) achieve this. To this end, we studied three key integrators (AGL24, SVP, and SOC1) involved in floral transition, in two members of the family, namely, the legume parasite Pilostyles boyacensis and the Salicaceae parasite Apodanthes caseariae. We identified AGL24, SVP, and SOC1 homologs and assessed their copy numbers in the reference transcriptomes of endoholoparasites and their hosts. Subsequently, we determined their phylogenetic affinities. In A. caseariae we found one AGL24A, one AGL24B, and two SVP copies. Whereas AGL24A likely belongs to the host (Salicaceae), AGL24B and SVP genes appear to be endogenously transcribed by the parasite. No SOC1 homologs were identified. In Pilostyles boyacensis we found at least one copy of AGL24A and AGL24B, along with five SVP variants, all of them likely belonging to the host (Dalea cuatrecasasii). We also found three SOC1 copies in P. boyacensis transcriptomes; however, two belonging to its host, and one likely endogenous. Preliminary data from in-situ hybridization in D. cuatrecasasii and P. boyacensis point to extensive usage of host genes, especially DacuAGL24A, by the parasite. Conversely, expression of D. cuatrecasasii SVP homologs, the only flowering repressors found in the system, is low in both plants. Our results suggest that endoholoparasites achieve reproductive transition by utilizing specific transcription factors from the host.