The seed transcriptome of Rafflesia reveals horizontal gene transfer and convergent evolution: Implications for conserving the world's largest flower

Abstract

Societal Impact StatementRafflesia is a genus of parasitic plants with the largest flowers in the world, unique to the threatened forest habitats of tropical Asia. Here, we report on genes that are active (the transcriptome) in Rafflesia seeds as part of a larger effort to understand Rafflesia. Rafflesia has never been grown successfully outside of its native range. Consequently, seed banking is not yet possible, precluding a critical management strategy for conservation. The study of Rafflesia seed biology is a critical step to improve its cultivation, which will educate the public about unique species and the importance of conserving their habitats.Summary Rafflesia is of great interest as one of the only two plants known to have completely lost its chloroplast genome. Rafflesia is a holoparasite and an endophyte that lives inside the tissues of its host, a tropical grape vine (Tetrastigma), emerging only to bloom—with the largest flower of any plant. Here, we report the first Rafflesia seed transcriptome and compare it with those of other plants to deepen our understanding of its extraordinary life history. We assembled a transcriptome from RNA extracted from seeds of the Philippine endemic Rafflesia speciosa and compared this with those of other plants, including Arabidopsis, parasitic plants Striga and Cuscuta, and the mycoheterotrophic orchid Anoectochilus. Genetic and metabolic seed pathways in Rafflesia were generally similar to the other plant species. However, there were some notable exceptions. We found evidence of horizontal transfer of a gene potentially involved in circumventing host defenses. Moreover, we identified a possible convergence among parasitic plants because Rafflesia, Striga, and Cuscuta shared important similarities. We were unable to find evidence of genes involved in mycorrhizal symbiosis, suggesting that mycoheterotrophy is unlikely to play a role in Rafflesia parasitism. To date, ex situ propagation of Rafflesia by seed has been mostly unsuccessful. Our research is a bold step forward in understanding the fundamentals of Rafflesia seed biology that will inform the continued propagation and seed‐banking efforts concerning this recalcitrant plant. We discuss our findings in the broader context of the conservation of a genus in peril.