Photosynthetic activity in the heterotrophic plant genus Cuscuta (Convolvulaceae) is modulated by phylogeny and ontogeny.

Abstract

Background and aims: Photosynthesis is central to plant function, yet it has been repeatedly lost or diminished in parasitic angiosperm lineages. This variation raises questions about how photosynthetic function is retained, modified, or repurposed in the evolutionary context of parasitism. Cuscuta species, as a model system for studying parasitism, exhibit varying degrees of plastid functionality and photosynthetic ability, based on genomic and ultrastructure studies. However, few direct physiological studies exist, and none that span multiple developmental stages of autotrophic, mixotrophic, and non-photosynthetic species in a phylogenetic framework.

Methods: To address this gap, we paired photosynthetic activity measurements from Imaging-PAM fluorometry with quantitative analysis of chlorophylls and carotenoids from multiple developmental stages in fourteen Cuscuta species, representing the phylogenetic breadth of the genus, and a closely related autotrophic species. Multivariate data were analyzed using nonparametric hypothesis tests, and comparative phylogenetic patterns were explored through Bayesian model testing.

Key results: Photosynthetic activity, chlorophyll and carotenoid content were highest in meristematic regions (e.g., shoot tips and developing seeds) and lowest in older stems or haustoria. Neoxanthin, a carotenoid typically highly conserved in plants, appears to have been lost once in Cuscuta and subsequently re-gained in certain lineages. Complex relationships between photosynthetic activity and lutein epoxide concentration suggest differing roles in developmental stages with high and low energetic needs.

Conclusions: These findings provide substantial evidence that photosynthesis in Cuscuta is not vestigial but rather modulated based on developmental stage and across phylogenetic history, revealing a dynamic interplay between parasitism and photosynthetic function.