Plastid Genome Evolution Across the Roridulaceae-Sarraceniaceae Clade (Ericales) in Relation to Carnivorous Strategies

杜鹃花科-瓶子草科分支(杜鹃花目)质体基因组进化与食肉策略的关系

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Abstract

The Roridulaceae-Sarraceniaceae (RS) clade within Ericales exhibits strikingly divergent carnivorous strategies. To investigate how these differences shape plastid genome (plastome) evolution, we analyzed four representative species: Roridula gorgonias (Roridulaceae), which absorbs nutrients from insect feces without digestive enzymes; and three pitfall trap Sarraceniaceae species-Heliamphora minor (relying on microbial decomposition), Darlingtonia californica (with digestive enzymes, lacking endocytosis), and Sarracenia leucophylla (with digestive enzymes and endocytosis). Across RS species, ndh genes frequently exhibit severely disrupted or completely lost open reading frames (ORFs). Compared with Sarraceniaceae species exhibiting greater degrees of carnivorous specialization, Roridula gorgonias plastomes exhibit markedly accelerated and structurally dynamic evolution, including partial loss of the clpP gene, frequent insertion events, elevated nonsynonymous (d (N)) and synonymous (d (S)) substitution rates, widespread relaxation of purifying selection, multiple sites under positive selection across plastome genes, and reduced RNA editing efficiency at conserved codons. In contrast, variation in digestive traits and endocytotic capability among Sarraceniaceae species corresponds to only subtle plastome-level differences, with limited changes in GC content, gene number, and evolutionary rates. These results indicate that plastome evolution within the RS clade is not predicted by the degree of carnivorous specialization alone, but instead is best explained by context-dependent effects of trophic strategy and other ecological pressures. In Roridula gorgonias, the pronounced plastome dynamics likely reflect the combined influence of carnivory and recurrent wildfire stress in nutrient-poor habitats, thereby facilitating the accumulation of higher mutational loads.

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