Abstract
The emergence of the carnivory syndrome and traps in plants is one of the most intriguing questions in evolutionary biology. In the present study, we addressed it by comparative transcriptomics analysis of leaves and leaf-derived pitcher traps from a predatory plant Nepenthes ventricosa × Nepenthes alata. Pitchers were collected at three stages of development and a total of 12 transcriptomes were sequenced and assembled de novo. In comparison with leaves, pitchers at all developmental stages were found to be highly enriched with upregulated genes involved in stress response, specification of shoot apical meristem, biosynthesis of sucrose, wax/cutin, anthocyanins, and alkaloids, genes encoding digestive enzymes (proteases and oligosaccharide hydrolases), and flowering-related MADS-box genes. At the same time, photosynthesis-related genes in pitchers were transcriptionally downregulated. As the MADS-box genes are thought to be associated with the origin of flower organs from leaves, we suggest that Nepenthes species could have employed a similar pathway involving highly conserved MADS-domain transcription factors to develop a novel structure, pitcher-like trap, for capture and digestion of animal prey during the evolutionary transition to carnivory. The data obtained should clarify the molecular mechanisms of trap initiation and development and may contribute to solving the problem of its emergence in plants.
Highlights
Predator plants attract arthropods that serve both as pollinators for sexual reproduction and as prey captured and digested in traps; traps represent modified leaves developed to support plant survival in the nutrient-deficient environment (Jürgens et al, 2012; Pavlovicand Saganová, 2015; Bartlett, 2017)
The results revealed activation of genes associated with defense response, shoot apical meristem (SAM) organization, anthocyanin biosynthesis, and flowering, including MADS-domain transcription factors (TFs), in pitchers
Considering that MADS-box genes are thought to have been involved in the evolution of plant flower organs, we suggest that the emergence of the pitcher structure was due to highly conserved MADS-domain TFs, which usually determine the identity of floral meristems and organs in extant plants
Summary
Predator plants attract arthropods that serve both as pollinators for sexual reproduction and as prey captured and digested in traps (active or passive); traps represent modified leaves developed to support plant survival in the nutrient-deficient environment (Jürgens et al, 2012; Pavlovicand Saganová, 2015; Bartlett, 2017). The list of green predators contains more than 650 species representing 19 genera, 12 families, and five orders of the flowering plants, both monocots and eudicots (Pavlovicand Saganová, 2015). Nepenthes species develop typical photosynthetic leaves whose tips form a tendril as an extension of the midrib, to which a pitcher-like pitfall trap is attached (Owen and Lennon, 1999). The main pitcher characteristics attracting the prey are color patterns (UV fluorescence/visible wavebands), sweet fragrance of the secreted extrafloral nectar, and high CO2 levels (Kurup et al, 2013; Baby et al, 2017)
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