Abstract

Carnivorous plants exploit animals as a nutritional source and have inspired long-standing questions about the origin and evolution of carnivory-related traits. To investigate the molecular bases of carnivory, we sequenced the genome of the heterophyllous pitcher plant Cephalotus follicularis, in which we succeeded in regulating the developmental switch between carnivorous and non-carnivorous leaves. Transcriptome comparison of the two leaf types and gene repertoire analysis identified genetic changes associated with prey attraction, capture, digestion and nutrient absorption. Analysis of digestive fluid proteins from C. follicularis and three other carnivorous plants with independent carnivorous origins revealed repeated co-options of stress-responsive protein lineages coupled with convergent amino acid substitutions to acquire digestive physiology. These results imply constraints on the available routes to evolve plant carnivory.

Highlights

  • Carnivorous plants exploit animals as a nutritional source and have inspired long-standing questions about the origin and evolution of carnivory-related traits

  • Cephalotus follicularis (Cephalotus), a carnivorous plant native to southwest Australia that belongs to the monospecific family Cephalotaceae in the order Oxalidales, forms both carnivorous pitcher leaves and non-carnivorous flat leaves (Fig. 1)

  • As we succeeded in regulating the developmental switch between pitcher and flat leaves by ambient temperature (Fig. 1b and Supplementary Fig. 1f,g), their transcriptomes were compared

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Summary

Introduction

Carnivorous plants exploit animals as a nutritional source and have inspired long-standing questions about the origin and evolution of carnivory-related traits. RNase T2, known as a constituent of digestive fluids[1,8,9], is enriched among orthogroups composed only of genes from Cephalotus and another carnivorous plant Utricularia gibba (Supplementary Table 18). To further investigate the origin and evolution of digestive enzymes of Cephalotus and three other distantly related carnivorous plants (Drosera adelae, N. alata and Sarracenia purpurea), we sequenced fragments of digestive fluid proteins and identified 35 corresponding genes (Fig. 2a and Supplementary Tables 25–28).

Results
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