Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory

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.

Convergent and divergent evolution in carnivorous pitcher plant traps

“…Fukushima et al . () have shown recently that Arabidopsis genes related to the genes coding for digestive fluid proteins in carnivorous plants are upregulated under biotic and abiotic stresses. The authors suggest that the co‐option of stress response proteins may be a widespread pattern in the evolution of carnivorous plant enzymes.…”

“…Cephalotus produces pitchers and non-carnivorous flat leaves in synchrony. Recently, Fukushima et al (2017) have sequenced the transcriptome of both leaf types and have shown that the genes involved in adaxial-abaxial polarity are upregulated in pitcher-bearing shoots. The authors also identified an upregulation of genes involved in sucrose, wax and cutin biosynthesis.…”

Phytobiological Warfare: An Evolutionary Approach to Botanical Medicine

“…5 Evolutionarily related non-carnivorous species do not appear to express this antiviral activity suggesting the antiviral capability may be necessary for carnivorous plant sustainability. A model is proposed where specific plants develop adaptations to deal with potential pathogens or pressures present in their environment.…”

Evaluating the adaptive evolutionary convergence of carnivorous plant taxa through functional genomics

“…From Dionaea mupcipula, functions of proteins identified via proteomic analysis of the trap fluid (Schulze et al, 2012) were listed, with the addition of genes related to transport that had been specifically targeted by other studies (Owen et al, 1999;Böhm et al, 2016). Similarly, in Nepenthep, proteomic analysis of trap fluid released a list of functions likely to be associated with plant carnivory (Rotloff et al, 2016), with other studies assaying for a specific digestion-associated enzyme and detecting transport activity via traps' glandular symplasts (An, Fukushima, &Kobayashi, 2002 andScherzer et al, 2013, respectively). In the bladderwort Utricularia gibba L., transcriptomic analysis was used to detect statistically increased expression of genes in traps and leaves putatively associated with carnivory (Ibarra-Laclette et al, 2011).…”

“…Four were available: Cephalotup follicularip (Fukushima, Fang, et al, 2017), Dropera capenpip (Butts, Bierma, & Martin, 2016), Genlipea aurea (Leushkin et al, 2013), and Utricularia gibba (Lan et al, 2017). The carnivorous taxa sampled represent three independent origins of plant carnivory (Genlipea and Utricularia likely sharing a single origin) in three plant orders (Caryophyllales, Oxalidales, and Lamiales).…”