Inside the trap: gland morphologies, digestive enzymes, and the evolution of plant carnivory in the Caryophyllales

Abstract

The digestion of prey by carnivorous plants is determined in part by suites of enzymes that are associated with morphologically and anatomically diverse trapping mechanisms. Chitinases represent a group of enzymes known to be integral to effective plant carnivory. In non-carnivorous plants, chitinases commonly act as pathogenesis-related proteins, which are either induced in response to insect herbivory and fungal elicitors, or constitutively expressed in tissues vulnerable to attack. In the Caryophyllales carnivorous plant lineage, multiple classes of chitinases are likely involved in both pathogenic response and digestion of prey items. We review what is currently known about trap morphologies, provide an examination of the diversity, roles, and evolution of chitinases, and examine how herbivore and pathogen defense mechanisms may have been coopted for plant carnivory in the Caryophyllales.

Figure 1

Characteristics of multicellular glands associated with plant carnivory in the Caryophyllales. Multicellular glands involved in plant carnivory are either sessile, stalked, or pitted, and may contain either xylem or phloem. Phylogenetic relationships depicted among major carnivorous plant genera of the Caryophyllales are based upon maximum likelihood and Bayesian inference analyses and character states refer to stochastic character mapping of gland states [16••]. Gray in the phylogeny represents non-carnivorous taxa, while black represent carnivorous taxa. Illustrations located below character states depict examples of gland types for members of the carnivorous Caryophyllales and outgroup Plumbaginaceae (not to scale). For more detail in regard to gland morphologies, see [,–19,21,64].

Figure 2

Molecular evolution of class I chitinases in the carnivorous Caryophyllales. (a) Phylogenetic reconstruction for subclasses Ia and Ib chitinases of the carnivorous plants of the Caryophyllales based on the Bayesian inference analyses for HMM-derived class I chitinases homologs, with posterior probabilities indicated at nodes on the 50% majority rule tree [14••]. Nepenthes khasiana chitinases in bold (Nepenthes khasiana ChitI-1 and Nepenthes khasiana ChitI-3) are homology modeled in (b). (b) Residues colored green or yellow within the three-dimensional models for subclass Ia Nepenthes khasiana ChitI-1 and subclass Ib Nepenthes khasiana ChitI-3 represent sites interacting with NAG. Yellow residues highlight differences between the two subclasses. Site 276 (asterisk) is identified as under positive selection in Nepenthes subclass Ia chitinases (Phe276). Models based on previous analyses of N. khasiana class I chitinase structures [14••].