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Plant carnivory in the Caryophyllales: phylogenetic relationships, morphological adaptations, and molecular evolution of digestive enzymes among carnivorous genera


Phylogenetic relationships among carnivorous plants of the angiosperm order Caryophyllales are explored using Bayesian statistics and maximum-likelihood based searches of phylogeny. Nuclear ribosomal (ITS) and chloroplast intergenic spacer (PY-IGS) regions, along with previously- sequenced DNA are utilized for phylogenetic reconstructions. Taxonomic relationships across genera are refined and three strongly supported clades are identified: monophyletic Droseraceae, Nepenthaceae, and a third clade containing Ancistrocladaceae, Dioncophyllaceae, and Drosophyllaceae. In combination with phylogenetic reconstruction, stochastic character mapping is utilized to assess evolutionary changes in the morphology of glands found on the lamina and involved in the digestion of prey. Adaptive changes resulting in the evolution of the carnivorous gland are discussed, which may have occurred either by emargination of the leaf blade or homologous transformation of pinnae.

A variety of enzymes are excreted from the carnivorous gland that aid in prey digestion. Within the carnivorous plants of the Caryophyllales, two subclasses of class I chitinases have been identified to play a role in the digestion of prey. Proteins produced by the large and diverse chitinase gene family are involved in the hydrolyzation of glycosidic bonds in chitin, a polymer of N-acetylglucosamines. Members of these subclasses, depending on the presence or absence of a C-terminal extension, can be secreted from specialized digestive glands found within morphologically diverse traps that develop from plant leaves. Homology among carnivorous plant class I chitinases and the method by which these enzymes have been adapted for the carnivorous habit are investigated. Novel class I chitinase homologs are recovered from Ancistrocladus, Dionaea, Drosera, Nepenthes, and Triphyophyllum, in addition to class I chitinases available from sequenced angiosperm genomes. Substitutions specific to carnivorous plant class I chitinases are revealed by detecting sites under positive selection, which may confer functional differences as indicated by protein structure homology-modeling.

To study gene function in non-model organisms, a virus induced gene silencing (VIGS) method was developed. VIGS has been shown to be effective for transient knockdown of gene expression in plants to analyze the effects of specific genes in development and stress related responses. It is demonstrated that the barley stripe mosaic virus (BSMV) is able to infect two species within the Zingiberaceae, and that BSMV-VIGS can be applied to specifically downregulate phytoene desaturase in the culinary ginger Zingiber officinale. BSMV-VIGS is likely to be effective in other angiosperms susceptible to BSMV infection. This should enable targeted studies for identifying gene function to be carried out in ecologically and evolutionarily important groups.

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