Carnivorous pitcher plants: insights in an old topic.

Plant insect interactions are usually recognized as a scenario where herbivorous insects feed on a host plant. However, also the opposite situation is known, where plants feed on insects. Carnivorous pitcher plants of the genus Nepenthes as well as other pitcher plants obtain many nutrients from caught insect prey. Special features of the pitcher traps' surface are responsible for attraction and trapping insects. Once caught, the prey is digested in the fluid of the pitchers to release nutrients and make them available for the plant. Nutrients are taken up by special glands localized on the inner surface of the pitchers. These glands also secrete the hydrolyzing enzymes into the digestion fluid. Although this is known for more than 100 years, our knowledge of the pitcher fluid composition is still limited. Only in recent years some enzymes have been purified from the pitcher fluid and their corresponding genes could be identified. Among them, many pathogenesis-related proteins have been identified, most of which exhibiting hydrolytic activities. The role of these proteins as well as the role of secondary metabolites, which have been identified in the pitcher fluid, is discussed in general and in the context of further studies on carnivorous plants that might give answers to basic questions in plant biology.

[1]  A. Iwamatsu,et al.  Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases. , 2004, The Biochemical journal.

[2]  M. Riedel,et al.  Chemical composition of epicuticular wax crystals on the slippery zone in pitchers of five Nepenthes species and hybrids , 2007, Planta.

[3]  A. Jürgens,et al.  Do carnivorous plants use volatiles for attracting prey insects , 2009 .

[4]  Walter Federle,et al.  Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  M. Chase,et al.  Murderous plants: Victorian Gothic, Darwin and modern insights into vegetable carnivory , 2009 .

[6]  Y. Heslop-Harrison.  Enzyme release in carnivorous plants. , 1975, Frontiers of biology.

[7]  Tatsuro Hamada,et al.  Proteome analysis of pitcher fluid of the carnivorous plant Nepenthes alata. , 2008, Journal of proteome research.

[8]  A. Mithöfer,et al.  Micropreparation of single secretory glands from the carnivorous plant Nepenthes. , 2009, Analytical biochemistry.

[9]  C. Pieterse,et al.  Significance of inducible defense-related proteins in infected plants. , 2006, Annual review of phytopathology.

[10]  S. Mcpherson.  Pitcher Plants of the Old World , 2009 .

[11]  D. Gallie,et al.  Signal Transduction in the Carnivorous Plant Sarracenia purpurea (Regulation of Secretory Hydrolase Expression during Development and in Response to Resources) , 1997, Plant Physiology.

[12]  S. Gorb,et al.  Function of epidermal surfaces in the trapping efficiency of Nepenthes alata pitchers. , 2002, The New phytologist.

[13]  B. Hawkins,et al.  From Carnivore to Detritivore? Isotopic Evidence for Leaf Litter Utilization by the Tropical Pitcher Plant Nepenthes ampullaria , 2003, International Journal of Plant Sciences.

[14]  J. A. Moran.  Pitcher Dimorphism, Prey Composition and the Mechanisms of Prey Attraction in the Pitcher Plant Nepenthes Rafflesiana in Borneo , 1996 .

[15]  W. Qin,et al.  The development of the pitcher plant Sarracenia purpurea into a potentially valuable recombinant protein production system. , 2009 .

[16]  Z. Tökés,et al.  Digestive enzymes secreted by the carnivorous plant Nepenthes macferlanei L. , 1974, Planta.

[17]  J. A. Moran,et al.  Aspects of pitcher morphology and spectral characteristics of six Bornean Nepenthes pitcher plant species: implications for prey capture , 1999 .

[18]  R. J. Robins,et al.  The Carnivorous Plants , 1989 .

[19]  S. H. Vines.  The Proteolytic Enzyme of Nepenthes (II) , 1898 .

[20]  L. Adamec.  Mineral nutrition of carnivorous plants: A review , 1997, The Botanical Review.

[21]  M. Wohlfarth,et al.  Droserone from cell cultures of Triphyophyllum peltatum (Dioncophyllaceae) and its biosynthetic origin. , 2000, Phytochemistry.

[22]  T. Uchiumi,et al.  Analysis of feeding mechanism in a pitcher ofNepenthes hybrida , 1993, Journal of Plant Research.

[23]  P. Stephenson,et al.  Cloning and Characterization of a Ribonuclease, a Cysteine Proteinase, and an Aspartic Proteinase from Pitchers of the Carnivorous Plant Nepenthes ventricosa Blanco , 2006, International Journal of Plant Sciences.

[24]  W. Baumgartner,et al.  Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness , 2010, Journal of Experimental Biology.

[25]  A. Zilberstein,et al.  Isolation and characterization of chitinase genes from pitchers of the carnivorous plant Nepenthes khasiana. , 2006, Journal of experimental botany.

[26]  M. Riedel,et al.  Slippery surfaces of carnivorous plants: composition of epicuticular wax crystals in Nepenthes alata Blanco pitchers , 2003, Planta.

[27]  B. Gowen,et al.  Ion fluxes across the pitcher walls of three Bornean Nepenthes pitcher plant species: flux rates and gland distribution patterns reflect nitrogen sequestration strategies , 2010, Journal of experimental botany.

[28]  Y. Forterre,et al.  A Viscoelastic Deadly Fluid in Carnivorous Pitcher Plants , 2007, PLoS ONE.

[29]  J. A. Moran,et al.  The carnivorous syndrome in Nepenthes pitcher plants , 2010, Plant signaling & behavior.

[30]  Elena Gorb,et al.  Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention , 2004, Journal of Experimental Biology.

[31]  P. Dittrich,et al.  Molecular Phylogeny of Nepenthaceae Based on Cladistic Analysis of Plastid trnK Intron Sequence Data , 2001 .

[32]  M. Chase,et al.  Carnivorous plants: phylogeny and structural evolution. , 1992, Science.

[33]  K. Rembold,et al.  Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant , 2009, Biology Letters.

[34]  Jorge M. González,et al.  Carnivory in pitcher plants of the genus Heliamphora (Sarraceniaceae) , 2006 .

[35]  N. Goh,et al.  Phenolic constituents from the leaves of the carnivorous plant Nepenthes gracilis. , 2002, Fitoterapia.

[36]  W. Frommer,et al.  Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes. , 1999, The Plant journal : for cell and molecular biology.

[37]  A. Pavlovič,et al.  Carnivorous syndrome in Asian pitcher plants of the genus Nepenthes. , 2007, Annals of botany.

[38]  S. Carmeli,et al.  Induced production of antifungal naphthoquinones in the pitchers of the carnivorous plant Nepenthes khasiana , 2009, Journal of experimental botany.

[39]  G. Bringmann,et al.  Nepenthes insignis uses a C2-portion of the carbon skeleton of L-alanine acquired via its carnivorous organs, to build up the allelochemical plumbagin. , 2002, Phytochemistry.

[40]  R. Matthews.  A ribonuclease from Nepenthes spp , 1960 .

[41]  A. Anderson,et al.  Pathways for Nutrient Transport in the Pitchers of the Carnivorous Plant Nepenthes alata , 1999 .

[42]  H. Meimberg,et al.  Introduction of a Nuclear Marker for Phylogenetic Analysis of Nepenthaceae , 2006, Plant biology.

[43]  A. Ellison,et al.  Energetics and the evolution of carnivorous plants--Darwin's 'most wonderful plants in the world'. , 2009, Journal of experimental botany.

[44]  J. A. Moran,et al.  Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size. , 2010, The New phytologist.