Many plants have evolved adaptations in order to survive in low nitrogen environments. One of the best-known adaptations is that of plant symbiosis with nitrogen-fixing bacteria; this is the major route by which nitrogen is incorporated into plant biomass. A portion of this plant-associated nitrogen is then lost to insects through herbivory, and insects represent a nitrogen reservoir that is generally overlooked in nitrogen cycles. In this review we show three specialized plant adaptations that allow for the recovery of insect nitrogen; that is, plants gaining nitrogen from insects. First, we show specialized adaptations by carnivorous plants in low nitrogen habitats. Insect carnivorous plants such as pitcher plants and sundews ( Nepenthaceae/ Sarraceniaceae and Drosera respectively) are able to obtain substantial amounts of nitrogen from the insects that they capture. Secondly, numerous plants form associations with mycorrhizal fungi that can provide soluble nitrogen from the soil, some of which may be insect-derived nitrogen, obtained from decaying insects or insect frass. Finally, a specialized group of endophytic, insect-pathogenic fungi (EIPF) provide host plants with insect-derived nitrogen. These soil-inhabiting fungi form a remarkable symbiosis with certain plant species. They can infect a wide range of insect hosts and also form endophytic associations in which they transfer insect-derived nitrogen to the plant. Root colonizing fungi are found in disparate fungal phylogenetic lineages, indicating possible convergent evolutionary strategies between taxa, evolution potentially driven by access to carbon-containing root exudates.
References
[1]
Schulten, H.R.; Schnitzer, M. The chemistry of soil organic nitrogen: A review. Biol. Fertil. Soils 1998, 26, 1–15, doi:10.1007/s003740050335.
[2]
Cocking, E.C. Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 2003, 252, 169–175, doi:10.1023/A:1024106605806.
[3]
Mary, B.; Recous, S.; Darwis, D.; Robin, D. Interactions between decomposition of plant residues and nitrogen cycling in soil. Plant Soil 1996, 181, 71–82, doi:10.1007/BF00011294.
Sprent, J.I. Benefits of Rhizobium to agriculture. Trends Biotechnol. 1986, 4, 124–129, doi:10.1016/0167-7799(86)90145-9.
[7]
Johansson, J.F.; Paul, L.R.; Finlay, R.D. Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol. Ecol. 2006, 48, 1–13, doi:10.1016/j.femsec.2003.11.012.
[8]
Koller, R.; Rodriguez, A.; Robin, C.; Scheu, S.; Bonkowski, M. Protozoa enhance foraging efficiency of arbuscular mycorrhizal fungi for mineral nitrogen from organic matter in soil to the benefit of host plants. New Phytol. 2013, 199, 203–211, doi:10.1111/nph.12249.
[9]
Liaw, Y.P. Comparison of field, laboratory, and theoretical estimates of global nitrogen fixation by lightning. J. Geophys. Res. 1990, 95, 22489–22494, doi:10.1029/JD095iD13p22489.
[10]
Blossey, B.; Hunt-Joshi, T.R. Belowground herbivory by insects: Influence on plants and aboveground herbivores. Annu. Rev. Entomol. 2003, 48, 521–547, doi:10.1146/annurev.ento.48.091801.112700.
[11]
Post, W.M.; Pastor, J.; Zinke, P.J.; Stangenberger, A.G. Global patterns of soil nitrogen storage. Nature 1985, 317, 613–616, doi:10.1038/317613a0.
[12]
Parsons, L.L.; Smith, M.S.; Murray, R.E. Soil denitrification dynamics: Spatial and temporal variations of enzyme activity, populations, and nitrogen gas loss. Soil Sci. Soc. Am. J. 1991, 55, 90–95, doi:10.2136/sssaj1991.03615995005500010016x.
[13]
Goulding, K.W.Y.; Bailey, N.J.; Bradbury, N.J.; Hargreaves, P.; Howe, M.; Murphy, D.V.; Poulton, P.R.; Willison, T.W. Nitrogen deposition and its contribution to nitrogen cycling and associated soil processes. New Phytol. 1998, 139, 49–58.
[14]
Whittaker, J.B. Insects and plants in a changing atmosphere. J. Ecol. 2001, 89, 507–518, doi:10.1046/j.0022-0477.2001.00582.x.
[15]
Wardle, D.A. A comparative assessment of factors which influence microbial biomass carbon and nitrogen in the soil. Biol. Rev. 1992, 67, 321–358, doi:10.1111/j.1469-185X.1992.tb00728.x.
[16]
Vitousek, P.M.; Howarth, R.W. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 1991, 13, 87–115.
[17]
Elser, J.J.; Bracken, M.E.S.; Cleland, E.E.; Gruner, D.S.; Harpole, W.S.; Hillebrand, H.; Ngai, J.T.; SeabloomE, W.; Shurin, J.B.; Smith, J.E. Global analysis of nitrogen and phos-phorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 2007, 10, 1135–1142, doi:10.1111/j.1461-0248.2007.01113.x.
[18]
Gutschick, V.P. Evolved strategies in nitrogen acquisition by plants. Am. Nat. 1981, 118, 607–637.
Agren, G.I. Nitrogen productivity of some conifers. Can. J. For. Res. 1983, 13, 494–500, doi:10.1139/x83-073.
[21]
Huenneke, L.F.; Hamburg, S.P.; Koide, R.; Mooney, H.A.; Vitousek, P.M. Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 1990, 71, 478–491, doi:10.2307/1940302.
[22]
Shaver, G.R.; Chapin, F.S. Response to fertilization by various plant growth forms in an Alaskan tundra: Nutrient accumulation and growth. Ecology 1980, 61, 662–675, doi:10.2307/1937432.
[23]
Field, C.; Mooney, H.A. The photosynthesis-nitrogen relationship in wild plants. In On the Economy of Plant Form and Function; Givnish, T.J., Ed.; Cambridge University Press: Cambridge, UK, 1986; pp. 25–55.
Melillo, J.M.; Aber, J.D.; Muratore, J.F. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 1982, 63, 621–626, doi:10.2307/1936780.
[26]
Melilo, J.M.; Aber, J.D.; Linkins, A.E.; Ricca, A.; Fry, B.; Nadelhoffer, K.J. Carbon and nitrogen dynamics long the decay continuum: Plant litter to soil organic matter. Dev. Plant Soil Sci. 1989, 39, 53–62.
[27]
Kelley, K.R.; Stevenson, F.J. Forms and nature of organic N in soil. Fert. Res. 1995, 42, 1–11, doi:10.1007/BF00750495.
[28]
Ayers, E.; Dromph, K.M.; Cook, R.; Ostle, N.; Bardgett, R.D. The influence of below-ground herbivory and defoliation of a legume on nitrogen transfer to neighbouring plants. Funct. Ecol. 2007, 21, 256–263, doi:10.1111/j.1365-2435.2006.01227.x.
[29]
Mattson, W.J. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 1980, 11, 119–161.
[30]
Maron, J.L. Insect herbivory above and belowground: Individual and joint effects on plant fitness. Ecology 1998, 79, 1281–1293, doi:10.1890/0012-9658(1998)079[1281:IHAABI]2.0.CO;2.
[31]
Murray, P.J.; Hatch, J.B.; Cliquet, J.B. Impact of insect root herbivory on the growth and nitrogen and carbon contents of white clover (Trifolium repens) seedlings. Can. J. Bot. 1996, 74, 1591–1595, doi:10.1139/b96-192.
[32]
Fagan, W.F.; Siemann, E.; Mitter, C.; Denno, R.F.; Huberty, A.F.; Woods, A.; Elser, J.J. Nitrogen in Insects: Implications for Trophic Complexity and Species Diversification. Am. Nat. 2002, 160, 784–802.
[33]
Van Emden, H.F. Pest Control, 2nd ed. ed.; Edward Arnold Publication: London, UK, New York, NY, USA, 1989.
[34]
Kummerow, J.; Alexander, J.V.; Neel, J.W.; Fishbeck, K. Symbiotic nitrogen fixation in Ceanothus roots. Am. J. Bot. 1978, 65, 63–69, doi:10.2307/2442555.
[35]
Brewer, J.S. A demographic analysis of fire-stimulated seedling establishment of Sarracenia alata (Sarraceniacae). Am. J. Bot. 2001, 88, 1250–1257, doi:10.2307/3558336.
[36]
Müller, K.F.; Borsch, T.; Legendre, L.; Porembski, S.; Barthlott, W. Recent progress in understanding the evolution of carnivorous Lentibulariaceae (Lamiales). Plant Biol. 2006, 8, 748–757, doi:10.1055/s-2006-924706.
[37]
Moran, J.A.; Clarke, C.; Gowen, B.E. The use of light in prey capture by the tropical pitcher plant Nepenthes aristolochioides. Plant Signal. Behav. 2012, 7, 957–960, doi:10.4161/psb.20912.
[38]
Jaffi, K.; Blum, M.S.; Fales, H.M.; Mason, R.T.; Cabrera, A. Insect attractants from pitcher plants of the genus Heliamphora (Sarraceniacae). J. Chem. Ecol. 1995, 21, 379–384, doi:10.1007/BF02036725.
[39]
Adamec, L. Mineral nutrition of carnivorous plants: A review. Bot. J. 1997, 63, 273–299.
[40]
Ellison, A.M.; Gotelli, N.J. Nitrogen availability alters the expression of carnivory in the northern pitcher plant, Sarraceniapurpurea. Proc. Natl. Acad. Sci. USA 2002, 99, 4409–4412, doi:10.1073/pnas.022057199.
[41]
Volkov, A.G.; Adesina, T.; Markin, V.S.; Jovanov, E. Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiol. 2008, 146, 694–702.
Jaffe, K.; Michelangeli, F.; Gonzalez, J.M.; Miras, B.; Ruiz, M.C. Carnivory in Pitcher Plants of the Genus Heliamphora (Sarraceniaceae). New Phytol. 1992, 122, 733–744.
[44]
Gaume, L.; Forterre, Y. A viscoelastic deadly fluid in carnivorous pitcher plants. PLoS One 2007, 2, e1185, doi:10.1371/journal.pone.0001185.
[45]
Joel, D.M. Mimicry and mutualism in carnivorous pitcher plants (Sarraceniaceae, Nepenthaceae, Cephalotaceae, Bromeliaceae). Biol. J. Linn. Soc. 1988, 35, 185–197, doi:10.1111/j.1095-8312.1988.tb00465.x.
[46]
Fielding, D.J.; Trainor, E.; Zhang, M. Diet influences rates of carbon and nitrogen mineralization from decomposing grasshopper frass and cadavers. Biol. Fertil. Soils 2012, doi:10.1007/s00374-012-0702-5.
[47]
Hunter, M.D. Insect population dynamics meets ecosystem ecology: Effects of herbivory on soil nutrient dynamics. Agr. For. Entomol. 2001, 3, 77–84, doi:10.1046/j.1461-9563.2001.00100.x.
[48]
Frost, C.J.; Hunter, M.D. Recycling of nitrogen in herbivore feces: Plant recovery, herbivore assimilation, soil retention, and leaching losses. Oecologia 2007, 151, 42–53, doi:10.1007/s00442-006-0579-9.
[49]
Zaady, E.; Groffman, M.; Shachak, M.; Wilby, A. Consumption and release ofnitrogen by the harvester termite Anacanthotermes ubachi navas in the northern Negev desert, Israel. Soil Biol. Biochem. 2003, 35, 1299–1303, doi:10.1016/S0038-0717(03)00200-1.
[50]
Lovett, G.M.; Ruesink, A.E. Carbon and nitrogen mineralization from decomposing gypsy moth frass. Oecologia 1995, 104, 133–138, doi:10.1007/BF00328577.
[51]
Hollinger, D.Y. Herbivory and the cycling of nitrogen and phosphorus in isolated California oak trees. Oecologia 1986, 70, 291–297, doi:10.1007/BF00379254.
Sánchez, C. Lignocellulosic residues: Biodegradation and bioconversion by fungi. Biotechnol. Adv. 2009, 27, 185–194, doi:10.1016/j.biotechadv.2008.11.001.
[54]
George, E.; Marschner, H.; Jakobsen, I. Role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Crit. Rev. Biotechnol. 1995, 15, 257–270, doi:10.3109/07388559509147412.
[55]
Marschner, H.; Dell, B. Nutrient uptake in mycorrhizal symbiosis. Plant Soil 1994, 159, 89–102.
[56]
Govindarajulu, M.; Pfeffer, P.E.; Jin, H.; Abubaker, J.; Douds, D.D.; Allen, J.W.; Bucking, H.; Lammers, P.J.; Shachar-Hill, Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 2005, 435, 819–823, doi:10.1038/nature03610.
Talbot, J.M.; Allison, S.D.; Treseder, K.K. Decomposers in disguise: Mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 2008, 22, 955–963, doi:10.1111/j.1365-2435.2008.01402.x.
[60]
Harrison, M.J. Biotrophic interfaces and nutrient transport in plant/fungal symbioses. J. Exp. Bot. 1999, 63, 1013–1022.
[61]
Gaude, N.; Bortfeld, S.; Duensing, N.; Lohse, M.; Franziska, K. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo a massive and specific reprogramming during arbuscular mycorrhizal development. Plant J. 2012, 69, 510–528, doi:10.1111/j.1365-313X.2011.04810.x.
[62]
Kobae, Y.; Tamura, Y.; Takai, S.; Banba, M.; Hata, S. Localized expression of arbus-cular mycorrhiza-inducible ammonium trans-porters in soybean. Plant Cell Physiol. 2010, 51, 1411–1415, doi:10.1093/pcp/pcq099.
[63]
Wulf, A.; Manthey, K.; Doll, J.; Perlick, A.M.; Linke, B.; Bekel, T.; Folker, M.; Franken, P.; Kuster, H.; Kranjinski, F. Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Am. Phytopath. Soc. 2003, 16, 306–314.
[64]
Benedetto, A.; Magurno, F.; Bonfante, P.; Lanfranco, L. Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 2005, 15, 620–627, doi:10.1007/s00572-005-0006-9.
[65]
Harrison, M.J. A sugar transporter from Medicago truncatula: Altered expression pat-terns in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J. 1996, 9, 491–503.
[66]
Pearson, J.N.; Jakobsen, I. Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol. 1993, 124, 481–488, doi:10.1111/j.1469-8137.1993.tb03839.x.
[67]
Hobbie, J.E.; Hobbie, E.A. 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in arctic tundra. Ecology 2006, 87, 816–822, doi:10.1890/0012-9658(2006)87[816:NISFAP]2.0.CO;2.
[68]
Newsham, K.K. A meta-analysis of plant responses to dark septate root endophytes. New Phytol. 2011, 190, 783–193, doi:10.1111/j.1469-8137.2010.03611.x.
[69]
Usuki, F.; Narisawa, K. A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chae-tospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 2007, 99, 175–184, doi:10.3852/mycologia.99.2.175.
[70]
Hashiba, T.; Narisawa, K. The development and endophytic nature of the fungus Heteroconium chaetospira. FEMS Microbiol. 2005, 252, 191–196, doi:10.1016/j.femsle.2005.08.039.
[71]
Porras-Alfaro, A.; Bayman, P. Hidden fungi, emergent properties: Endophytes and microbiomes. Annu. Rev. Phytopathol. 2011, 49, 291–315, doi:10.1146/annurev-phyto-080508-081831.
[72]
Sasan, R.K.; Bidochka, M.J. The insect-pathogenic fungus Metarhizium robertsii (Claviciptaceae) is alos in endophyte that stimulates plant root development. Am. J. Bot. 2012, 99, 101–107, doi:10.3732/ajb.1100136.
[73]
Akello, J.; Dubois, T.; Gold, C.S.; Coyne, D.; Nakavuma, J.; Paparu, P. Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.). J. Invertebr. Pathol. 2007, 96, 34–42, doi:10.1016/j.jip.2007.02.004.
[74]
Roberts, D.W.; Hajek, A.E. Entomopathogenic fungi as bioinsecticides. In Frontiers of Industrial Mycology; Leatham, G.F., Ed.; Chapman and Hall: New York, NY, USA, 1992; pp. 114–159.
[75]
Arnold, A.E.; Lutzoni, F. Diversity and host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots? In Ecology; 2007; Volume 88, pp. 541–549.
Behie, S.W.; Padilla-Guerrero, I.E.; Bidochka, M.J. Nutrient transfer to plants by phylogenetically diverse fungi suggests convergent evolutionary strategies in rhizospheric symbionts. Commun. Integr. Biol. 2013, 6, 1–4.
[78]
Plummer, G.L.; Kethley, J.B. Foliar absorption of amino acids, peptides, and other nutrients by the pitcher plant, Sarracenia flava. Bot. Gaz. 1964, 125, 245–260.
