Browse Subject Areas

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Fungal Endophyte Diversity in Sarracenia

  • Anthony Glenn,

    Affiliation Toxicology and Mycotoxin Research Unit, Russell Research Center, United State Department of Agriculture Agricultural Research Service, Athens, Georgia, United States of America

  • Michael S. Bodri

    Affiliation Department of Biology, North Georgia College & State University, Dahlonega, Georgia, United States of America

Fungal Endophyte Diversity in Sarracenia

  • Anthony Glenn, 
  • Michael S. Bodri


Fungal endophytes were isolated from 4 species of the carnivorous pitcher plant genus Sarracenia: S. minor, S. oreophila, S. purpurea, and S. psittacina. Twelve taxa of fungi, 8 within the Ascomycota and 4 within the Basidiomycota, were identified based on PCR amplification and sequencing of the internal transcribed spacer sequences of nuclear ribosomal DNA (ITS rDNA) with taxonomic identity assigned using the NCBI nucleotide megablast search tool. Endophytes are known to produce a large number of metabolites, some of which may contribute to the protection and survival of the host. We speculate that endophyte-infected Sarracenia may benefit from their fungal associates by their influence on nutrient availability from within pitchers and, possibly, by directly influencing the biota within pitchers.


The carnivorous North American genus Sarracenia is represented by 9 species of wet savannah and bog-associated herbaceous perennial plants characterized by hollow cylindrical or tubular pitfall-trap leaves bounded by a lid or hood and arranged in circular rosettes. The modified leaves (pitchers), typically 1/6 to 1/3 fluid-filled, are attractive to arthropods due to their conspicuous color and secreted nectar. Pitchers are differentiated into 4–5 Hooker zones [1], as described in [2], each with a specialized function (Fig. 1). Zone 1, attraction, is the pitcher lid, containing nectar glands. Zone 2, conduction, includes the pitcher lip and extends partially into the tubular portion of the pitcher. It produces nectar as well as a powdery ablative waxy material that can interfere with arthropod locomotion. Zone 3, glandular, contains sunken glands that produce digestive enzymes. Zone 4, digestion/absorption, is submerged by the fluid contained within the pitcher. The lack of cuticle within this zone enhances nutrient absorption. Zone 5, present only in S. purpurea L. (Purple Pitcher Plant) and S. rosea Naczi, Case and R.B. Case (Burke's Southern Pitcher Plant) and at the bottom of the trap, has no known function although it has some similarity to zone 3. Although prey capture differs slightly among the species, the ultimate fate of the prey is to die within the pitcher, generally at the bottom, where they are digested by enzymes secreted by the plant [3] and/or by the resident microbial and small invertebrate community [4]. Zone 4 has received the majority of scientific attention because, in addition to the digestive enzymes produced by the plants, it contains “a microcosm composed of larval insects, fungi, algae, rotifers, nematodes, and bacteria that, together, ultimately break down nutrients from insect prey for the plant” [5]. Additionally, this microcosm is potentially amenable to analysis and manipulation of its inhabitants, allowing for detailed experimental study of their role and impact.

Figure 1. Sagittal section of Sarracenia purpurea illustrating the 5 Hooker zones.

Zone 1, attraction; zone 2, conduction; zone 3, glandular; zone 4, digestion/absorption; zone 5, no known function although it has some similarity to zone 3. (Photograph © Barry Rice,

The evolution of carnivory is partially attributed to the adaptation and persistence of these plants to nutrient-poor habitats [6]. Beginning with Darwin [7], multiple studies have addressed the different facets of carnivory and its independent evolution 6 times in 5 angiosperm orders [8]. Givnish et al. [9] and Benzing [10] postulated, in cost-benefit models, that carnivory evolved to provide increased nutrients and impart an energetic advantage to plants found in environments limited in nutrients but not water and sunlight. In Sarracenia, these studies typically examine the composition and role played in nutrient availability, transformation and allocation by the microecosytem that exists within pitchers [4], [5], [11][15].

Little attention has been paid to nutrient capture by roots of carnivores. Most species are restricted to extremely nitrogen-limited habitats and subsequently, in the case of Sarracenia, acquire up to 80% of their nitrogen from prey captured in their leaves rather than from weakly developed root systems [15]. Because construction costs of traps is comparable to that of rhizomes and roots in Sarracenia [16], it is advantageous for these plants to invest in structures that have a better chance of nutrient capture. The poorly developed root structures and primary mode of nutrient acquisition via the modified leaves led to the belief that carnivorous plants lacked mycorrhizal associations even though the roots may occasionally be colonized by facultative mycorrhizas [17]. Fungal hyphae that colonize plant root tissue without any deleterious effects are often endophytic species [18].

Rodriguez et al. [19] are of the opinion that all plants in natural ecosystems are symbiotic with fungal endophytes that, in turn, influence their evolution and ecology [20], the community structure of the plants [21], and the other organisms associated with the plant [22]. Bioactive compounds [23] and enzymes [24] produced by endophytes are thought to possibly influence nutrition and/or growth of the endophyte. These same chemicals could theoretically affect the microcosm present within the pitchers of Sarracenia and therefore nutrient availability to the plant. Because endophytes have the ability to influence the communities associated with an infected plant, this study was undertaken to ascertain the presence of Sarracenia pitcher endophytes and the restricted distribution, if any, of the endophytes to the different Hooker zones. In this preliminary study we wish to hereby report the existence of fungal endophytes within the leaf tissue of multiple Sarracenia species and further report the first instance of carnivorous plant endophytes cultured specifically from leaves. In addition, we speculate on the possible roles these endophytes may play in regards to the digestive processes and nutrient utilization of their host plants.


Of the 7 individual pitchers collected from S. oreophila, bacteria were cultured on brain-heart infusion from 4 individual plants and only from Hooker zone 3–4 after 4 days of incubation at 25°C. As only 10 morphologically similar bacterial colonies were produced from over 168 leaf sections of S. oreophila, no further attempts were made to isolate bacteria from other species of pitcher plant. All subsequent investigations targeted growth and isolation of fungal endophytes.

Fungi were isolated from all 4 species of Sarracenia and from Hooker zones 2–3 and 3–4, with almost 100% of pieces positive for endophytes (data not shown). Histological sections were examined microscopically for the presence of fungal hyphae. Vegetative fungal hyphae were observed and appeared to be confined to the intercellular spaces (Fig. 2).

Figure 2. Gross and histological appearance of a fungal isolate of Sarracenia oreophila.

A, Appearance of Colletotrichum gloeosporioides #3 isolated from S. oreophila on potato dextrose agar and B, in a hand-cut thick tissue section (400× magnification) stained in 1% acid fuchsin. Note the fungal hyphae growing between cells denoted by the arrow.

S. purpurea harbored the greatest diversity of endophytes based upon the DNA sequencing of dissimilar morphotypes as no isolate was represented more than once and none were isolated from the other Sarracenia species (Table 1). In contrast, S. minor was infected with only a single species, Colletotrichum gloeosporioides (Penz.) Penz. and Sacc. Overall, Colletotrichum spp. was the most common genus, infecting at least one plant of each Sarracenia species. Three ITS alleles were identified among the isolates of C. gloeosporioides. Two alleles were identified in the isolates from S. minor and differed at 2 nucleotide positions. These 2 alleles each differed at 11 nucleotide positions compared to the third C. gloeosporioides allele in the 2 isolates from S. oreophila.

Table 1. Fungal endophyte isolates from Sarracenia identified based on sequence data from the internal transcribed spacer regions of nuclear ribosomal DNA (ITS rDNA).

Both the Ascomycota and Basidiomycota phyla were represented by endophytes from Sarracenia leaves. Four unidentified basidiomycetes were isolated from S. psittacina and S. purpurea (2 species each). All megablast ITS rDNA queries identified GenBank accessions with E-values of zero (identities >97%), except for endophyte strain SPs5-1 (Table 1), which was most similar to a basidiomycete accession (EU622841) with an E-value of 1e-176, which indicates this Sarracenia endophyte may not have been previously sequenced and deposited in the GenBank database or may represent a novel taxon. In addition to the ascomycete Colletotrichum of the class Sordariomycetes (order Glomerellales), 5 additional orders from 4 classes were represented: Pleosporales (Dothideomycetes); Diaporthales and Xylariales (Sordariomycetes); Eurotiales (Eurotiomycetes); and Helotiales (Leotiomycetes) (Fig. 3).

Figure 3. Representational phylogeny showing the taxonomic distribution of fungal endophytes isolated from Sarracenia.

Fungi isolated in this study are denoted by an asterisk [*] following the taxa name.


The highly diverse nonclavicipitaceous endophytes can be divided into 3 functional groups based upon host colonization patterns, mechanism of transmission, biodiversity levels within plant tissues and ecological function [19]. All classes have broad host ranges but class 3 exist as highly localized independent infections restricted to above ground plant tissues allowing for extremely high in planta biodiversity while class 4 are primarily ascomycetous fungi restricted to roots where they form inter- and intracellular hyphae and microsclerotia and are capable of extensive tissue colonization [19]. Members of class 2, species within the Ascomycota or Basidiomycota such as the fungi we have isolated from leaves of Sarracenia species, infect and colonize via appressoria or by direct penetration by hyphae [25]. Some are known to confer fitness benefits to their host, especially if there are habitat-specific selective pressures placed on the host [26]. These selective pressures have been associated with pH, temperature, drought, and salinity but also likely include growth in nutrient-deficient soils. Class 2 endophytes have also been demonstrated to increase plant biomass under stressful conditions [19]. Colonization of Sarracenia plants by endophytes in the spring may account for the subsequent increase in pitcher size observed over the course of the growing season particularly for S. leucophylla. Many endophytes produce phytohormones such as indole-3-acetic acid, cytokines, and other plant growth-promoting substances [27]. We also speculate that endophyte-infected plants benefit from their fungal associates by their influence on nutrient availability from within pitchers and, possibly, by directly influencing the biota within the pitchers. Tan and Zou [27] postulate that horizontal gene transfer may explain why some endophytes are capable of producing phytochemicals characteristic of the host. Although speculative at this point, carnivorous host plants may have co-evolved along with fungi and now rely on endophytes for production or augmentation of levels of some of the digestive enzymes found within their pitchers.

Cost-benefit models predict that carnivory could result in an increased rate of photosynthesis manifested in one form as an increase in total leaf mass, but experiments to support this have been equivocal [13], [28], [29]. While most nutrient supplementation studies do identify a significant increase in growth, excess nutrients may not lead directly to increased photosynthetic rates [8]. Cyperus erythrorhizos Muhl. (Redroot Flatsedge), a C4 plant growing in nutrient deficient wetlands, habitat similar to that for many Sarracenia, have a high photosynthetic nitrogen use efficiency (PNUE) [30] in contrast to the low PNUE of Sarracenia [13], which are likely C3 plants. The activity of endophytes within pitcher plant leaf tissue may explain the PNUE observations in comparison to non-carnivorous plants growing in similar habitats. The presence of endophytes could also help discern why discordant data exists between the construction costs of carnivorous leaves versus phyllodia, help elucidate how carbon derived from prey is utilized, and further clarify the relationship between plant biomass and photosynthesis in nutrient-manipulated plants. For example, non-feeding Sarracenia are phosphorus-limited or nitrogen+phosphorus co-limited while artificially fed plants are more strongly nitrogen-limited [13]. Of the nitrogen available from prey, 60% is sequestered by bacteria in the pitchers [4], [31]. Over a growing season, plants will rely on prey-based phosphorus to boost photosynthetic efficiency due to nitrogen-limitation from bacterial sequestration [13]. It has been observed that endophyte growth limitation by lack of an adequate nitrogen source or phosphate components of the nutritional environment leads to the synthesis of secondary metabolites [32] and these metabolites, released into the plant tissue or pitcher milieu, can alter growth characteristics if they are plant growth regulators or impact the micro-organisms present within the pitcher if antimicrobial in nature.

The endophyte isolates of Sarracenia may contribute to their hosts' fitness by means of the production of biologically active compounds. Basidiomycetous endophytes are rarely isolated from higher plants and these are often orchid mycorrhizas [33]. While many of these latter species are associated with white rot and brown rot of trees and may be saprobes or latent pathogens, their production of lignocellulolytic enzymes and potential to produce bioactive secondary metabolites may favor their association with Sarracenia pitchers. S. purpurea, for example, from which two basidiomycete isolates were obtained, has open pitchers that often accumulate plant debris. Degradation of captured plant debris by these fungi would be beneficial to host and endophyte.

Every Ascomycota endophyte taxa isolated from Sarracenia in this study has been proven to produce biologically active compounds. Two isolates representative of the Pleosporales were found, one being a member of the polyphyletic anamorph Paraconiothyrium/Coniothyrium and the other being an unidentified taxon. Members of the Pleosporales exhibit a diversity of habits, including parasites, saprobes, and endophytes [34]. Preussomerins, isolated from various fungi, including Edenia gomezpompae M.C. González, Anaya, Glenn, Saucedo, and Hanlin, a Pleosporales endophyte of Callicarpa, possess a wide range of biological properties, including antibacterial, algicidal, herbicidal, antiplasmodial, antitumor, and antifungal activities, including inhibition of other endophytes and phytopathogens [35]. Interestingly, the genus Paraconiothyrium was erected to segregate mycoparasitic species from Coniothyrium species [36]. An endophyte that utilized other fungi as a food source could influence competition for resources within the flooded and enzyme-poor pitchers of S. purpurea, from which this isolate was made.

Endophytic penicillia are widespread and heterogenous, and various species have been reported as endophytes of plants with 20 species of Penicillium isolated from the roots of Picea mariana (Miller) Britton Sterns, and Poggenburg (Black Spruce) alone [37]. By the end of 1984, over 380 biologically active metabolites were known from Penicillium [32] and even more are now known. Of the 6450 biologically active compounds identified from microfungi up through 2009, over 30% have been obtained from Aspergillus and Penicillium [38] and these compounds exhibit a vast diversity of activity.

Cryptosporiopsis spp. (teleomorph Pezicula spp.) have had biologically active compounds isolated that exhibit antibacterial, antifungal and algicidal activities [39]. Echinocandin isolated from Cryptosporiopsis sp. and Pezicula sp. was shown, in vitro, to inhibit pathogens of the respective host plants [40]. Many strains of Pezicula synthesize, in vitro, fungicidal compounds such as mullein, mycorrhizin, epi-ethiosolide, cryptosporopsin, and cryptocandin [39], [41] postulated to help it to maintain a mutualistic role with its host.

Potent antifungal agents, the sordarins, are synthesized by members of the Xylariales, a trait more frequently attributed to this group than to any other fungal order [42]. Species of Xylaria have been shown to produce potent antifungal and antibacterial metabolites [43]. The Xylariales may either be colonizers that will later decompose cellulose when the host plant dies or be true endophytes, although obvious benefits to the host plant have yet to be documented [44].

Phomopsis and Colletotrichum are common isolates from dicot leaves and frequently dominate endophyte assemblages of the host [45]. Phomopsis spp. are not host specific and exhibit high host variability. The genus is a very rich source of secondary biological compounds with antifungal, herbicidal, algicidal, antimicrobial, and plant growth regulating activities [46].

Fungi of the genus Colletotrichum are well documented as significant plant endophytes [47][50]. C. gloeosporioides in particular has been reported from at least 470 host genera and more than 2000 taxa [51] primarily as a host-specific pathogen although C. gloeosporioides is now recognized as a broadly defined species complex that contains multiple clades, each of which may represent a genetically isolated species [52]. Lu et al. [50] isolated metabolites of a Colletotrichum sp. from Artemisia annua and Zou et al. [23] similarly isolated metabolites of C. gloeosporioides from Artemisia mongolica that have antimicrobial and antifungal properties. Tan and Zou [27] found that culture broth from C. gloeosporioides could promote the growth of host callus. As this genus was represented in every species of Sarracenia studied, and isolated multiple times, there is great potential for a mutualistic relationship between this endophyte and host that could be further elucidated by an examination of the secondary products, if any are produced by the fungus and compared to the native metabolites and enzymes produced by sterile plants. Furthermore, some light could be shed on the problem of nutrient limitation and stoichiometry of carnivorous plants should sterile and endophyte-infected plants be utilized and compared under experimental conditions.

It is well established that some of the large number of metabolites produced by endophytes offer a significant benefit to their host plant [27]. These benefits could contribute to the protection and survival of the host by acting as growth regulators, antimicrobials, and mediators of environmental stress. In the case of Sarracenia, these metabolites could have an even broader impact due to the unique structure of the trap leaf, which would function to capture and store excreted materials within the pitcher where the chemicals would interact with prey as well as a complex microcosm of associated organisms.

This is the first instance of Coniothyrium/Paraconiothyrium, Penicillium, Cryptosporiopsis, Phomopsis and Colletotrichum spp. ascertained to be endophytes of the family Sarraceniaceae and, to our knowledge, the first report of fungal endophytes of leaves of any carnivorous and proto-carnivorous plant family. The isolation of Colletotrichum spp. from multiple Sarracenia individuals of all 4 species at locations 300+ miles apart, as well as during different years, strongly suggests that at least this fungal genus is a true pitcher plant endophyte. This study only concerned the isolation of fungal endophytes. Our preliminary assay also indicates a potential diversity of bacterial endophytes as well. The role, if any, of the fungal endophytes we isolated from Sarracenia is unknown as is whether they produce any biological compounds that may be of benefit to the plants. At this time it is unknown if these endophytes truly contribute to carnivory in Sarracenia and further investigation concerning the role of endophytes and/or their metabolites in successful carnivory is highly desired.

Materials and Methods

A single mature pitcher was collected from 7–8 different individuals of 4 species of Sarracenia (S. minor Walter [Hooded Pitcher Plant], S. oreophila [Kearney] Wherry [Green Pitcher Plant], S. psittacina Michaux [Parrot Pitcher Plant], S. purpurea). Sampling of S. oreophila, a critically endangered species only found in small isolated populations scattered in 7 non-coastal plain counties in 3 southeastern states, was permitted by the Georgia Chapter of the Nature Conservancy in August 2006. S. minor and S. psittacina were sampled in July 2009 under permit by the U.S. Fish and Wildlife Service, Okefenokee National Wildlife Refuge. S. minor and S. psittacina are coastal plain inhabitants. Ranging from extreme southeastern North Carolina to northern Florida, S. minor is found in 119 counties in 4 states. S. psittacina is irregularly distributed in 67 counties in 6 states. Highlands Biological Station, an interinstitutional research center of the University of North Carolina, permitted sampling of S. purpurea, also in July of 2009. S. purpurea has the most expansive range of all Sarracenia. It is found in 25 states as well as Canada. The individuals sampled in the mountains of western North Carolina are considered a disjunct population of S. purpurea ssp. purpurea. Populations of all plants sampled were natural stands with minimal human impact. In addition to the temporal isolation by collection date, S. minor and S. psittacina are geographically isolated from S. oreophila and S. purpurea by more than 300 miles. S. oreophila and S. purpurea sites are approximately 50 miles apart and separated by mountains. Species were selected to represent erect (S. oreophila, S. minor) or decumbent (S. psittacina, S. purpurea) pitcher habit as well as lids that are open (S. oreophila, S. purpurea) or overhanging (S. minor, S. psittacina). These 4 species, in addition to the contrasting morphologies, also differ by means of their digestive physiologies. All pitchers were live (no sign of senescence), firm, and green and assumed to be free of disease. Pitchers were processed for endophyte culture within 24 hours of collection.

A culture dependent approach was utilized to isolate endophytes. This approach, by the nature of the isolation technique, does influence the species of endophyte that can be isolated. Pitchers were cut longitudinally and washed carefully for 1 hr under running tap water with the addition of dishwashing soap. Pitcher halves were then further sectioned to represent Hooker zones 2–3 and 3–4, conduction-glandular and glandular-digestion/absorption respectively. The top and bottommost sections were discarded. These retained sections were surface sterilized by dipping into 95% EtOH for 1 min followed by immersion in a 10% household bleach plus Tween-20 (3 drops/100 ml) solution for 10 min. A second alcohol dip of 30 sec duration preceded a final wash in sterile ultra-pure water. Sterilized leaf sections were cleaved aseptically into a minimum of 12 small segments, approximately 3 mm×3 mm, and placed onto 2% water agar. Sterilized sections of leaf from S. oreophila were also placed onto 3.7% brain-heart-Infusion agar (Bacto™ Brain Heart Infusion, Becton, Dickinson and Company, Sparks, MD). Incubation of samples was performed in the dark at 25°C until the outgrowth of endophytes from the cut edges of the leaf material was discerned. Hyphal tips originating from leaf segments on water agar were transferred to Petri dishes containing potato dextrose agar (PDA; Difco™ Potato Dextrose Agar, Becton, Dickinson and Company, Sparks, MD), grown for 8–10 d, and periodically checked for culture purity. Pure cultures were obtained by hyphal tipping onto PDA so that morphology of the fungal culture could be observed. Fungi were grouped into morphotypes based upon appearance on PDA. Selected isolates within dissimilar morphotypes from each Sarracenia species were utilized for sequencing.

Representative leaf sections from which fungi were cultured were preserved and stained in 1% acid fuchsin and cleared in 85% lactic acid in preparation for later histological processing. Histology was performed by embedding plant sections in JB-4 (JB-4 Mini Kit, Polysciences, Inc., Warrington, PA) following dehydration in ascending grades of EtOH baths and infiltration of the polymer according to the manufacturer's directions. Sectioning was done with a microtome (Energy Beam Sciences, Inc., JB-4, Energy Beam Sciences, East Granby, CT) utilizing a glass knife or preserved sections were cut by hand with razor blades.

The identity of fungal isolates was determined based on PCR amplification and sequencing of the internal transcribed spacer sequences of nuclear ribosomal DNA (ITS rDNA). DNA was isolated from fungal cultures using a Bio-Rad Aqua Pure Genomic DNA Kit (Bio-Rad Laboratories, Hercules, CA). The ITS rDNA region (ITS1-5.8S rDNA-ITS2) was amplified and sequenced using primers ITS5 and ITS4 as previously described [53]. Sequencing was performed by the United States Department of Agriculture–Agricultural Research Service South Atlantic Area Sequencing Facility (Athens, GA, USA). The DNA sequences were deposited in GenBank (Table 1). Taxonomic identity of strains was assigned using the NCBI nucleotide megablast search tool ( A threshold of 97%, the lowest identity observed for any of the blast searches, was used to determine the identity of the sequences. Only ITS nucleotide accessions associated with voucher strains were considered for taxonomic assignment of the Sarracenia endophytes.


Sampling of S. oreophila was permitted by the Georgia Chapter of The Nature Conservancy. S. minor and S. psittacina were sampled under permit by the U.S. Fish and Wildlife Service, Okefenokee National Wildlife Refuge. Highlands Biological Station, an inter-institutional research center of the University of North Carolina, permitted sampling of S. purpurea.

Author Contributions

Conceived and designed the experiments: AG MSB. Performed the experiments: AG MSB. Analyzed the data: AG MSB. Contributed reagents/materials/analysis tools: AG MSB. Wrote the paper: AG MSB.


  1. 1. Hooker JD (1859) On the origin and development of the pitcher of Nepenthes, with an account of some new Bornean plants of the genus. Transactions of the Linnean Society of London 22: 415–424.
  2. 2. Lloyd FE (1976) The carnivorous plants. New York: Dover Publishing Inc. 352 p.
  3. 3. Hepburn JS, Jones FM (1927) The enzymes of the pitcher liquor of Sarraceniaceae. Transactions of the Wagner Free Institute of Science 11: 49–68.
  4. 4. Butler JL, Gotelli NJ, Ellison AM (2008) Linking the brown and green: Nutrient transformation and fate in the Sarracenia microecosystem. Ecology 89: 898–904.
  5. 5. Koopman MM, Fuselier DM, Hird S, Carstens BC (2010) The carnivorous pale pitcher plant harbors diverse, distinct, and time-dependent bacterial communities. Applied and Environmental Microbiology 76: 1851–1860.
  6. 6. Gallie DR, Chang S-C (1997) Signal transduction in the carnivorous plant Sarracenia purpurea. Regulation of secretory hydrolase expression during development and in response to resources. Plant Physiology 115: 1461–1471.
  7. 7. Darwin C (1875) Insectivorous plants. Available: via the Internet. Accessed 17 June 2011.
  8. 8. Ellison AM, Gotelli NJ (2009) Energetics and the evolution of carnivorous plants –Darwin's ‘most wonderful plants in the world’. Journal of Experimental Botany 60: 19–42.
  9. 9. Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD (1984) Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist nutrient-poor habitats. American Naturalist 124: 479–497.
  10. 10. Benzing DH (2000) Bromeliaceae: Profile of an adaptive radiation. Cambridge: Cambridge University Press. 710 p.
  11. 11. Gray SM, Miller TE, Mouquet N, Daufresne T (2006) Nutrient limitation in detritus-based microsocms in Sarracenia purpurea. Hydrobiologia 573: 173–181.
  12. 12. Siragusa AJ, Swenson JE, Casamatta DA (2007) Culturable bacteria present in the fluid of the hooded-pitcher plant Sarracenia minor based on 16S rDNA gene sequence data. Microbial Ecology 54: 324–331.
  13. 13. Farnsworth EJ, Ellison AM (2008) Prey availability directly affects physiology, growth, nutrient allocation and scaling relationships among leaf traits in 10 carnivorous plant species. Journal of Ecology 96: 213–221.
  14. 14. Peterson CN, Day S, Wolfe BE, Ellison AM, Kolter R, et al. (2008) A keystone predator controls bacterial diversity in the pitcher-plant (Sarracenia purpurea) microecosystem. Environmental Microbiology 10: 2257–2266.
  15. 15. Karagatzides JD, Butler JL, Ellison AM (2009) The pitcher plant Sarracenia purpurea can directly acquire organic nitrogen and short-circuit the inorganic nitrogen cycle. PLoS ONE 4: 1–9.
  16. 16. Karagatzides JD, Ellison AM (2009) Construction costs, payback times, and the leaf economics of carnivorous plants. American Journal of Botany 96: 1612–1619.
  17. 17. Crowder AA, Pearson MC, Grubb PJ, Langlois PH (1990) Biological flora of the British Isles: Drosera. Journal of Ecology 78: 233–267.
  18. 18. Quilliam RS, Jones DL (2010) Fungal root endophytes of the carnivorous plant Drosera rotundifolia. Mycorrhiza 20: 341–348.
  19. 19. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: Diversity and functional roles. New Phytologist 182: 314–330.
  20. 20. Brundrett MC (2006) Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In: Schulz BJE, Boyle CJC, Sieber TN, editors. Microbial Root Endophytes. Berlin: Springer-Verlag. pp. 281–293.
  21. 21. Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285: 1742–1745.
  22. 22. Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409: 78–81.
  23. 23. Zou WX, Meng JC, Lu H, Chen GX, Shi GX, et al. (2000) Metabolites of Colletotrichum gloeosporioides, an endophytic fungus in Artemisia mongolica. Journal of Natural Products 63: 1529–1530.
  24. 24. Li HM, Sullivan R, Moy M, Kobayashi DY, Belanger FC (2004) Expression of a novel chitinase by the fungal endophyte in Poa ampla. Mycologia 96: 526–536.
  25. 25. Ernst M, Mendgen KW, Wirsel SGR (2003) Endophytic fungal mutualists: Seed-borne Stagonospora spp. enhance reed biomass production in axenic microcosms. Molecular Plant-Microbe Interactions 16: 580–587.
  26. 26. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, et al. (2008) Stress tolerance in plants via habitat-adapted symbiosis. International Society of Microbial Ecology 2: 404–416.
  27. 27. Tan RX, Zou WX (2001) Endophytes: A rich source of functional metabolites. Natural Product Reports 18: 448–459.
  28. 28. Ellison AM, Gotelli NJ (2002) Nitrogen availability alters the expression of carnivory in the northern pitcher plant Sarracenia purpurea. Proceedings of the National Academy of Sciences USA 99: 4409–4412.
  29. 29. Wakefield AE, Gotelli NJ, Whittman SE, Ellison AM (2005) The effect of prey addition on nutrient stoichiometry, nutrient limitation, and morphology of the carnivorous plant Sarracenia purpurea (Sarraceniaceae). Ecology 86: 1737–1743.
  30. 30. Faulkner AA, Holland MM, Moore MT, Cooper CM (2006) Nitrogen use efficiency of c3 and c4 wetland Cyperus species in a long-term greenhouse experiment. 91st Annual Meeting of the Ecological Society of America, Memphis, Tennessee.
  31. 31. Butler JL, Ellison AM (2007) Nitrogen cycling dynamics in the carnivorous pitcher plant, Sarracenia purpurea. Functional Ecology 21: 835–843.
  32. 32. Mantle PG (1987) Secondary metabolites of Penicillium and Acremonium. In: Peberdy JF, editor. Penicillium and Acremonium. New York: Plenum Press. pp. 161–243.
  33. 33. Rungjindamai N, Pinruan U, Choeyklin R, Hattori T, Jones EBG (2008) Molecular characterization of basidiomycetous endophytes isolated from leaves, rachis and petioles of the oil palm, Elaeis guineensis, in Thailand. Fungal Diversity 33: 139–161.
  34. 34. Zhang Y, Schoch CL, Fournier J, Crous PW, de Gruyter J, et al. (2009) Multi-locus phylogeny of Pleosporales: A taxonomic, ecological and evolutionary re-evaluation. Studies in Mycology 64: 85–102.
  35. 35. Macías-Rubalcava ML, Hernández-Bautista BE, Jiménez-Estrada , González MC, Glenn AE, et al. (2008) Naphthoquinone spiroketal with allelochemical activity from the newly discovered endophytic fungus Edenia gomezpompae. Phytochemistry 69: 1185–1196.
  36. 36. Verkley GJ, De Silva M, Wicklow DT, Crous PW (2004) Paraconiothyrium, a new genus to accommodate the mycoparasite Coniothyrium minitans, anamorphs of Paraphaeosphaeria, and four new species. Studies in Mycology 50: 323–335.
  37. 37. Stone JK, Bacon CW, White JF Jr (2000) An overview of endophytics microbes: Endophytism defined. In: Bacon CW, White JF Jr, editors. Microbial endophytes. New York: Marcel Dekker, Inc. pp. 3–30.
  38. 38. Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Sasse F, Jansen R, et al. (2009) Fungal endophytes and bioprospecting. Fungal Biology Reviews 23: 9–19.
  39. 39. Schulz B, Sucker J, Aust HJ, Krohn K, Ludewig K, et al. (1995) Biologically active secondary metabolites of Pezicula species. Mycological Research 99: 1007–1015.
  40. 40. Noble HM, Langley D, Sidebottom PJ, Lane SJ, Fisher PJ (1991) An echinocandin from an endophytic Cryptosporiopsis sp. and Pezicula sp. in Pinus sylveslris and Fagus sylvatica. Mycological Research 95: 1439–1440.
  41. 41. Strobel GA, Miller RV, Martinez-Miller C, Condron MM, Teplow DB, et al. (1999) Cryptocandin, a potent antimycotic from the endophytic fungus Cryptosporiopsis cf. quercina. Microbiology 145: 1919–1926.
  42. 42. Vicente F, Basilio A, Platas G, Collado J, Bills GF, et al. (2009) Distribution of the antifungal agents sordarins across filamentous fungi. Mycological Research 113: 754–770.
  43. 43. Brunner F, Petrini O (1992) Taxonomy of some Xylaria species and xylariaceous endophytes by isozyme electrophoresis. Mycological Research 96: 723–733.
  44. 44. Davis EC, Franklin JB, Shaw AJ, Vigalys R (2003) Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: Phylogenetics, distribution, and symbiosis. American Journal of Botany 90: 1661–1667.
  45. 45. Murali TS, Suryanarayanan TS, Geeta R (2006) Endophytic Phomopsis species: Host range and implications for diversity estimates. Canadian Journal of Microbiology 52: 673–680.
  46. 46. Rukachaisirikul V, Sommart U, Phongpaichit S, Sakayaroj J, Kirtikara K (2007) Metabolites from the endophytic fungus Phomopsis sp. PSU-D15. Phytochemistry 69: 783–787.
  47. 47. Smith CS, Chand T, Harris RF, Andrews JH (1989) Colonization of a submersed aquatic plant, Eurasian water milfoil Myriophyllum spicatum, by fungi under controlled conditions. Applied and Environmental Microbiology 55: 2326–2332.
  48. 48. Freeman S, Rodriquez RJ (1993) Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260: 75–78.
  49. 49. Okane I, Nakagiri A, Ito T (1997) Preliminary study of endophytic fungi in evergreen plants from Ishigaki and Iriomote Islands. pp. 45–51. Institute for Fermentation Research Communications (Osaka).
  50. 50. Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Science 151: 67–73.
  51. 51. Sutton BC (1980) The coelomycetes, fungi imperfecti with pycnidia, acervuli and stromata. Oxfordshire: CABI Publishing. 696 p.
  52. 52. Du M, Schardl CL, Nuckles EM, Vaillancourt LJ (2005) Using mating-type gene sequences for improved phylogenetic resolution of Collectotrichum species complexes. Mycologia 97: 641–658.
  53. 53. Glenn AE, Rykard DM, Bacon CW, Hanlin RT (1998) Molecular characterization of Myriogenospora atramentosa and its occurrence on some new hosts. Mycological Research 102: 483–490.