Abstract
A single tropical plant species can harbour hundreds of endophyte species within its tissues. Beyond this, little is known about the relationship between endophyte colonization, leaf traits and spectral properties of leaves. We explore these relationships in Coccoloba cereifera, a plant well known for its symbiotic properties. Endophyte richness in C. cereifera was statistically correlated with leaf traits such as water content, the ratio of fresh weight/dry weight and polyphenol/leaf specific weight. Endophyte diversity was also related to spectral vegetation indices of chlorophyll content. The associations among endophyte diversity, leaf traits and spectral reflectance pose new questions and present new opportunities to better understand plant–fungal symbioses and related leaf optical properties.
Similar content being viewed by others
References
Abe F, Inaba H, Katoh T, Hotchi M (1990) Effects of iron and desferrioxamine on Rhizopus infection. Mycopathologia 110:87–91
Arnold AE (2005) Diversity and Ecology of fungal endophytes in tropical forests. In: Deshmukh S (ed) Current trends in mycological research. Oxford & IBH Publishing Co. Pvt. Ltd., New Delhi, pp 49–68
Arnold AE, Engrelbrecht BMJ (2007) Fungal endophytes nearly double minimum leaf conductance in seedlings of a neotropical tree species. J Trop Ecol 23:369–372
Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549
Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. PNAS 100:15649–15654
Barthod S, Cerovic Z, Epron D (2007) Can dual chlorophyll fluorescence excitation be used to assess the variation in the content of UV-absorbing phenolics compounds in leaves of temperate tree species along a light gradient? J Exp Bot 58:1753–1760
Bissegger M, Sieber TN (1994) Assemblages of endophytic fungi in coppice shoots of Castanea sativa. Mycologia 86:648–655
Cannon PF, Simmons CM (2002) Diversity and host preference of leaf endophytic fungi in the Iwokrama Forest Reserve, Guyana. Mycologia 94:210–220
Carroll GC, Carroll FE (1978) Studies on the incidence of coniferous endophytes in the Pacific Northwest. Can J Botany 56:3034–3043
Carter GA, Knapp AK (2001) Leaf optical properties in higher plants: linking spectral characteristics to stress and chlorophyll concentration. Am J Bot 88:677–684
Castro-Esau KL, Sánchez-Azofeifa GA, Rivard B (2006a) Comparison of spectral indices obtained using multiple spectroradiometers. Remote Sens Environ 103:276–288
Castro-Esau KL, Sánchez-Azofeifa GA, Rivard B, Wright SJ, Quesada M (2006b) Variability in leaf optical properties of Mesoamerican trees and the potential for species classification. Am J Bot 93:517–530
Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297
Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744
Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335
Conover WJ (1980) Practical nonparametric statistics, 2nd edn. Wiley, New York, p 493
Costa-Pinto L, Azevedo JL, Pereira JO, Vieira MLC, Labate CA (2000) Symptomless infection of banana and maize by endophytic fungi impairs photosynthetic efficiency. New Phytol 147:609–615
de Vega C, Ortiz PL, Arista M, Talavera S (2007) The endophytic system of Mediterranean Cytinus (Cytinaceae) developing on five host Cistaceae species. Ann Bot Lond 100:1209–1217
Espinosa-Garcia FJ, Langenheim JH (1990) The endophytic fungal community in leaves of a coastal redwood population-diversity and spatial patterns. New Phytol 116:89–97
Faeth SH, Bultman TL (2002) Endophytic fungi and interactions among host plants, herbivores and natural enemies. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 89–123
Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia 90:14–20
Fisher PJ, Anson AE, Petrini DO (1986) Fungal endophytes in Ulex europaeus and Ulex gallii. T Brit Mycol Soc 86:153–156
Fukshansky LA, Remisowsky AM, McClendon J, Ritterbusch A, Richter T, Mohr H (1993) Absorption spectra of leaves corrected for scattering and distributional error: a radiative transfer and absorption statistics treatment. Photochem Photobiol 57:538–555
Gamboa MA, Bayman P (2001) Communities of endophytic fungi in leaves of a tropical timber tree Guarea guidonia: Meliaceae. Biotropica 33:352–360
Gamon JA, Surfus JS (1999) Assessing leaf pigment content and activity with a reflectometer. New Phytol 143:105–117
Hamayun M, Khan SA, Ahmad N, Tang D-S, Kang S-M, Na C-I, Sohn E-Y, Hwang Y-H, Shin D-H, Lee BH, Kim J-G, Lee I-J (2009) Cladosporium sphaerospermum as a new plant growth-promoting endophyte from the roots of Glycine max L. Merr World J Microbiol Biotechnol 25:627–632
Harborne JB (1989) Methods in plant biochemistry. In: Dey PM, Harborne JB (eds) Plant phenolics, vol 1. Chapman Hall, London, pp 1–28
Holden M (1976) Chlorophylls. In: Goodwin TW (ed) Chemistry and biochemistry of plant pigments, vol 2. Academic Press, London, pp 1–37
Hunt MG, Rasmussen S, Newton PCD, Parsons AJ, Newman JA (2005) Near-term impacts of elevated CO2, nitrogen and fungal endophyte-infection on Lolium perenne L. growth, chemical composition and alkaloid production. Plant Cell Environ 28:1345–1354
Lodge DJ, Fisher PJ, Sutton BC (1996) Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycologia 88:733–738
Lüttge U (2008) Physiological ecology of tropical plants. Springer, Berlin, p 458
Madeira JA, Fernandes GW (1999) Reproductive phenology of sympatric taxa of Chamaecrista Leguminosae. in Serra do Cipó, Brazil. J Trop Ecol 15:463–479
Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940
Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol 133:727–733
Martin F, Duplessis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie F (2001) Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154
Meyer S, Cerovic ZG, Goulas Y, Montpied P, Demotes-Mainard S, Bidel LPR, Moya I, Dreyer E (2006) Relationships between optically assessed poyphenols and chlorophyll contents, and leaf mass per area ratio in woody plants: a signature of the carbon-nitrogen balance within leaves? Plant Cell Environ 29:1338–1348
Moreira RG, McCauley RA, Corttes-Palomec AC, Lovato MB, Fernandes GW, Oyama K (2008) Isolation and characterization of microsatellite loci in Coccoloba cereifera (Polygonaceae), an endangered species endemic to the Serra do Cipo. Brazil Mol Ecol Resour 8:854–856
Moreira RG, McCauley RA, Corttes-Palomec AC, Fernandes GW, Oyama K (2009) Spatial genetic structure of Coccoloba cereifera (Polygonaceae), a critically endangered microendemic species of Brazilian rupestrian fields. Conserv Genet 11:1247–1255
Oki Y, Soares NR, Storquio M, Correa-Junior A, Fernandes GW (2009) The influence of the endophytic fungi on the herbivores from Baccharis dracunculifolia (Asteraceae). Neotrop Biol Conserv 4:83–88
Omacini M, Chaneton EJ, Ghersa CM, Muller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81
Peters S, Aust HJ, Draeger S, Schulz B (1998) Interactions in dual cultures of endophytic fungi with host and nonhost plant calli. Mycologia 90:360–367
Pinar A, Curran PJ (1996) Grass chlorophyll and the reflectance red edge. Int J Remote Sens 17:351–357
Rayner ADM, Boddy L (1986) Population structure and the infection biology of wood-decay fungi in living trees. Adv Plant Pathol 5:119–160
Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant fungal symbiosis. Science 298:1581
Reicosky DA, Hanover JW (1978) Physiological effects of surface waxes. I. Light reflectance for glaucous and nonglaucous Picea pungens. Plant Physiol 62:101–104
Ribeiro KT, Fernandes GW (2000) Patterns of abundance of a narrow endemic species in a tropical and infertile montane habitat. Plant Ecol 147:205–218
Ribeiro KT, Codeço CT, Fernandes GW (2003) Local and regional spatial distribution of an eruptive and a latent herbivore insect species. Aust Ecol 28:99–107
Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Global Change 9:261–272
Rodriguez RJ, White Jr, JF ArnoldAE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biol Rev 21:67–74
Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343
Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686
Seena S, Sridhar KR (2004) Endophytic fungal diversity of 2 sand dune wild legumes from the southwest coast of India. Can J Microbiol 50:1015–1021
Silva CA, Oliva MA, Vieira MF, Fernandes GW (2008) Trioecy in Coccoloba cereifera Schwacke (Polygonaceae), a narrow endemic and treatened tropical species. Brazilian Arch Biol Technol 5:1003–1010
Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens Environ 81:337–354
Souza AQL, Souza ADL, Astolfi Filho S, Belém PML, Sarquis MIM, Pereira JO (2004) Antimicrobial activity of endophytic fungi isolated from Amazonian toxic plants: Palicourea longiflora aubl. rich and Strychnos cogens bentham. Acta Amazonica 34:185–195
Steinbauer MJ (2000) Specific leaf weight as an indicator of juvenile leaf toughness in Tasmanian bluegum (Eucalyptus globulus ssp. globulus): implications for insect defoliation. Aust For 64:32–37
Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol R 67:491–502
Suryanarayanan TS, Thennarasan S (2004) Temporal variation in endophyte assemblages of Plumeria rubra leaves. Fungal Divers 15:197–204
Tellenbach C, Grunig CR, Sieber TN (2010) Suitability of quantitative real-time PCR to estimate the biomass of fungal root endophytes. Appl Environ Microbiol 76:5764–5772
Wilson D (2000) Ecology of woody plant endophytes. In: Bacon CW, White Jr JF (eds) Microbial endophytes. Marcel Dekker, New York, pp 389–420
Acknowledgments
This paper is dedicated to Hubert Ziegler (founding editor of Trees: Structure and Function) for his contribution to innovative ideas in the science of plant physiology and ecology. We are grateful to Paul Savard, Daniela Esteves, Michel Storquio, Barbara Rosa and Isabela Nascimento for field measurements and assistance in the laboratory; Fernando A. O. Silveira, Daniel Negreiros, Marina B. M. Costa for comments on the manuscript. The research was supported by the National Science and Engineering Research Council of Canadá (NSERC), the Inter-American Institute for Global Change Research (IAI) under its collaborative Research Network Program (Tropi-Dry, CRN2-021) funded by the U.S. National Science Foundation (GEO 0452325), the Fundação de Amparo e Pesquisa de Minas Cerais (APQ-01278-08, EDT 465/07, CRA 122/07, RDP-00048-10); the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 309633/2007-9, 476178/2008-8, 474292/2010-0, 559279/2008-6, 558250/2009-2, 151817/2008-1); and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES 002/2010 DRI/CGCI, BEX 323710-9).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Hampp.
Rights and permissions
About this article
Cite this article
Sanchez-Azofeifa, A., Oki, Y., Wilson Fernandes, G. et al. Relationships between endophyte diversity and leaf optical properties. Trees 26, 291–299 (2012). https://doi.org/10.1007/s00468-011-0591-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-011-0591-5