Colonization of Seeds by Soilborne Fungi: Linking Seed Dormancy-Defense Syndromes, Evolutionary Constraints, and Fungal Traits

  • Simon Maccracken StumpEmail author
  • Carolina Sarmiento
  • Paul-Camilo Zalamea
  • James W. Dalling
  • Adam S. Davis
  • Justin P. Shaffer
  • A. Elizabeth Arnold


The diverse soilborne fungi that recruit to seeds after dispersal include some of the most important agents of seed mortality, as well as strains that enhance germination or inhabit seeds without detriment. Ecological factors that influence seed colonization are not well understood yet are fundamental to the interactions between soilborne fungi and seeds that ultimately influence plant demography and community structure. Here we present current perspectives on seed defense syndromes and related frameworks for predicting colonization success of fungi, with a focus on seeds of tropical pioneer trees. We present a case study that tests whether fungal host range can be predicted by field observations of host use, seed defense syndromes, or phylogenetic relatedness of fungi or hosts. We show that phylogenetic relatedness of hosts, but not fungi, is a strong predictor of fungal colonization of seeds. We posit that the impacts of individual fungi and microbial consortia on seed viability and germination may in turn reflect fungal interactions with the suites of plant defenses codified recently under the broad framework of seed dormancy-defense syndromes. Our findings set the stage for experiments that track colonization, germination, and seedling establishment in the field, important for understanding impacts of fungi on the recruitment of tropical trees.


Barro Colorado Island Clonostachys Effective specialization Fusarium Lasiodiplodia Phylogenetic signal Pioneer trees Trichoderma 



We thank Margaret Wilch, Kayla Garcia, Daniel Roche, Abby Robison, and the support staff on BCI for assistance, guidance, and logistical support during the experiment. We thank Peter Chesson, M. Natalia Umaña, and Meghan Krishnadas for helpful discussion and advice on statistics. This work was funded by NSF DEB-1119758 to AEA and NSF DEB-1120205 to JWD and ASD. PCZ was supported in part by a grant from the Simons Foundation to the Smithsonian Tropical Research Institute (429440, WTW). SMS was supported by NSF DGE-0841234 and the University of Arizona and gratefully acknowledges the Department of Ecology and Evolutionary Biology and the Institute for the Environment for funding support. We thank the Smithsonian Tropical Research Institute and the Republic of Panama for the opportunity to conduct research there.


  1. Agrios GN (2005) Plant pathology, vol 5E. Academic Press, CambridgeGoogle Scholar
  2. Agudelo-Romero P, de la Iglesia F, Elena SF (2008) The pleiotropic cost of host-specialization in tobacco etch potyvirus. Infect Genet Evol 8:806–814. Scholar
  3. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723. Scholar
  4. Arnold AE, Mejía LC, Kyllo D et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654. Scholar
  5. Augspurger CK, Wilkinson HT (2007) Host specificity of pathogenic pythium species: implications for tree species diversity. Biotropica 39:702–708. Scholar
  6. Barrett LG, Kniskern JM, Bodenhausen N (2009) Continua of specificity and virulence in plant host-pathogen interactions: causes and consequences. New Phytol 183:513–529. Scholar
  7. Bashyal B, Aggarwal R, Banerjee S, Gupta S, Sharma S (2014) Pathogenicity, ecology and genetic diversity of the Fusarium spp. associated with an emerging bakanae disease of rice (Oryza sativa L.) in India. In: Kharwar R, Upadhyay R, Dubey N, Raghuwanshi R (eds) Microbial Diversity and Biotechnology in Food Security. Springer, New DelhiGoogle Scholar
  8. Beckstead J, Meyer SE, Reinhart KO et al (2014) Factors affecting host range in a generalist seed pathogen of semi-arid shrublands. Plant Ecol 215:427–440. Scholar
  9. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745. Scholar
  10. Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383. Scholar
  11. Crawley MJ (2007) The R book, vol 1E. Wiley, HobokenCrossRefGoogle Scholar
  12. Dalling JW, Brown TA (2009) Long-term persistence of pioneer species in tropical rain forest soil seed banks. Am Nat 173:531–535. Scholar
  13. Dalling JW, Swaine MD, Garwood NC (1997) Soil seed bank community dynamics in seasonally moist lowland tropical forest, Panama. J Trop Ecol 13:659–680. Scholar
  14. Dalling JW, Swaine MD, Garwood NC (1998) Dispersal patterns and seed bank dynamics of pioneer trees in moist tropical forest. Ecology 79:564–578.[0564:DPASBD]2.0.CO;2CrossRefGoogle Scholar
  15. Dalling JW, Davis AS, Schutte BJ et al (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J Ecol 99:89–95. Scholar
  16. de Vienne DM, Hood ME, Giraud T (2009) Phylogenetic determinants of potential host shifts in fungal pathogens. J Evol Biol 22:2532–2541. Scholar
  17. Desprez-Loustau ML, Robin C, Buee M et al (2007) The fungal dimension of biological invasions. Trends Ecol Evol 22:472–480. Scholar
  18. Ebert D (1998) Evolution - experimental evolution of parasites. Science 282:1432–1435. Scholar
  19. Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. Scholar
  20. Gallery RE, Dalling JW, Arnold AE (2007) Diversity, host affinity, and distribution of seed-infecting fungi: a case study with Cecropia. Ecology 88:582–588. Scholar
  21. Gallery RE, Moore DJP, Dalling JW (2010) Interspecific variation in susceptibility to fungal pathogens in seeds of 10 tree species in the neotropical genus cecropia. J Ecol 98:147–115. Scholar
  22. Gilbert GS (2005) The dimension of plant disease in tropical forests. In: Burlesem DFRP, Pinard MA, Sue E (eds) Biotic interactions in the tropics: their role in the maintenance of species diversity. Cambridge University Press, Cambridge, pp 141–164CrossRefGoogle Scholar
  23. Gilbert GS, Parker IM (2016) The evolutionary ecology of plant disease: a phylogenetic perspective. Annu Rev Ecol Syst 54:549–578. Scholar
  24. Godoy O, Kraft NJ, Levine JM (2014) Phylogenetic relatedness and the determinants of competitive outcomes. Ecol Lett 17:836–844. Scholar
  25. Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic Press, CambridgeGoogle Scholar
  26. Hoffman MT, Arnold AE (2010) Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 76:4063–4075. Scholar
  27. Kirkpatrick B, Bazzaz F (1979) Influence of certain fungi on seed germination and seedling survival of four colonizing annuals. J Appl Ecol 16:515–527. Scholar
  28. Kluger CG, Dalling JW, Gallery RE et al (2008) Host generalists dominate fungal communities associated with seeds of four neotropical pioneer species. J Trop Ecol 24:351–354. Scholar
  29. Little TJ, Watt K, Ebert D (2006) Parasite-host specificity: experimental studies on the basis of parasite adaptation. Evolution 60:31–38. Scholar
  30. Mariadassou M, Robin S, Vacher C (2010) Uncovering latent structure in valued graphs: a variational approach. Ann Appl Stat 4:715–742. Scholar
  31. Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 446:752–755. Scholar
  32. Pagel MD (1992) A method for the analysis of comparative data. J Theor Biol 156:431–442. Scholar
  33. Parker IM, Gilbert GS (2004) The evolutionary ecology of novel plant-pathogen interactions. Annu Rev Ecol Evol Syst 35:675–700. Scholar
  34. Parker GA, Smith JM (1990) Optimality theory in evolutionary biology. Nature 348:27–33. Scholar
  35. Pažoutová S, Olšovská J, Linka M et al (2000) Chemoraces and habitat specialization of Claviceps purpurea populations. Appl Environ Microb 66:5419–5425. Scholar
  36. Peters J (2000) Tetrazolium testing handbook: contribution no. 29 to the handbook on seed testing. Association of Official Seed AnalystsGoogle Scholar
  37. Pizano C, Mangan SA, Herre EA et al (2010) Above- and belowground interactions drive habitat segregation between two cryptic species of tropical trees. Ecology 92:47–56. Scholar
  38. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  39. Sarmiento C, Zalamea PC, Dalling JW et al (2017) Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest. Proc Natl Acad Sci USA 114:11458–11463. Scholar
  40. Shaffer JP, Sarmiento C, Zalamea P-C, Gallery RE, Davis AS, Baltrus DA, Arnold AE (2016) Diversity, specificity, and phylogenetic relationships of endohyphal bacteria in fungi that inhabit tropical seeds and leaves. Front Ecol Evol 4:116. Scholar
  41. Shaffer JP, Zalamea PC, Sarmiento C et al (2018) Context-dependent and variable effects of endohyphal bacteria on interactions between fungi and seeds. Fungal Ecol 36:117CrossRefGoogle Scholar
  42. Schupp EW, Howe HF, Augspurger CK, Levey DJ (1989) Arrival and survival in tropical treefall gaps. Ecology 70:562–564. Scholar
  43. Silvera K, Skillman JB, Dalling JW (2003) Seed germination, seedling growth and habitat partitioning in two morpho-types of the tropical pioneer tree Trema micrantha; in a seasonal forest in Panama. J Trop Ecol 19:27–34. Scholar
  44. Stamatakis A (2006) Raxml-vi-hpc: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. Scholar
  45. Wallis CM, Stone AL, Sherman DJ et al (2007) Adaptation of plum pox virus to a herbaceous host (Pisum sativum) following serial passages. J Gen Virol 88:2839–2845. Scholar
  46. Webb CO, Ackerly DD, McPeek MA et al (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. Scholar
  47. Whipps JM (1987) Effect of media on growth and interactions between a range of soil-borne glasshouse pathogens and antagonistic fungi. New Phytol 107:127–142. Scholar
  48. Zalamea P, Sarmiento C, Arnold AE et al (2015) Do soil microbes and abrasion by soil particles influence persistence and loss of physical dormancy in seeds of tropical pioneers? Front Plant Sci 5:1–15. Scholar
  49. Zalamea PC, Dalling JW, Sarmiento C et al (2018) Dormancy-defense syndromes and tradeoffs between physical and chemical defenses in seeds of pioneer species. Ecology 99:1988–1998. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Simon Maccracken Stump
    • 1
    • 2
    Email author
  • Carolina Sarmiento
    • 3
  • Paul-Camilo Zalamea
    • 3
  • James W. Dalling
    • 3
    • 4
  • Adam S. Davis
    • 5
  • Justin P. Shaffer
    • 6
  • A. Elizabeth Arnold
    • 1
    • 6
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA
  2. 2.School of Forestry and Environmental StudiesYale UniversityNew HavenUSA
  3. 3.Smithsonian Tropical Research InstitutePanamaRepublic of Panama
  4. 4.Department of Plant BiologyUniversity of IllinoisUrbanaUSA
  5. 5.Department of Crop SciencesUniversity of IllinoisUrbanaUSA
  6. 6.School of Plant SciencesUniversity of ArizonaTucsonUSA

Personalised recommendations