Soil-borne fungi influence seed germination and mortality, with implications for coexistence of desert winter annual plants

Autoři: Yue M. Li aff001;  Justin P. Shaffer aff003;  Brenna Hall aff004;  Hongseok Ko aff005
Působiště autorů: School of Natural Resources and the Environment, University of Arizona, Tucson, Arizona, United States of America aff001;  Arizona-Sonora Desert Museum, Tucson, Arizona, United States of America aff002;  School of Plant Sciences, University of Arizona, Tucson, Arizona, United States of America aff003;  College of Public Health, University of Arizona, Tucson, Arizona, United States of America aff004;  Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, United States of America aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224417


Soil-borne fungi influence coexistence of plant species in mesic environments, but much less is known about their effects on demographic processes relevant to coexistence in arid and semi-arid systems. We isolated 43 fungal strains that naturally colonize seeds of an invasive winter annual (Brassica tournefortii) in the Sonoran Desert, and evaluated the impact of 18 of them on seed germination and mortality of B. tournefortii and a co-occurring native annual (Plantago ovata) under simulated summer and winter temperatures. Fungi isolated from B. tournefortii seeds impacted germination and mortality of seeds of both plant species in vitro. Seed responses reflected host-specific effects by fungi, the degree of which differed significantly between the strains, and depended on the temperature. In the winter temperature, ten fungal strains increased or reduced seed germination, but substantial seed mortality due to fungi was not observed. Two strains increased germination of P. ovata more strongly than B. tournefortii. In the summer temperature, fungi induced both substantial seed germination and mortality, with ten strains demonstrating host-specificity. Under natural conditions, host-specific effects of fungi on seed germination may further differentiate plant species niche in germination response, with a potential of promoting coexistence. Both host-specific and non-host-specific effects of fungi on seed loss may induce polarizing effects on plant coexistence depending on the ecological context. The coexistence theory provides a clear framework to interpret these polarizing effects. Moreover, fungi pathogenic to both plant species could induce host-specific germination, which challenges the theoretical assumption of density-independent germination response. These implications from an in vitro study underscore the need to weave theoretical modeling, reductive empirical experiments, and natural observations to illuminate effects of soil-borne fungi on coexistence of annual plant species in variable desert environments.

Klíčová slova:

Deserts – Fungal pathogens – Fungi – Invasive species – Plant fungal pathogens – Plants – Seed germination – Seeds


1. Chesson P. Updates on mechanisms of maintenance of species diversity. J Ecol. 2018;106: 1773–1794. doi: 10.1111/1365-2745.13035

2. Bever JD. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol. 2003;157: 465–473. doi: 10.1046/j.1469-8137.2003.00714.x

3. Mordecai EA. Pathogen impacts on plant communities: unifying theory, concepts, and empirical work. Ecol Monogr. 2011;81: 429–441. doi: 10.1890/10-2241.1

4. Levin SA. Community equilibria and stability, and an extension of the competitive exclusion principle. Am Nat. 1970;104: 413–423. doi: 10.2307/2459310

5. Tilman D. Resource Competition and Community Structure. Princeton, New Jersey: Princeton University Press; 1982.

6. Allen JA. Frequency-dependent selection by predators. Phil Trans R Soc Lond B. 1988;319: 485–503. doi: 10.1098/rstb.1988.0061 2905488

7. Kuang JJ, Chesson P. Interacting coexistence mechanisms in annual plant communities: Frequency-dependent predation and the storage effect. Theor Popul Biol. 2010;77: 56–70. doi: 10.1016/j.tpb.2009.11.002 19945475

8. Chesson P. Quantifying and testing species coexistence mechanisms. In: Valladares F, Camacho A, Elosegui A, Estrada M, Gracia C, Senar JC, et al., editors. Unity in Diversity: Reflection on Ecology after the Legacy of Ramon Magalef. Bilbao: Fundacion BBVA; 2008. pp. 119–164.

9. Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis CE, et al. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature. 2014;506: 85–88. doi: 10.1038/nature12911 24463522

10. Beckstead J, Meyer SE, Connolly BM, Huck MB, Street LE. Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. J Ecol. 2010;98: 168–177. doi: 10.1111/j.1365-2745.2009.01599.x

11. Bonanomi G, Mingo A, Incerti G, Mazzoleni S, Allegrezza M. Fairy rings caused by a killer fungus foster plant diversity in species-rich grassland. J Veg Sci. 2012;23: 236–248. doi: 10.1111/j.1654-1103.2011.01353.x

12. Bradley DJ, Gilbert GS, Martiny JBH. Pathogens promote plant diversity through a compensatory response. Ecol Lett. 2008;11: 461–469. doi: 10.1111/j.1461-0248.2008.01162.x 18312409

13. Hersh MH, Vilgalys R, Clark JS. Evaluating the impacts of multiple generalist fungal pathogens on temperate tree seedling survival. Ecology. 2012;93: 511–520. doi: 10.1890/11-0598.1 22624206

14. Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman JMT, van der Putten WH. Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr. 2007;77: 147–162. doi: 10.1890/06-0502

15. Klironomos JN. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature. 2002;417: 67. doi: 10.1038/417067a 11986666

16. Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, et al. Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature. 2010;466: 752. doi: 10.1038/nature09273 20581819

17. Sarmiento C, Zalamea P-C, Dalling JW, Davis AS, Stump SM, U’Ren JM, et al. Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest. Proc Natl Acad Sci. 2017; 201706324. doi: 10.1073/pnas.1706324114 28973927

18. Van der Putten WH, Dijk CV, Peters B a. M. Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature. 1993;362: 53. doi: 10.1038/362053a0

19. Mordecai EA. Consequences of pathogen spillover for cheatgrass-invaded grasslands: coexistence, competitive Exclusion, or priority effects. Am Nat. 2013;181: 737–747. doi: 10.1086/670190 23669537

20. Chesson P, Kuang JJ. The interaction between predation and competition. Nature. 2008;456: 235–238. doi: 10.1038/nature07248 19005554

21. Mordecai EA. Pathogen impacts on plant diversity in variable environments. Oikos. 2015;124: 414–420. doi: 10.1111/oik.01328

22. Keane RM, Crawley MJ. Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol. 2002;17: 164–170.

23. Andonian K, Hierro JL, Khetsuriani L, Becerra PI, Janoyan G, Villareal D, et al. Geographic mosaics of plant–soil microbe interactions in a global plant invasion. J Biogeogr. 2012;39: 600–608. doi: 10.1111/j.1365-2699.2011.02629.x

24. Parker IM, Saunders M, Bontrager M, Weitz AP, Hendricks R, Magarey R, et al. Phylogenetic structure and host abundance drive disease pressure in communities. Nature. 2015;520: 542–544. doi: 10.1038/nature14372 25903634

25. Meyer SE, Merrill KT, Allen PS, Beckstead J, Norte AS. Indirect effects of an invasive annual grass on seed fates of two native perennial grass species. Oecologia. 2014;174: 1401–1413. doi: 10.1007/s00442-013-2868-4 24399482

26. Smith SD, Monson RK, Anderson JE. Desert Annuals. In: Smith SD, Monson RK, Anderson JE, editors. Physiological Ecology of North American Desert Plants. Berlin, Heidelberg: Springer Berlin Heidelberg; 1997. pp. 179–189. doi: 10.1007/978-3-642-59212-6_9

27. Venable DL, Pake CE, Caprio AC. Diversity and coexistence of Sonoran Desert winter annuals. Plant Species Biol. 1993;8: 207–216. doi: 10.1111/j.1442-1984.1993.tb00071.x

28. Angert AL, Huxman TE, Chesson P, Venable DL. Functional tradeoffs determine species coexistence via the storage effect. Proc Natl Acad Sci U S A. 2009;106: 11641–11645. doi: 10.1073/pnas.0904512106 19571002

29. Allington GRH, Koons DN, Morgan Ernest SK, Schutzenhofer MR, Valone TJ. Niche opportunities and invasion dynamics in a desert annual community. Ecol Lett. 2012; 158–166. doi: 10.1111/ele.12023 23126368

30. Chesson P, Huntly NJ, Roxburgh SH, Pantastico-Caldas M, Facelli JM. The storage effect: definition and tests in two plant communities. Temporal Dynamics and Ecological Process. Cambridge, United Kindom: Cambridge University Press; 2013. Available:

31. Adondakis S, Venable DL. Dormancy and germination in a guild of Sonoran Desert annuals. Ecology. 2004;85: 2582–2590. doi: 10.1890/03-0587

32. Baskin CC, Baskin JM. Chapter 4—Germination Ecology of Seeds with Nondeep Physiological Dormancy. Seeds. San Diego: Academic Press; 1998. pp. 49–85. Available:

33. Li YM, Chesson P. Seed demographic comparisons reveal spatial and temporal niche differentiation between native and invasive species in a community of desert winter annual plants. Evol Ecol Res. 2018;19: 71–84.

34. Huang Z, Liu S, Bradford KJ, Huxman TE, Venable DL. The contribution of germination functional traits to population dynamics of a desert plant community. Ecology. 2016;97: 250–261. doi: 10.1890/15-0744.1 27008793

35. Barrows CW, Allen EB, Brooks ML, Allen MF. Effects of an invasive plant on a desert sand dune landscape. Biol Invasions. 2009;11: 673–686. doi: 10.1007/s10530-008-9282-6

36. Huxman TE, Kimball S, Angert AL, Gremer JR, Barron-Gafford GA, Venable DL. Understanding past, contemporary, and future dynamics of plants, populations, and communities using Sonoran Desert winter annuals. Am J Bot. 2013;100: 1369–1380. doi: 10.3732/ajb.1200463 23838034

37. Kimball S, Angert AL, Huxman TE, Venable DL. Differences in the timing of germination and reproduction relate to growth physiology and population dynamics of Sonoran Desert winter annuals. Am J Bot. 2011;98: 1773–1781. doi: 10.3732/ajb.1100034 22003177

38. Salo LF, McPherson GR, Williams DG. Sonoran desert winter annuals affected by density of red brome and soil nitrogen. Am Midl Nat. 2005;153: 95–109. doi: 10.1674/0003-0031(2005)153[0095:SDWAAB]2.0.CO;2

39. Van Devender TR, Felger RS, Búrquez A. Exotic plants in the Sonoran Desert region, Arizona and Sonora. Proceedings of the California Exotic Pest Plant Council Symposium. California Exotic Pest Plant Council Berkeley, CA; 1997. pp. 1–6.

40. Li YM, Dlugosch KM, Enquist BJ. Novel spatial analysis methods reveal scale-dependent spread and infer limiting factors of invasion by Sahara mustard. Ecography. 2015;38: 311–320. doi: 10.1111/ecog.00722

41. Kirkpatrick BL, Bazzaz FA. Influence of certain fungi on seed germination and seedling survival of four colonizing annuals. J Appl Ecol. 1979;16: 515–527. doi: 10.2307/2402526

42. Crist TO, Friese CF. The impact of fungi on soil seeds: implications for plants and granivores in a semiarid shrub-steppe. Ecology. 1993;74: 2231–2239. doi: 10.2307/1939576

43. MacDougall AS, Gilbert B, Levine JM. Plant invasions and the niche. J Ecol. 2009;97: 609–615. doi: 10.1111/j.1365-2745.2009.01514.x

44. Shea K, Chesson P. Community ecology theory as a framework for biological invasions. Trends Ecol Evol. 2002;17: 170–176.

45. Thomas KA, Guertin P. Southwest Exotic Mapping Program (SWEMP); 2007 [cited 2018 May 04] Database: U.S. Geological Survey [Internet]. Available:

46. Pake CE, Venable DL. Seed banks in desert annuals: implications for persistence and coexistence in variable environments. Ecology. 1996;77: 1427–1435. doi: 10.2307/2265540

47. Shaffer JP, Zalamea P-C, Sarmiento C, Gallery RE, Dalling JW, Davis AS, et al. Context-dependent and variable effects of endohyphal bacteria on interactions between fungi and seeds. Fungal Ecol. 2018;36: 117–127. doi: 10.1016/j.funeco.2018.08.008

48. Gallery RE, Dalling JW, Arnold AE. Diversity, host affinity, and distribution of seed-infecting fungi: a case study with Cecropia. Ecology. 2007;88: 582–588. doi: 10.1890/05-1207 17503585

49. Shaffer JP, Sarmiento C, Zalamea P-C, Gallery RE, Davis AS, Baltrus DA, et al. Diversity, specificity, and phylogenetic relationships of endohyphal bacteria in fungi that inhabit tropical seeds and leaves. Front Ecol Evol. 2016;4. doi: 10.3389/fevo.2016.00115

50. Carbone I, White JB, Miadlikowska J, Arnold AE, Miller MA, Kauff F, et al. T-BAS: Tree-Based Alignment Selector toolkit for phylogenetic-based placement, alignment downloads and metadata visualization: an example with the Pezizomycotina tree of life. Bioinformatics. 2017;33: 1160–1168. doi: 10.1093/bioinformatics/btw808 28003260

51. U’Ren JM, Dalling JW, Gallery RE, Maddison DR, Davis EC, Gibson CM, et al. Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analysing fungal environmental samples. Mycol Res. 2009;113: 432–449. doi: 10.1016/j.mycres.2008.11.015 19103288

52. U’Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE. Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot. 2012;99: 898–914. doi: 10.3732/ajb.1100459 22539507

53. Bangle DN, Walker LR, Powell EA. Seed germination of the invasive plant Brassica tournefortii (Sahara mustard) in the Mojave Desert. West North Am Nat. 2008;68: 334–342.

54. Das M. Effect of storage duration and temperature on seed germination of Plantago ovata L., P. indica L. and Lepidium sativum L (Asalio). Med Plants-Int J Phytomedicines Relat Ind. 2016;8: 85–92. doi: 10.5958/0975-6892.2016.00011.3

55. Hurlbert SH, Lombardi CM. Final collapse of the Neyman-Pearson decision theoretic framework and rise of the neoFisherian. Ann Zool Fenn. 2009;46: 311–349. doi: 10.5735/086.046.0501

56. McShane BB, Gal D, Gelman A, Robert C, Tackett JL. Abandon statistical significance. Am Stat. 2019;73: 235–245. doi: 10.1080/00031305.2018.1527253

57. Stephens PA, Buskirk SW, del Rio CM. Inference in ecology and evolution. Trends Ecol Evol. 2007;22: 192–197. doi: 10.1016/j.tree.2006.12.003 17174005

58. Hall P. The Bootstrap and Edgeworth Expansion. New York: Springer Science & Business Media; 1992.

59. Efron B, Tibshirani R. An Introduction to the Bootstrap. New York: Chapman and Hall; 1993.

60. Cox DR. A remark on multiple comparison methods. Technometrics. 1965;7: 223–224. doi: 10.1080/00401706.1965.10490250

61. Stewart-Oaten A. Rules and judgments in statistics: three examples. Ecology. 1995;76: 2001–2009. doi: 10.2307/1940736

62. Hurlbert SH, Lombardi CM. Lopsided reasoning on lopsided tests and multiple comparisons. Aust N Z J Stat. 2012;54: 23–42. doi: 10.1111/j.1467-842X.2012.00652.x

63. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2018. Available:

64. Canty A, Ripley BD. boot: Bootstrap R (S-Plus) Functions. 2017.

65. Warton DI, Hui FKC. The arcsine is asinine: the analysis of proportions in ecology. Ecology. 2011;92: 3–10. doi: 10.1890/10-0340.1 21560670

66. McCarthy-Neumann S, Ibáñez I. Plant–soil feedback links negative distance dependence and light gradient partitioning during seedling establishment. Ecology. 2013;94: 780–786. doi: 10.1890/12-1338.1

67. Li L, Chesson P. The effects of dynamical rates on species coexistence in a variable environment: the paradox of the plankton revisited. Am Nat. 2016;188: E46–E58. doi: 10.1086/687111 27420794

68. Gilbert GS. Evolutionary ecology of plant diseases in natural ecosystems. Annu Rev Phytopathol. 2002;40: 13–43. doi: 10.1146/annurev.phyto.40.021202.110417 12147753

69. Kuang JJ, Chesson P. Coexistence of annual plants: Generalist seed predation weakens the storage effect. Ecology. 2009;90: 170–182. doi: 10.1890/08-0207.1 19294923

70. Agrios GN. Chapter Two—Parasitism and Disease Development. In: Agrios GN, editor. Plant Pathology (Fifth Edition). Fifth Edition. San Diego: Academic Press; 2005. pp. 77–104. doi: 10.1016/B978-0-08-047378-9.50008–7

71. Horst JL, Venable DL. Frequency-dependent seed predation by rodents on Sonoran Desert winter annual plants. Ecology. 2018;99: 196–203. doi: 10.1002/ecy.2066 29083479

72. Platt JR. Strong inference: certain systematic methods of scientific thinking may produce much more rapid progress than others. Science. 1964;146: 347–353. doi: 10.1126/science.146.3642.347 17739513

73. Sagarin R, Pauchard A. Observational approaches in ecology open new ground in a changing world. Front Ecol Environ. 2010;8: 379–386. doi: 10.1890/090001

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