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Niche specialization in Bromus tectorum seed bank pathogens

Published online by Cambridge University Press:  13 June 2018

Susan E. Meyer ,
Julie Beckstead  and
Phil S. Allen
Susan E. Meyer*
Affiliation:
USFS Rocky Mountain Research Station Shrub Sciences Laboratory, Provo, Utah, USA
Julie Beckstead
Affiliation:
Department of Biology, Gonzaga University, Spokane, Washington, USA
Phil S. Allen
Affiliation:
Department of Plant and Wildlife Science, Brigham Young University, Provo, Utah, USA
*
Author for correspondence: Susan E. Meyer, E-mail: smeyer@fs.fed.us
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Abstract

Niche theory predicts that when two species exhibit major niche overlap, one will eventually be eliminated through competitive exclusion. Thus, some degree of niche specialization is required to facilitate coexistence. We examined whether two important seed bank pathogens on the invasive winter annual grass Bromus tectorum (cheatgrass, downy brome) exhibit niche specialization. These pathogens utilize seed resources in complementary ways. Pyrenophora semeniperda is specialized to attack dormant seeds. It penetrates directly through the seed coverings. Hyphae ramify first through the endosperm and then throughout the seed. Seed death results as the embryo is consumed. In contrast, the Fusarium seed rot pathogen (Fusarium sp.) is specialized to attack non-dormant seeds in the early stages of germination. It cannot penetrate seed coverings directly. Instead, it responds to a cue emanating from the radicle end with directional hyphal growth and subsequent penetration at the point of radicle emergence, causing seed death. Non-dormant seeds usually escape P. semeniperda through germination even if infected because it develops more slowly than Fusarium. When water stress slows non-dormant seed germination, both P. semeniperda and Fusarium can attack and cause seed mortality more effectively. The Fusarium seed rot pathogen can sometimes reach epidemic levels and may result in B. tectorum stand failure (‘die-off’). Stands usually re-establish from the persistent seed bank, but if P. semeniperda has also reached high levels and eliminated the seed bank, a die-off can persist indefinitely.

Keywords

cheatgrassdie-offFusarium seed rot pathogenPyrenophora semeniperdaseed dormancystand failurewater stress
Type
Review Paper
Information
Seed Science Research , Volume 28 , Special Issue 3: Seeds as Systems , September 2018 , pp. 215 - 221
Copyright
Copyright © Cambridge University Press 2018 

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References

Allen, PS, Finch-Boekweg, H and Meyer, S.E. (in press) A proposed mechanism for high pathogen-caused mortality in the seed bank of an invasive annual grass. Fungal Ecology.Google Scholar
Bair, NB, Meyer, SE and Allen, PS (2006) A hydrothermal after-ripening time model for seed dormancy loss in Bromus tectorum L. Seed Science Research 19, 17–28.Google Scholar
Barth, C et al. (2015) A hydrothermal time model for conidial germination and mycelial growth of the desert seed pathogen Pyrenophora semeniperda. Fungal Biology 119, 720–730.Google Scholar
Baughman, OW and Meyer, SE (2013) Is Pyrenophora semeniperda the cause of downy brome (Bromus tectorum) die-offs? Invasive Plant Science and Management 6, 105–111.Google Scholar
Bauer, M, Meyer, SE and Allen, PS (1998) A simulation model to predict seed dormancy loss in the field for Bromus tectorum L. Journal of Experimental Botany 49, 1235–1244.Google Scholar
Beckstead, J et al. (2016) Lack of host specialization on winter annual grasses in the seed pathogen Pyrenophora semeniperda. PLoS ONE 11, e0151058. doi:10.1371/journal.pone.0151058Google Scholar
Beckstead, J et al. (2007) A race for survival: can Bromus tectorum seeds escape Pyrenophora semeniperda-caused mortality by germinating quickly? Annals of Botany 99, 907–914.Google Scholar
Beckstead, J, Meyer, SE et al. (2014) Factors affecting host range in a generalist seed pathogen of semi-arid shrublands. Plant Ecology 215, 427–440.Google Scholar
Bever, JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75, 1965–1977.Google Scholar
Blaney, CS and Kotanen, PM (2001) Effects of fungal pathogens on seeds of native and exotic plants: a test using congeneric pairs. Journal of Applied Ecology 38, 1104–1113.Google Scholar
Chambers, JC et al. (2014) Resilience to stress and disturbance, and resistance to Bromus tectorum L. invasion in cold desert shrublands of western North America. Ecosystems 17, 360–375.Google Scholar
Chambers, JC and MacMahon, JA (1994) A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25, 263–292.Google Scholar
Christensen, M, Meyer, SE and Allen, PS (1996) A hydrothermal time model of seed after-ripening in Bromus tectorum L. Seed Science Research 6, 155–164.Google Scholar
Evidente, A et al. (2002) Cytochalasins Z1, Z2 and Z3, three 24-oxa [14] cytochalasans produced by Pyrenophora semeniperda. Phytochemistry 60, 45–53.Google Scholar
Finch, H, Allen, PS and Meyer, SE (2013) Environmental factors influencing Pyrenophora semeniperda-caused seed mortality in Bromus tectorum. Seed Science Research 23, 57–66.Google Scholar
Finch-Boekweg, H et al. (2016) Postdispersal infection and disease development of Pyrenophora semeniperda in Bromus tectorum seeds. Phytopathology 106, 236–243.Google Scholar
Fitt, BD et al. (2006) Coexistence of related pathogen species on arable crops in space and time. Annual Review of Phytopathology 44, 163–182.Google Scholar
Franke, JL, Geary, B and Meyer, SE (2014) Identification of the infection route of a Fusarium seed pathogen into non-dormant Bromus tectorum seeds. Phytopathology 104, 1306–1313.Google Scholar
Gilbert, GS (2002) Evolutionary ecology of plant diseases in natural ecosystems. Annual Review of Phytopathology 40, 13–43.Google Scholar
Hawkins, KK (2013) Secondary dormancy and summer conditions influence outcomes in the Pyrenophora semeniperda-Bromus tectorum pathosystem. MSc thesis, Brigham Young University. http://scholarsarchive.byu.edu/cgi/viewcontent.cgi?article=5206andcontext=etdGoogle Scholar
Hawkins, KK, Allen, PS and Meyer, SE (2017) Secondary dormancy induction and release in Bromus tectorum seeds: the role of temperature, water potential, and hydrothermal time. Seed Science Research 27, 12–25.Google Scholar
Klironomos, JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 67–70.Google Scholar
Masi, M, Evidente, A et al. (2014) Effect of strain and cultural conditions on the production of cytochalasin B by the potential mycoherbicide Pyrenophora semeniperda (Pleosporaceae, Pleosporales). Biocontrol Science and Technology 24, 53–64.Google Scholar
MacLean-Fletcher, S and Pollard, TD (1980) Mechanism of action of cytochalasin B on actin. Cell 20, 329–341.Google Scholar
Meyer, SE (2010) Ecological genetics of floret mass variation in Bromus tectorum, pp. 116–117 in Pendleton, RL, Meyer, SE and Schultz, BS (eds), Conference Proceedings: Seed Ecology III – The Third International Society for Seed Science Meeting on Seeds and the Environment – ‘Seeds and Change’; 20–24 June 2010; Salt Lake City, Utah, USA. Albuquerque, NM, US Department of Agriculture, Forest Service, Rocky Mountain Research Station. https://www.fs.usda.gov/treesearch/pubs/36962Google Scholar
Meyer, SE and Allen, PS (2009) Predicting seed dormancy loss and germination timing for Bromus tectorum in a semi-arid environment using hydrothermal time models. Seed Science Research 19, 225–39.Google Scholar
Meyer, SE, Beckstead, J and Pearce, JL (2016) Community ecology of fungal pathogens on Bromus tectorum, pp. 193–223 in Chambers, J, Germino, M and Brown, C (eds), Exotic Annual Bromus Grasses in Semiarid Ecosystems of the Western US: Assessing Causes, Consequences, and Management Alternatives. New York: Springer.Google Scholar
Meyer, SE et al. (2014a) Does Fusarium-caused seed mortality contribute to Bromus tectorum stand failure in the Great Basin? Weed Research 54, 511–519.Google Scholar
Meyer, SE et al. (2015) Mycelial growth rate and toxin production in the seed pathogen Pyrenophora semeniperda: resource trade-offs and temporally varying selection. Plant Pathology 64, 1450–1460.Google Scholar
Meyer, SE et al. (2014b) Indirect effects of a seed bank pathogen on the interactions between Bromus tectorum and two native perennial grasses. Oecologia 174, 1401–1413.Google Scholar
Meyer, SE et al. (2007) Impact of the pathogen Pyrenophora semeniperda on Bromus tectorum seedbank dynamics in North American cold deserts. Weed Research 47, 54–62.Google Scholar
Meyer, SE, Stewart, TE and Clement, S (2010) The quick and the deadly: growth versus virulence in a seed bank pathogen. New Phytologist 187, 209–216.Google Scholar
Nicholson, JA (2014) Cheatgrass die-off phenomena: what are the short and long term recovery factors of Bromus tectorum stand failure? MS thesis, Brigham Young University, Provo, Utah.Google Scholar
Nelson, EB (1991) Exudate molecules initiating fungal responses to seeds and roots, pp. 197–209 in Keister, DL and Cregan, PB (eds), The Rhizosphere and Plant Growth. Beltsville Symposia in Agricultural Research vol. 14. Dordrecht, the Netherlands: Springer.Google Scholar
O'Donnell, K et al. (2013) Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genetics and Biology 52, 20–31.Google Scholar
Orrock, JL and Damschen, EI (2005) Fungi-mediated mortality of seeds of two old-field plant species. The Journal of the Torrey Botanical Society 132, 613–617.Google Scholar
Polechová, J and Storch, D (2008) Ecological niche, pp. 1088–1097 in Lek, S et al. (eds), Encyclopedia of Ecology, first edition, vol. 2. Amsterdam: Elsevier.Google Scholar
Smith, DC, Meyer, SE and Anderson, VJ (2008) Factors affecting Bromus tectorum seed bank carryover in western Utah. Rangeland Ecology and Management 61, 430–436.Google Scholar
Stewart, TE, Allen, PS and Meyer, SE 2009. First report of Pyrenophora semeniperda in Turkey and Greece. Plant Disease 93, 1351.Google Scholar
Taylor, DL et al. (2014) A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning. Ecological Monographs 84, 3–20.Google Scholar
Weisberg, PJ et al. (2017) Development of remote sensing indicators for mapping episodic die-off of an invasive annual grass (Bromus tectorum) in the Great Basin, USA. Ecological Indicators 79, 173–181.Google Scholar
Yonow, T, Kriticos, DJ and Medd, RW (2004) The potential geographic range of Pyrenophora semeniperda. Phytopathology 94, 805–812.Google Scholar
Zhang, G and Berbee, ML (2001) Pyrenophora phylogenetics inferred from ITS and glyceradehyde-3-phosphate dehydrogenase gene sequences. Mycologia 93, 1048–1063.Google Scholar