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, 14 (10), e0224417
eCollection

Soil-borne Fungi Influence Seed Germination and Mortality, With Implications for Coexistence of Desert Winter Annual Plants

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Soil-borne Fungi Influence Seed Germination and Mortality, With Implications for Coexistence of Desert Winter Annual Plants

Yue M Li et al. PLoS One.

Abstract

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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1
(Panel A) Effects on the fractions of seed germination differed strongly between the fungal strains and between the summer (black markers) and the winter (grey markers) temperature regimes. (Panel B) Host-specific effects on seed germination were observed in both temperature regimes. Fractions of germination of uninoculated seeds (controls) are shown as inserts on the right. In Panel A, effect sizes of germination were estimated as average changes in the fractions of germination between seeds inoculated by a fungal strain vs. controls. Asterisks indicate effects that were significant according to t-tests (α = 0.05; p-values of t-tests in S2 Table). In Panel B, effect sizes of host-specificity were estimated as the differences between the two plant species in their effect sizes of seed germination in response to the same fungal strain. In both panels, bars indicate 95% confidence intervals of effect sizes obtained by nonparametric bootstrapping. Taxonomic assignments of fungal strains to genus levels were provided by T-BAS [50].
Fig 2
Fig 2
(Panel A) Effects on the fractions of seed mortality differed strongly between the fungal strains and were more pronounced in the summer (black markers) than in the winter (grey markers) temperature regime. (Panel B) Host-specific effects on seed mortality were observed only in the summer temperature regime, and largely toward B. tournefortii. Fractions of mortality of uninoculated seeds (controls) are shown as inserts on the right. In Panel A, effect sizes of seed mortality were estimated as average changes in the fractions of mortality between seeds inoculated by a fungal strain vs. controls. Asterisks indicate effects that were significant according to t-tests (α = 0.05; p-values of t-tests in S2 Table). In Panel B, effect sizes of host-specificity were estimated as the differences between the two plant species in their effect sizes of seed mortality in response to the same fungal strain. In both panels, bars indicate 95% confidence intervals of effect sizes obtained by nonparametric bootstrapping. Taxonomic assignments of fungal strains to genus levels were provided by T-BAS [50].
Fig 3
Fig 3
Some fungi caused losses of the in vitro seed banks (Panel A), and some of these effects were host-specific (Panel B). In Panel A, effect sizes of seed loss were estimated as average changes in the combined fractions of seed mortality and germination in the summer temperature regime between seeds inoculated by a fungal strain vs. controls. Asterisks indicate effects that were significant according to t-tests (α = 0.05; p-values of t-tests in S2 Table). In Panel B, effect sizes of host-specificity were estimated as the differences between the two plant species in their effect sizes of seed loss in response to the same fungal strain. In both panels, bars indicate 95% confidence intervals obtained via nonparametric bootstrapping. Taxonomic assignments of fungal strains to genus levels were provided by T-BAS [50].

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Grant support

Funding comes from National Science Foundation https://www.nsf.gov/ (grant number DEB-1353715), U.S. Marine Corps http://www.marines.mil/ (grant number W9126G-14-2-0045), and U.S. Navy https://www.navy.mil (grant number N62473-18-2-0015). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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