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Thermotolerance generated by plant/fungal symbiosis
ble S2) than those of nonsymbiotic plants in
soils Յ40°C. In soils above 40°C, nonsymbi-
otic plants did not survive while symbioticplants thrived. The beneficial effect of fungal
symbiosis increased with soil temperatures,demonstrating that Curvularia
sp. providedthermal protection for D. lanuginosum
. We rei-
Regina S. Redman,1,2 Kathy B. Sheehan,3,5 Richard G. Stout,4,5
sp. from D. lanuginosum
Russell J. Rodriguez,1,2* Joan M. Henson3,5
roots at 45°C field soil temperatures, indicat-ing that thermal protection was also providedto the fungus, which corroborated our labo-
All plants studied in natural ecosystems are
or inoculated with Curvularia
sp. by pipet-
symbiotic with fungi (1
), which obtain nu-
ting 105 spores between the crown and first
In addition to thermotolerance, the basis of
trients while either positively, negatively,
leaf. In the absence of thermal stress, en-
mutualism in this system may involve other
or neutrally affecting host fitness (2
benefits (e.g., nutrient acquisition by the fun-
adaptation to selective pressures is consid-
gus). Several possible symbiotic mechanisms
could confer thermotolerance. In planta, the
). To test whether mutualistic fungi con-
fungal endophyte produces cell wall melanin
tribute to plant adaptation, we collected
with thermal tape (Fig. S1), nonsymbiotic
(Fig. S3) that may dissipate heat along the
200 Dichanthelium lanuginosum
plants (45/45) became shriveled and chlo-
hyphae and/or complex with oxygen radicals
from geothermal soils at 10 sites in Lassen
rotic at 50°C (Fig. 1A). In contrast, symbi-
generated during heat stress (9
otic plants (45/45) tolerated constant 50°C
the endophyte may act as a “biological trigger”
soil temperature for 3 days and intermittent
allowing symbiotic plants to activate stress-
soil temperatures as high as 65°C for 10
response systems more rapidly and strongly
days. All nonsymbiotic plants (45/45) died
than nonsymbiotic plants (10
Plants and their roots were removed and as-
during the 65°C heat regime, whereas sym-
sessed for fungal colonization (5
). A fungal
biotic plants (45/45) survived. The endo-
References and Notes
1. O. Petrini, in Microbiology of the Phyllosphere
, N. J.
Fokkema, J. van den Heuvel, Eds. (Cambridge Univ.
Press, Cambridge, 1986), pp. 175–187.
2. D. H. Lewis, in The Biology of Mutualism
, D. H.
Boucher, Ed. (Croom Helm, London, 1985), pp. 29–
3. M. F. Smallwood, C. M. Calvert, D. J. Bowles, Eds.,
Plant Responses to Environmental Stress
4. R. S. Redman, A. Litvintseva, K. B. Sheehan, J. M.
Henson, R. J. Rodriguez, Appl. Environ. Microbiol. 65
5. Materials and Methods are available as supporting
6. A. Sivanesan, Mycol. Pap. 158
, 104 (1987).
7. T. J. White, T. Bruns, S. Lee, J. Taylor, in PCR
Protocols: A Guide to Methods and Applications
M. A. Innis, D. H. Gelfand, J. J. Sninsky, T. J. White,
Eds. (Academic Press, San Diego, CA, 1990), pp.
8. R. S. Redman, D. D. Dunigan, R. J. Rodriguez, New
, 705 (2001).
9. J. F. Davidson, B. Whyte, P. H. Bissinger, R. H. Schiestl,
Proc. Natl. Acad. Sci. U.S.A. 93
10. R. S. Redman et al.
, Plant Physiol. 119
, 795 (1999).
11. We thank T. Al-Niemi, L. Brasche, M. Bateson, E.
Kuhn, A. Litvintseva, and J. Duda for technical and
ﬁeld assistance. This project was made possible by
the permission, assistance, and guidelines of YNP and
LVNP. This work was supported by grants from the
U.S. Geological Survey, the NSF (9977922), the U.S.
Army Research Ofﬁce (DAAHO4-96-1-01194), and
Representative symbiotic (with Curvularia
sp.) and nonsymbiotic
plants with rhizosphere temperatures of 50°C for 3 days
Supporting Online Material
or 65°C for 8 hours/day for 10 days under laboratory conditions (A
in 40° or 45°C soil under ﬁeld conditions (B
void of the fungus, we conclude that this Curvu-
phyte was reisolated from surface sterilized
sp., like all known Curvularia
roots and leaves of all surviving plants,
indicating that both the fungus and the host
1U.S. Geological Survey, WFRC, 6505 NE 65th Street,
the thermotolerance of D. lanuginosum
Seattle, WA 98115, USA. 2Department of Botany,
University of Washington, Seattle, WA 98195, USA.
removed seed coats and surface sterilized
symbiotic seedlings in pasteurized geother-
3Department of Microbiology, 4Department of Plant
) to generate endophyte-free plants.
mal soil collected and returned to Amphi-
Sciences, and 5Thermal Biology Institute, Montana
Treated seeds were planted in sterile ma-
theater Springs ( YNP) in May 2001 (Fig.
State University, Bozeman, MT 59717, USA.
To whom correspondence should be addressed. E-
month, plants were either mock-inoculated
greener with greater root and leaf masses (Ta-
www.sciencemag.org SCIENCE VOL 298 22 NOVEMBER 2002
The Influence of the Environment and Other Exogenous Agents on Spontaneous Abortion Risk R. Samuel McLaughlin Centre for Population Health Risk Assessment Abstract It has been estimated that close to 30% of all pregnancies end in spontaneous abortion. Although about 60% of spontaneous abortions are thought to be due to genetic, infectious, hormonal and immunological factors, the rol
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