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(American Journal of Botany. 1999;86:634-639.)
© 1999 Botanical Society of America, Inc.

Evolutionary significance of isopreneemission from mosses1

David T. Hanson 2, 4, Sarah Swanson 3 , Linda E. Graham 2 and Thomas D. Sharkey 2

2 University of Wisconsin-Madison, Department of Botany, 132 Birge Hall, 430 Lincoln Drive, Madison, Wisconsin 53706-1381, and 3 University of California-Berkeley, Department of Plant Biology, 111 Koshland Hall, Berkeley, California 94720-3102

Received for publication May 12, 1998. Accepted for publication October 15, 1998.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Isoprene emission has been documented and characterized from species in all major groups of vascular plants. We report in our survey that isoprene emission is much more common in mosses and ferns than later divergent land plants but is absent in liverworts and hornworts. The light and temperature responses of isoprene emission from Sphagnum capillifolium (Ehrh.) Hedw. are similar to those of other land plants. Isoprene increases thermotolerance of S. capillifolium to the same extent seen in higher plants as measured by chlorophyll fluorescence. Sphagnum species in a northern Wisconsin bog experienced large temperature fluctuations similar to those reported in tree canopies. Since isoprene has been shown to help plants cope with large, rapid temperature fluctuations, we hypothesize the thermal and correlated dessication stress experienced by early land plants provided the selective pressure for the evolution of light-dependent isoprene emission in the ancestors of modern mosses. As plants radiated into different habitats, this capacity was lost multiple times in favor of other thermal protective mechanisms.

Key Words: bryophyte • evolution • heat stress • isoprene • micrometeorology • pteridophyte • Sphagnum • thermotolerance


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Isoprene (2-methyl-1,3-butadiene) emitting species occur in almost all major groups of land plants including dicots, monocots, gymnosperms, pteridophytes, and mosses (Rasmussen, 1978 ; Zimmerman, 1979 ; Evans et al., 1982 ; Isidorov, Zenkevich, and Ioffe, 1985 ; Hewitt and Street, 1992 ). Dicots, gymnosperms, and pteridophytes have similar light and temperature responses of isoprene emission (Sanadze and Kursanov, 1966 ; Tingey et al., 1979 , 1987 ; Monson and Fall, 1989 ; Loreto and Sharkey, 1990 ). In all of these groups, a 10°C increase in temperature can increase isoprene emission two- to eightfold and isoprene emission generally saturates around 1000 µmol photons·m-2·s-1 (Tingey et al., 1979 , 1987 ; Evans, Tingey, and Gumpertz, 1985 ; Monson and Fall, 1989 ; Loreto and Sharkey, 1990 ; Sharkey and Loreto, 1993 ).

Isoprene increases thermotolerance of photosynthesis in oak and kudzu leaves (Sharkey and Singsaas, 1995 ; Sharkey, 1996 ; Singsaas et al., 1997 ). Singsaas et al. (1997) demonstrated a dose-dependent increase in thermotolerance of 0.5°–3.6°C by measuring chlorophyll fluorescence in low light. This protection occurred at leaf temperatures frequently experienced by leaves at the top of oak canopies (D. T. Hanson, J.-Z. Shi, E. L. Singsaas, and T. D. Sharkey, University of Wisconsin, unpublished data). Since isoprene emission can change rapidly with leaf temperature, it may be most beneficial to plants experiencing rapid temperature fluctuations (Singsaas et al., 1997 ). Relative to aqueous environments, plants in an aerial environment will experience greater temperature variability due to a larger radiant heat load and the low heat capacity of air relative to water. Exposure to new physical conditions on land required several physiological and structural changes for early land plants (Graham, 1993 ; Kenrick and Crane, 1997 ); a mechanism for protection from rapid temperature fluctuations may have been one of the necessary innovations for successful adaptation to land.

Here we report a survey of isoprene emission among bryophytes and pteridophytes and micrometeorological measurements of light and temperature experienced by Sphagnum moss in a northern Wisconsin bog. Based on these results we speculate on the evolutionary origins of light-dependent isoprene emission in the land plant lineage and the implications this has for early plant life on land.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Plant material
Bryophyte material for the isoprene emission survey was collected from Kemp Natural Resources Station (Woodruff, Wisconsin; 45°50'25'' N, 89°40'47'' W) and brought back to Madison, Wisconsin, for analysis. Axenic cultures of Polytrichum commune Hedw. were provided by AgResearch International Inc. (Madison, Wisconsin). Pteridophyte material used in the isoprene emission survey was obtained from the teaching collection in the Botany Department's greenhouses at the University of Wisconsin-Madison. Sphagnum capillifolium used for the light and temperature response measurements was collected from Jyme Lake Bog at Kemp Station in northern Wisconsin. Samples collected on 6 June 1997 were brought back to Madison and maintained at natural densities in a greenhouse while measurements were made. Samples collected during 16–21 July 1997 were analyzed promptly after collection at Kemp Station. Additional S. capillifolium collected from Kemp Station was grown in a controlled-environment chamber (model PGW36, Conviron, Winnipeg, Manitoba, Canada) by pulverizing the top 2 cm of moss tissue in a blender and spreading it onto commercially available, dried Sphagnum moss (Bruce Company, Madison, Wisconsin). Plants were misted daily to field capacity with de-ionized water and weekly with one-tenth strength Gamborg's B-5 basal medium with minimal organics (catalog number G-5893, Sigma, St. Louis, Missouri). Light levels were ~250 µmol photons·m-2·s-1 with a 16 h daylength, and day/night growth temperatures were 18°/16°C.

Gas exchange
All measurements of photosynthesis and isoprene are based on the ground area covered by mosses growing at natural density. The natural density of moss samples was maintained by inverting the bottom of a plastic petri dish and pressing it into a patch of Sphagnum moss. Using the petri dish as a guide, the moss was cut at a depth of 1.5 cm with a pair of scissors. Photosynthesis was measured using a portable, open gas exchange system (LI-COR 6400, Lincoln, Nebraska) with a custom-built, water jacketed, glass chamber. Isoprene was measured by sampling from the air flow exiting the chamber using a portable gas chromatograph (Sentoscreen, Sentex Inc., Ridgefield, New Jersey). Sample times spanned 30–60 s and a condenser in an ice bath was installed between the chamber and the chromatograph to remove water from each sample prior to analysis. Light was provided by a slide projector mounted in a fixed position above the chamber. The photon flux at the moss surface was varied through the use of wire screens and monitored with a small gallium arsenide photodiode (part number G1118, Hamamatsu Corp., Bridgewater, New Jersey). The method used to generate isoprene standards is described in Singsaas et al. (1997) . Moss temperature was controlled by varying temperature in the water jacket of the moss chamber with a circulating water bath. Temperature was monitored with a 3 mil (0.0762 mm) wire thermocouple attached to the capitulum of a centrally located Sphagnum shoot.

Survey techniques
Pteridophytes were surveyed with a custom-built open gas exchange system and a gas chromatograph with a photoionization detector (Shimadzu Corp., Kyoto, Japan) as described in Sharkey and Loreto (1993) . Bryophytes in this survey were first checked with the same system described in the gas exchange section. This method was sensitive enough to resolve emission rates of ;lt60 pmol isoprene·m-2·s-1. For greater sensitivity, bryophyte samples were placed in 145-mL Erlenmeyer flasks sealed with a septum, incubated in growth chambers at 25°C and ~550 µmol photons·m-2·s-1 for several hours, and 10-mL air samples were assayed using a gas chromatograph with a photoionization detector (Shimadzu Corp., Kyoto, Japan). This increased resolution to <5 pmol isoprene·m-2·s-1.

Chlorophyll fluorescence
Chlorophyll fluorescence was measured with a pulse-amplitude modulated chlorophyll fluorometer (PAM-101, Walz, Effeltrich, Germany). Modulated excitation energy and the fluorescence signal were transmitted through a bifurcated fiber-optic cable to the plant material. Sphagnum capillifolium samples were cut to a depth of ~1.5 cm from a ground area of 1.6 cm2. These samples were placed in a fluorescence chamber which consisted of a polyvinyl chloride (PVC) T-connector for 0.5 inch (1.27 cm) pipe. Two of the open ends were sealed with septa (one for injections and the other for thermocouple wires) and the third open end allowed for a gas-tight seal with the fiber-optic cable. A copper-constantan thermocouple made from 3 mil (0.0762 mm) wire was twisted around a central capitulum and the sample was placed in the fluorescence chamber. The sample was kept in darkness for 30 min to reduce isoprene production and then the chamber was flushed with compressed air before measurements were made.

At the start of a run, the fluorescence chamber was submersed in a 25°C water bath and a baseline level of fluorescence was determined using low light (3.5 µmol photons·m-2·s-1). In runs with exogenous isoprene, a 140-µL injection of isoprene gas in nitrogen was added to the 9-mL chamber for a final concentration of 20 ppm. Air samples (250 µL) were taken from the chamber at the end of each run to determine the final concentration of isoprene. All isoprene concentration measurements were made with the Shimadzu Corp. (Kyoto, Japan) gas chromatograph described in the survey techniques section. To measure the temperature response of chlorophyll fluorescence, the water bath temperature was increased at a rate of 2°C/min. Fluorescence and temperature signals were recorded by a strip chart recorder.

Micrometeorology
Air temperature, moss temperature, and light level were measured at 5-s intervals for at least five continuous hours in the middle of the day on two occasions at Kemp Station. Light was measured with gallium arsenide photodiodes (part number G1118, Hamamatsu Corp., Bridgewater, New Jersey), and temperature was measured with spot-welded, chromel-constantan thermocouples made from 3 mil (0.0762 mm) wire. Air temperature was measured with a single-junction thermocouple with an aluminum foil shield to block direct solar radiation. The difference between moss and air temperature was measured with a differential thermocouple (Fig. 1). One junction was looped around the capitulum of the Sphagnum moss and pulled tight until it was embedded in the capitulum and thus shaded from direct solar radiation by upper branches and leaves in the capitulum. The other junction was a few cm away and shaded from direct solar radiation with a piece of aluminum foil (Fig. 1). Care was taken to minimize blockage of air flow around the thermocouple junctions that were shielded by aluminum foil. Absolute Sphagnum temperatures were determined by adding the air temperature to the difference between moss and air temperature. All data were logged with a CR-10 data logger and AM32 multiplexer from Campbell Scientific (Logan, Utah). Measurements were made on a Sphagnum bog in four different locations on 6 June: 1 m above water level; the top of an exposed hummock (S. fuscum, 40 cm above water surface); an exposed area of Sphagnum lawn (S. capillifolium, 10 cm above water surface); and in an exposed hollow (S. recurvum, 2.5 cm above water surface). On 17 and 18 July measurements were also made on a Sphagnum bog in the same types of locations as in June, except a shaded area of Sphagnum lawn (S. capillifolium, 10 cm above water surface) was monitored instead of a hollow.



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  		Fig. 1. Thermocouple setup for directly measuring the difference between moss temperature and air temperature. One thermocouple junction is embedded in the capitulum of the Sphagnum moss and the other junction is a few centimetres away and shaded from direct solar radiation with a piece of aluminum foil. The wire between the two junctions is constantan and is spot welded to chromel wire to create the thermocouple junction. The chromel wires are connected to copper wire, which is attached to the data logger. The chromel-copper junctions are insulated to ensure that both junctions are at the same temperature.

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Survey of isoprene emission in early divergent embryophytes
Of 32 pteridophyte species surveyed, 16 (50%) emitted detectable levels of isoprene (Table 1). Fifteen of the 16 mosses surveyed (94%) emitted isoprene, and no species of liverworts or hornworts examined emitted detectable levels of isoprene (Table 2). Axenic cultures of Polytrichum commune emitted isoprene, which ruled out contaminants as the source for isoprene. Overall, isoprene-emitting species were less common in later divergent land plant groups (Fig. 2).


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  		Table 1. Pteridophytes surveyed for isoprene emission.

 

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  		Table 2. Bryophytes surveyed for isoprene emission.

 


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  		Fig. 2. Frequency of isoprene emission in surveyed land plants. Land plant groups are arranged according to evolutionary position as determined by rbcL sequences (Mishler et al., 1994 ; Lewis, Mishler, and Vilgalys, 1997 ). The gymnosperm and angiosperm data were derived from a database of results from 59 publications. The database is available on the web at http://www.es.lancs.ac.uk/es/people/pg/pas/download.html and from the authors.

 
Characterization of isoprene emission in Sphagnum
In S. capillifolium, isoprene emission saturated at ~600 µmol photons·m-2·s-1 but the maximum emission rate in July was ~65% greater than in June (Fig. 3). Isoprene emission increased with increasing temperature from 20° to 40°C (Fig. 4). At 35°C isoprene emission in July was twice the rate in June while photosynthesis remained the same (Fig. 4).



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  		Fig. 3. Light response of photosynthesis ({circ}) and isoprene emission ({blacksquare}) from S. capillifolium in June and July. Capitulum temperature was 30°C. PAR, photosynthetically active radiation.

 


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  		Fig. 4. Temperature response of photosynthesis ({circ}) and isoprene emission ({blacksquare}) from S. capillifolium in June and July. Measurements were made at 1000 µmol photons·m-2·s-1.

 
Thermotolerance
When S. capillifolium was heated in the fluorescence chamber, fluorescence increased rapidly at 45.2° ± 0.1°C. The low light level used in the fluorescence measurement allowed some isoprene synthesis resulting in 1.8 ± 0.1 µmol/mol isoprene at the end of the experiment. When isoprene was added to the fluorescence chamber, yielding a final concentration of 10.0 ± 0.8 µmol/mol isoprene, fluorescence increased at 45.8° ± 0.1°C. This represents an increase in thermotolerance of 0.6°C (P = 0.03, N = 3). Singsaas et al. (1997) also found a 0.6°C increase in thermotolerance over this range of isoprene concentrations in kudzu (Pueraria lobata [Willd.] Ohwi.) (Fig. 5).



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  		Fig. 5. Measured and predicted values for the increase in thermotolerance in S. capillifolium resulting from the addition of isoprene. Increasing the isoprene concentration in the air around Sphagnum shoots from 1.8 ± 0.1 to 10 ± 0.8 µmol/mol isoprene resulted in a 0.6°C (P = 0.03, N = 3) increase in thermotolerance (see arrows). The predicted increase in thermotolerance for this change in isoprene concentration is 0.6°C, represented by the linear regression [y = -0.33 + 0.86 x log(isoprene)] redrawn from the dose response for kudzu from Singsaas et al. (1997) .

 
Micrometeorology on a northern Wisconsin bog
Sphagnum capitula reached higher temperatures and had larger temperature fluctuations at 10 cm above the water surface (lawn) than at 2.5 cm above the water surface (hollow) (Fig. 6). Within a 3-min period, when a cloud passed overhead (Fig. 6), the temperature of Sphagnum in the lawn decreased from 34.2°C to 21.5°C. The largest temperature change of Sphagnum in the hollow during this 10-min period was from 25.2°C to 22.6°C (Fig. 6). Light levels in June (Fig. 6) were almost always above the saturation level of 600 µmol photons·m-2·s-1 for isoprene emission (Fig. 3).



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  		Fig. 6. Temperature and light fluctuations in Sphagnum in a northern Wisconsin bog in June. Data were collected every 5 s for five continuous hours. This is a representative 10-min sample of temperatures in a Sphagnum lawn ({blacksquare}); a Sphagnum hollow ({blacktriangleup}); surface water temperatures ({circ}); and PAR (photosynthetically active radiation) at 1 m above the water ({square}). Within a 3-min period when a cloud passed overhead, Sphagnum in the lawn changed from 34.2°C to 21.5°C (large arrowhead), while Sphagnum in the hollow changed from 25.2°C to 22.6°C (small arrowhead). The cloud shadow passed over the light sensor and the two thermocouples at slightly different times, explaining why the moss temperature changes do not correlate precisely with the PAR change.

 
Sphagnum lawn temperatures averaged 3.1°C above the mean air temperature of 21.2°C (measured at 1 m above the water surface) in June and 1.6°C above the mean air temperature of 32.5°C in July when data were averaged over 5- and 7 h periods, respectively. Maximum moss temperatures recorded were 35.1°C in June and 45.0°C in July and occurred in the lawn in each case (Table 3). In all cases, the hummock (40 cm above the water surface) and exposed lawn were in similar light environments (data not shown), but the average temperature of the Sphagnum in the lawn was 1.2°C higher than the hummock in June and 3.4°C higher in July (Table 3). However, temperature fluctuation (as measured by the variance) increased as distance above the water surface increased (Table 3). In July, Sphagnum in a shaded lawn site reached higher maximum temperature than Sphagnum in a fully exposed lawn site and the shaded moss had a larger temperature variance than the exposed site (Table 3).


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  		Table 3. Sphagnum capillifolium capitulum temperature and air temperature (°C) on (A) 6 June and (B) 17 July. Variance was computed as the square of the standard deviation.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Isoprene emission is much more common in mosses than any other major group of land plants (Fig. 2). Our results show that isoprene emission from Sphagnum (Figs. 3, 4) and other moss species (data not shown) responded to light and temperature in a similar way as isoprene emission from ferns, gymnosperms, and angiosperms (Sanadze and Kursanov, 1966 ; Tingey et al., 1979 , 1987 ; Evans, Tingey, and Gumpertz, 1985 ; Monson and Fall, 1989 ; Loreto and Sharkey, 1990 ). Isoprene emission from mosses frequently consumes 0.5–8% of net carbon fixed by photosynthesis (D. T. Hanson and T. D. Sharkey, University of Wisconsin, unpublished data). Sphagnum also exhibits weather-mediated changes in capacity for isoprene emission (Figs. 3, 4), as has been seen in higher plants (Steinbrecher et al., 1997 ; Sharkey et al., in press ). Most importantly, using measurements of chlorophyll fluorescence, we demonstrated that isoprene provides the same level of increase in thermotolerance in Sphagnum (and likely all other groups of land plants) as is seen in oak and kudzu (Sharkey and Singsaas, 1995 ; Singsaas et al., 1997 ).

Researchers studying bryophytes in Northern Europe, the Arctic, and Antarctica show that bryophytes in exposed areas commonly reach temperatures of 30°–40°C, while the mosses are still moist and presumably active (Proctor, 1982 ; Longton, 1988 ; Sveinbjornsson and Oechel, 1992 ). Our data corroborate the results of these studies by showing that Sphagnum temperatures in northern Wisconsin bogs frequently exceed 35°–40°C in midsummer (Table 3), while the moss is still moist and functioning. In addition, Sphagnum temperatures in the lawn and hummock fluctuate just as much as higher plant leaf temperatures (Fig. 6). Even Sphagnum in the shade of shrubs and sedges experiences enough temperature fluctuation (Table 3) to predict that it would benefit from isoprene production.

Molecular evidence places bryophytes at the base of the monophyletic embryophytes with ferns diverging at an intermediate level prior to the evolution of angiosperms (Graham, Delwiche, and Mishler, 1991 ; Graham, 1993 , 1996 ; Mishler et al., 1994 ; Kenrick and Crane, 1997 ). Within the bryophytes, molecular data suggest liverworts are the first divergent land plants from charophycean algae and place mosses closer to the tracheophytes (Capesius and Bopp, 1997 ; Lewis, Mishler, and Vilgalys, 1997 ; Qiu et al., 1998 ). The pattern of decreasing frequency of isoprene emission from mosses to ferns and then to angiosperms (Fig. 2) shows that isoprene emission has become less common during the diversification of land plants. It also suggests an origin of light-dependent isoprene emission within the bryophytes in an organism diverging after the liverworts. A few reports have suggested isoprene emission from green algae (Bonsang, Polle, and Lambert, 1992 ; Milne et al., 1995 ; McKay et al., 1996 ), but the authors suggest the emission could be explained by bacterial contamination (Milne et al., 1995 ) or nonenzymatic breakdown of other compounds (McKay et al., 1996 ). In any case, it is clear that any algal isoprene emissions are not on the same scale as that seen in land plants.

The transition from growth in an aquatic environment to growth in an aerial environment could have provided a selective pressure favoring the evolution of thermotolerance mechanisms such as isoprene emission. Due to the large heat capacity of water compared to air, submersed organisms do not change temperature as rapidly as those growing in air. The results of this study show that Sphagnum capitula farther from surface water experience higher temperature maxima and greater temperature fluctuation than capitula closer to the water (Fig. 6, Table 3). Liverworts and hornworts rarely grow more than a few millimetres above their substrate (Schuster, 1966 ; Crum, 1991 ), and due to their low profile, they are not as likely to experience high temperatures and/or large temperature fluctuations as taller plants. In addition, liverworts generally grow in moist, shady environments (Schuster, 1966 ; Crum, 1991 ), and limited studies show that most liverworts do not tolerate heat and water stress very well (Clausen, 1964 ). Therefore, liverworts and hornworts are not likely to benefit from isoprene emission and the absence of isoprene emission may restrict them to moist or shady environments.

Edwards and Selden (1992) proposed four phases of colonization of land with gradual change between them. They hypothesized that microbial mats (prokaryotes and later algae) were followed by bryophyte-like plants (supported by fossil evidence), which overlapped with small axially organized plants with terminal sporangia (probably allied with tracheophytes), and finally, a major adaptive radiation phase. In this scenario, light-dependent isoprene emission (unique to land plants) would have evolved in bryophyte-like plants, which were the first organisms in the embryophyte lineage to live entirely in an aerial environment. Subsequently, many plants may have lost the capacity for isoprene emission in favor of other thermotolerance mechanisms, such as the low molecular weight chloroplast heat shock protein (Waters, Garrett, and Vierling, 1996 ; Heckathorn et al., 1998 ).

Given the protective function of isoprene, we can reasonably hypothesize why isoprene emission is so widespread in land plants and extremely common in mosses. We believe the thermal and correlated dessication stress of life on land provided the selective pressure for protecting photosynthesis from rapid temperate fluctuation. This protection was provided by the evolution of light-dependent isoprene emission in the bryophytes.


   FOOTNOTES
 
1 The authors thank Dr. Rowan Sage (University of Toronto, Toronto, Canada) for use of his moss photosynthesis chamber; Dr. Ray Fall (University of Colorado, Boulder, Colorado) for helpful discussions and information on bacteria and algae; Dr. Peter Bilkey of AgResearch International Inc. (Madison, Wisconsin) for axenic moss material and help with growing mosses; Kandis Elliot for illustration of Fig. 1 ; Kemp Natural Resource Station (Woodruff, Wisconsin) manager Tom Steele for use of the station lab and natural areas, and the Davis Fund from the University of Wisconsin Botany Department for travel expenses. Research supported by NSF grant IBN 9317900 and US EPA grant CR 823791. Back

4 Author for correspondence. Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Bonsang, B., C. Polle, and G. Lambert. 1992 Evidence for marine production of isoprene. Geophysical Research Letters 19: 1129–1132.[CrossRef][ISI]

Capesius, I., and M. BOPP. 1997 New classification of liverworts based on molecular and morphological data. Plant Systematics and Evolution 207: 87–97.[CrossRef][ISI]

Clausen, E. 1964 The tolerance of hepatics to desiccation and temperature. Bryologist 67: 411–417.

Crum, H. 1991 Liverworts and hornworts of southern Michigan. University of Michigan Herbarium, Ann Arbor, MI.

Edwards, D., and P. A. Selden. 1992 The development of early terrestrial ecosystems. Botanical Journal of Scotland 46: 337–365.

Evans, R. C., D. T. Tingey, and M. L. Gumpertz. 1985 Interspecies variation in terpenoid emissions from engelmann and sitka spruce seedlings. Forest Science 31: 132–142.

———, ———, ———, and W. F. Burns. 1982 Estimates of isoprene and monoterpene emission rates in plants. Botanical Gazette 143: 304–310.

Graham, L. E. 1993 The origin of land plants. Wiley&Sons, New York, NY.

———. 1996 Green algae to land plants: an evolutionary transition. Journal of Plant Research 109: 241–251.[CrossRef][ISI]

———, C. F. Delwiche, and B. D. Mishler. 1991 Phylogenetic connections between the ‘green algae’ and the ‘bryophytes.’ Advances in Bryology 4: 213–244.

Heckathorn, S. A., C. A. Downs, T. D. Sharkey, and J. S. Coleman. 1998 The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiology 116: 439–444.[Abstract/Free Full Text]

Hewitt, C., and R. A. Street. 1992 A qualitative assessment of the emission of non-methane hydrocarbon compounds from the biosphere to the atmosphere in the UK: present knowledge and uncertainties. Atmospheric Environment 26A: 3069–3077.

Isidorov, V. A., I. G. Zenkevich, and B. V. Ioffe. 1985 Volatile organic compounds in the atmosphere of forests. Atmospheric Environment 19: 1–8.

Jones, D. J. 1987 Encyclopaedia of ferns. Timber Press, Portland, OR.

Kenrick, P., and P. Crane. 1997 The origin and early evolution of plants on land. Nature 389: 33–39.[CrossRef]

Lewis, L. A., B. D. Mishler, and R. Vilgalys. 1997 Phylogenetic relationships of the liverworts (Hepaticae), a basal embryophyte lineage, inferred from nucleotide sequence data of the chloroplast gene rbcL. Molecular Phylogenetics and Evolution 7: 377–393.

Longton, R. E. 1988 Radiation and microclimate. In R. E. Longton, Biology of polar bryophytes and lichens, 106–140. Cambridge University Press, Cambridge, UK.

Loreto, F., and T. D. Sharkey. 1990 A gas-exchange study of photosynthesis and isoprene emission in Quercus rubra L. Planta 182: 523–531.[CrossRef][ISI]

McKay, W. A., M. F. Turner, B. M. R. Jones, and C. M. Halliwell. 1996 Emissions of hydrocarbons from marine phytoplankton—some results from controlled laboratory experiments. Atmospheric Environment 30: 2583–2593.[CrossRef][ISI]

Milne, P. J., D. D. Riemer, R. G. Zika, and L. E. Brand. 1995 Measurement of vertical distribution of isoprene in surface seawater, its chemical fate, and its emission from several phytoplankton monocultures. Marine Chemistry 48: 237–244.[CrossRef][ISI]

Mishler, B. D., L. A. Lewis, M. A. Buchheim, K. S. Renzaglia, D. J. Garbary, C. F. Delwiche, F. W. Zechman, T. S. Kantz, and R. S. Chapman. 1994 Phylogenetic relationships of the "green algae" and "bryophytes." Annals of the Missouri Botanical Garden 81: 451–483.[CrossRef][ISI]

Monson, R. K., and R. Fall. 1989 Isoprene emission from aspen leaves: the influence of environment and relation to photosynthesis and photorespiration. Plant Physiology 90: 267–274.[Abstract/Free Full Text]

Proctor, M. C. F. 1982 Physiological ecology: water relations, light and temperature response, carbon balance. In A. J. E. Smith [ed.], Bryophyte ecology, 333–382. Chapman Hall, New York, NY.

Qiu, Y.-L., Y. Cho, J. C. Cox, and J. D. Palmer. 1998 The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394: 671–674

Rasmussen, R. A. 1978 Isoprene plant species list. Special report, Washington State University, Pullman, WA.

Sanadze, G. A., and A. L. Kursanov. 1966 On certain conditions of the evolution of the diene C5H8 from poplar leaves. Soviet Plant Physiology 13: 184–189.

Schuster, R. M. 1966 The Hepaticae and Anthocerotae of North America. Columbia University Press, New York, NY.

Sharkey, T. D. 1996 Isoprene synthesis by plants and animals. Endeavor 20: 74–78.

———, and F. Loreto. 1993 Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia 95: 328–333.[CrossRef][ISI]

———, and E. L. Singsaas. 1995 Why plants emit isoprene. Nature 374: 769.

———, ———, M. T. Lerdau, and C. Geron. In press Weather effects on isoprene emission capacity and applications in emissions algorithms. Ecological Applications.

Singsaas, E. L., M. Lerdau, K. Winter, and T. D. Sharkey. 1997 Isoprene increases thermotolerance of isoprene emitting species. Plant Physiology 115: 1413–1420.[Abstract]

Steinbrecher, R., K. Hauff, R. Rabong, and J. Steinbrecher. 1997 Isoprenoid emission of oak species typical for the Mediterranean area: source strenth and controlling variables. Atmospheric Environment 31 (S1): 79–88.

Sveinbjornsson, B., and W. Oechel. 1992 Controls on the growth and productivity of bryophytes: environmental limitations under current and anticipated conditions. In J. W. Bates and A. M. Farmer [eds.], Bryophytes and lichens in a changing environment, 77–102. Oxford University Press, New York, NY.

Tingey, D. T., R. C. Evans, E. H. Bates, and M. L. Gumpertz. 1987 Isoprene emissions and photosynthesis in three ferns—the influence of light and temperature. Physiologia Plantarum 69: 609–616.[CrossRef]

———, M. Manning, L. C. Grothaus, and W. F. Burns. 1979 The influence of light and temperature on isoprene emission rates from live oak. Physiologia Plantarum 47: 112–118.[CrossRef]

Waters, E. R., J. L. Garrett, and E. Vierling. 1996 Evolution, structure and function of the small heat shock proteins in plants. Journal of Experimental Botany 47: 325–328.

Zimmerman, P. R. 1979 Determination of emission rates of hydrocarbons from indigenous species of vegetation in the Tampa/St. Petersburg Florida area. Washington State University, Pullman, WA. EPA 904/9–77–028.




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