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(American Journal of Botany. 2008;95:1225-1232.) doi: 10.3732/ajb.0800068 © 2008 Botanical Society of America, Inc. |
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Ecology |
2 Department of Biology, University of Oulu, P.O. Box 3000, FIN-90014, Oulu, Finl 3 Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, FIN-40014 Jyväskylä, Finl
Received for publication 21 February 2008. Accepted for publication 6 August 2008.
ABSTRACT
In most studies about dioecious plants, the role of arbuscular mycorrhizae (AM) and the potential sex-specific differences between the plant hosts have been overlooked. Because plant sexes frequently differ in drought tolerance and AM fungal colonization provides higher resistance to drought, we investigated whether the relation of mycorrhizal fungi with either male or female Antennaria dioica plants differs using a factorial experiment. We hypothesized that because AM usually increase growth rate and male plants usually grow larger than females, males should gain more benefit from the mycorrhizal symbiosis in terms of mineral nutrition and water supply. Because of higher demands of carbohydrates (C) in males, we expected males to allocate less C resources to the mycorrhizal fungus so that the associated fungi should benefit less of the association with males. In contrast to our initial hypothesis, the male plants, although faster growing under drought, did not gain more symbiosis-mediated benefits than did the females, and both sexes seemed to provide resources equally to their fungal symbiont. Therefore, we conclude that the two plant sexual morphs provide equal amounts of C to their fungal root symbionts and that they can gain specific benefits from the symbiosis, which, however, depend on soil water availability.
Key Words: Antennaria dioica • arbuscular mycorrhizae • Asteraceae • clonal growth • dioecy • drought • Glomus claroideum • mycorrhizal benefit • sexual dimorphism
Dioecious plant species are thought to be dimorphic as a result of selection for different reproductive optima for each sex (Lloyd and Webb, 1977
). Among dioecious plants, the two sexes allocate resources differently: females often invest relatively more resources into defense and reproduction, while males allocate more resources into vegetative growth (see Delph, 1999; Obeso, 2002 and references therein). Many studies report sexual dimorphism in life history traits after reproductive stage is achieved (see e.g., Geber et al., 1999), but less is known about the prereproductive stage as a result of the limitations of knowing the sex of a plant before flowers are produced for the first time. In recent years, however, the use of sex-specific genetic markers has provided a useful tool to identify plant sex. Tools for molecular genetic sexing are available for a limited but increasing number of species. Meanwhile, it is possible to use clonal plants for the same purpose; once a genet is sexed, the new ramets can be separated from the genet and studied knowing the sex. Research focusing on the vegetative phase is necessary because development to reproductive maturity depends on vegetative growth.
In most studies concerning life history traits in dimorphic plant species, the role of arbuscular mycorrhizas (AM) and the potential sex-specific differences have been overlooked. Arbuscular mycorrhizas are the most common form of mycorrhizal symbioses. They are formed in the roots of a wide variety of host plants by obligately symbiotic fungi of the phylum Glomeromycota (Schüßler et al., 2001). The relationship is ancient and was probably important in the colonization of land by vascular plants (Simon et al., 1993), which implies that dioecy in plants evolved during the 460 million years of coevolution between the AM fungi and land plants. In the AM symbiosis, photosynthates are allocated from the plant to the fungus, while the fungi acquire nutrients from the soil and pass them to the plant. The result of this is a net movement of P, N, and other minerals and water to the plant and of C to the fungus (Smith and Read, 1997). The resource exchange is considered to take place particularly in symbiosis-specific structures called arbuscules (Smith and Smith, 1990), and the AM fungus can store C in form of lipids in structures called vesicles (Jabaji-Hare et al., 1984). The fungus also produces large asexual resting spores that allow the fungus to pass unfavorable periods and the fungal population to persist in absence of host carbon for longer time.
Even though plant responses to colonization by AM fungi can range from growth promotion to growth depression (Janos, 2007), mycorrhizal plants are often more competitive and better able to tolerate environmental stress than nonmycorrhizal plants through improved nutrient acquisition (Smith and Read, 1997). In addition, the symbiosis may confer other benefits to the plant such as novel secondary compound production (Mosse et al., 1981), alleviation of salinity stress (Ruiz-Lozano et al., 1996), resistance to pathogens and herbivores (Azcón-Aguilar and Barea, 1992) and improved water acquisition (Ruiz-Lozano and Azcón, 1995). Drought is one of the most important abiotic factors limiting plant growth and reproduction in many regions (Kramer and Boyer, 1997). Different mortality due to different water availability can cause spatial segregation of the sexes in dioecious plant species (Houssard et al., 1992; Dudley, 2006). When this type of pattern exists, female plants usually perform better in wetter sites (for a list of cases, see e.g., Bierzychudek and Eckhart, 1988) and males better in drier sites (Freeman and McArthur, 1982; Ward et al., 2002), compared to their opposite sex. Indeed, water use efficiency (ratio of carbon fixed through photosynthesis to the amount of water lost through transpiration) has been found to be higher in males in almost all species studied (e.g., Leigh and Nicotra, 2003; Dawson et al., 2004; but see Kohorn, 1994 or Sleeman et al., 2002). Because AM colonization provides higher resistance to drought (Ellis et al., 1985; Augé, 2001; Porcel and Ruiz-Lozano, 2004) and the sexes frequently differ in drought tolerance (Freeman and McArthur, 1982; Houssard et al., 1992), one may hypothesize that the two sexes have evolved different mycorrhizal strategies when growing under conditions of different water availability. Because males usually grow larger under drought, one may expect them to profit more from mycorrhizas than females in terms of water uptake. Moreover, as drought also leads to nutrient deficiency (Pugnaire et al., 1993), higher growth rates in male plants may also render them more dependent on AM fungi for mineral nutrition.
In this study we investigated whether female and male plants in the dioecious model species Antennaria dioica have a different relationship with their AM symbionts. We hypothesized that because of the higher growth rate in males and because AM increase growth rate (Baas et al., 1989), male plants would benefit more from a mycorrhizal symbiosis for water and mineral nutrient resource acquisition than females of the same age. We assumed that there is a trade-off between resource allocation to the plant partner and resources available to the fungal symbiont. Consequently, because of the higher resource demand in males for growth, male plants should maintain lower mycorrhizal colonization rate than females, and the associated fungi should benefit less from the association with males. Because our preliminary field observations indicated that male Antennaria plants rather than females predominate in drier sites, we tested the plants under two water application regimes. We hypothesized that lowering the watering regime would reduce plant growth, but inoculation with AMF would help to alleviate this water stress.
MATERIALS AND METHODS
Study species
Our model plant, Antennaria dioica (L.) Gaertn. (Asteraceae) is a perennial, clonal, mat-forming, herbaceous plant that grows in heaths, dry grasslands, and sandy places. In addition, A. dioica is sometimes found in semiopen forests. It is widely distributed in temperate regions of the northern hemisphere although populations are declining due to the loss of suitable habitats (Eriksson, 1997). Antennaria dioica is dioecious, with female frequency ranging from 0 to 79% in Finland, with an average of 55% (S. Varga and M.-M. Kytöviita, unpublished manuscript). It has been previously reported to be colonized by AM fungi in the field (Harley and Harley, 1987; Eriksen et al., 2002).
Experimental design
In November 2003, A. dioica seeds collected from Muurame (62°07'N, 25°40'E) in central Finland were stratified for 2 weeks at 4°C in pots containing fine sand (grain size = 0.5 mm). After that, they were transferred to the greenhouse (16 h light, 20°C), and the seedlings were raised individually in pots (6.5 x 6.5 x 5 cm) filled with heat sterilized sand and vermiculite (4:1, v/v). The plants were transferred in September 2004 into larger pots (8 x 8 x 6.5 cm) using the same potting mixture. In December 2004, the seedlings were transferred to 5°C conditions for 4 months and then back to greenhouse conditions again. The sex of each plant individual was determined when the plants were flowering for the first time. In August 2005, the plants were divided into clonal fragments grown singly in a soil mix containing autoclaved garden soil, sand, and peat (2:2:1, v/v/v) supplemented with dolomite (5 g/L) to raise the pH to 6.20 and bone meal (1.5 g/L) to serve as a slow-release fertilizer.
The inoculation with AM fungal was performed in May 2006. Individual plants that had been divided into four fragments containing at least one ramet each were selected for the study to allow representation of the same individual genotype in each of the four treatments (described later). At the transplantation stage, all plants were weighed to determine their initial total biomass (root and shoot biomass) and number of ramets were counted. We selected clonal fragments of similar size to ensure we did not get effects due to differences in the initial plant biomass. Because of this, in the beginning of the experiment the sexes did not differ in plant total biomass (2.26 ± 0.25 g for females and 1.86 ± 0.24 g for males; F1,22 = 1.5, P = 0.23) or in the number of ramets (1.36 ± 0.08 for females and 1.44 ± 0.10 for males; F1,26 = 0.2, P = 0.70). Plant total biomass and the number of ramets were also similar among genotypes (Wald Z1 = 1.8, P = 0.08 and Wald Z1 = 1.7, P = 0.09, respectively). We performed a fully factorial block experiment with four factors: plant sex (female, male), AM inoculation (yes, no), watering regime (moderate, low), and plant genotype. Plant genotype was nested within sex. We selected clonal fragments from 14 female and 14 male individuals (28 genotypes). A similar number of ramets per clonal fragment (between 1 and 4) were allocated to each treatment combination (statistics not shown). Each clonal fragment was placed in a pot (12 x 13.5 x 6 cm) filled with the same soil mix as before. Half of the plants were inoculated with 2 mL water containing 125 spores of the AM fungus Glomus claroideum (referred as mycorrhizal plants hereafter), and the other half received the same amount of spore-wash water without spores (referred as nonmycorrhizal plants hereafter). The G. claroideum had originally been isolated from habitats of A. dioica in Ylistaro in central Finland (62°57'N, 22°31'E). All the plants received an additional 1 mL of a soil microbial suspension filtered through a 5.0 µm nitrocellulose Millipore (Millipore, Molsheim, France) filter to partially return the microflora to the sterilized soil. The plants were grown under greenhouse conditions at Oulu University Botanical Gardens (65°03'N, 25°27'E). Natural light was supplemented by 400 W Philips SON-T PIA Green Power lamps giving a light period of 18 h light/6 h darkness, with a light intensity of 392 ± 12 µmol•m–2•s–1 and a 20°C (light) and 16°C (dark) temperature regime. After plants grew for 2 months, the water application treatment started. The frequency of watering occasions was the same for the two treatments to facilitate watering. On each watering day, the moderate-watering treatment pots received 85 mL of water, that brought the water content of the pots to field capacity. The pots in the low-watering treatment received one-third volume less (57 mL). The plants were watered based on water depletion in the moderate-watering regime because we wanted to avoid water limitation in moderate-watering regime plants; therefore, the plants were watered when the substrate in the moderate-watering regime pots was moderately dry (every 2 to 3 days). Because drought of the substrate was dependent on the weather conditions and the plants’ increasing size, the watering frequency was adjusted accordingly over the duration of the experiment.
In October 2006, plant leaf chlorophyll fluorescence was measured (described later). In December 2006, 241 d after inoculation, the plants were watered and later on that day harvested, and shoot and root masses, and the number of ramets, floral shoots, and inflorescences (if any) were recorded, and roots were sampled to measure mycorrhizal colonization rate. Relative growth rate (RGR) was calculated as (log fresh total plant biomass at end – log fresh total plant biomass at beginning) ÷ number of experimental days. Mean ramet biomass was calculated by dividing the aboveground plant biomass by the number of ramets per pot.
Chlorophyll fluorescence measurements
Chlorophyll fluorescence was measured on a maximum water stress day using PAM-2000 chlorophyll fluorescence unit (Heinz Waltz, Effeltrich, Germany). The plants were dark adapted for 20 min and measured for variable fluorescence (Fv), which was calculated from minimal (F0) and maximal (Fm) fluorescence values. Five fully expanded leaves of each plant were measured, and the readings were then averaged (Spearmans’ rho intraclass correlations ranged between 0.55 and 0.80, P < 0.01). Dark-adapted values of Fv/Fm reflect the potential quantum efficiency of photosystem II (PSII) (Maxwell and Johnson, 2000). For healthy terrestrial leaves, Fv/Fm = 0.832 ± 0.004; values lower than this indicate a stress response (Björkman and Demmig, 1987).
Phosphorus content analysis
Plant shoot P content (mg per plant) and concentration (%, w/w) was determined using the procedure of John (1970). Plants’ aboveground biomass at the end of the experiment was dried in the oven (80°C, overnight) and milled. Plant material was acid digested using the Paar001H program in the Paar Physica multiwave sample preparation system (Perkin Elmer, Waltham, Massachusetts, USA). The P concentrations were measured colorimetrically, using an UV-160A Shimadzu analyzer from two subsamples, and the readings were then averaged. Correlation between the two subsamples was highly significant (Spearman’s rho = 0.996, P < 0.01). Shoot P contents were calculated by multiplication with the dry shoot biomass values.
Mycorrhizal analysis
The roots were stored in 50% ethanol and stained after clearing by incubation in 10% KOH for 4 d at room temperature and additional incubation in 1.5% alkaline H2O2 for 2 h at room temperature. After 2 h in 1% HCl, we incubated the roots at 80°C in 0.02% trypan blue staining solution for 2 h. The AM fungal root colonization was measured at 100x magnification as the proportion of intersects with hyphae, arbuscules, and vesicles in 10 root segments of 1.5 cm length. The AM fungal spores were extracted from the soil by wet-sieving and decanting, using a 50-µm sieve, then centrifuging at 3000 rpm in 60% sucrose solution for 3.5 min. All the spores per pot were counted at 12x magnification with a stereomicroscope.
Mycorrhizal plant benefit was defined as the performance ratio between mycorrhizal and nonmycorrhizal plants for final total plant biomass, RGR, number of ramets, ramet biomass, and shoot P concentration and P content. Because not all genotypes were represented at the end of the experiment due to plant death, mycorrhizal plant benefit was calculated by dividing the measured value for each mycorrhizal plant individual with the average value of the nonmycorrhizal plant individuals. Ratios higher than one indicate that plants profited, ratios lower than one indicate that plants suffered from mycorrhizal inoculation. Ratios close to one indicate no mycorrhizal benefit or cost for the plant from the symbiosis.
Data analysis
Differences in plant biomass and number of ramets in the beginning of the experiment were tested using a linear mixed-effects model with plant sex (male, M; female, F) as fixed factor and plant genotype nested within sex as a random factor. The significance of differences in plant variables were tested employing a linear mixed-effects model with plant sex (male, M; female, F), mycorrhizal inoculation (yes, AM; no, NM), and water treatment (moderate, Mod; low, Low) as fixed factors. Plant genotype was nested within sex and included in the model as a random factor to analyze its main effect, but we did not include the interactions with the other factors in the model due to lack of degrees of freedom in more complex designs. The random effect of plant genotype was estimated using restricted maximum likelihood (REML) given the unbalanced experimental design resulting from plant death. The Wald Z statistic is reported followed by its significance value (P). This Z statistic is obtained by dividing the random variable estimated via REML by its estimated asymptotic standard error. Note, however, that this test should not be taken as strictly conclusive (Fears et al., 1996). The effect of plant sex, genotype, and water treatment on mycorrhizal benefit was investigated using a linear mixed-effects model with plant sex, water treatment, and plant genotype as explained. The assumptions of normality were analyzed from the residuals of the model. Number of ramets, ramet mass, and shoot P concentration and content were analyzed from log transformed data, as was the benefit to ramet biomass. All other variables were analyzed using untransformed data. Thirty-four plants died during the experiment, and these plants were excluded from the analyses. All statistical analyses were conducted with the program SPSS version 16.0 (SPSS, Chicago, Illinois, USA).
RESULTS
Vegetative variables
After the 241 experimental days, total plant biomass ranged between 0.2 and 52 g (Fig. 1A). Fungal inoculation had a strong effect on all vegetative traits measured (Table 1 and Fig. 1). The effect of fungal inoculation interacted with the water treatment in terms of total plant biomass and number of ramets. There was also a near significant interaction between fungal inoculation and water treatment of RGR (Table 1 and Fig. 1); on average, mycorrhizal plants with moderate-watering regime were able to acquire more total biomass than mycorrhizal plants under the low-watering regime and had more ramets, but the opposite pattern was found for nonmycorrhizal plants (Fig. 1A, C). Sexual differences were only present in the number of ramets (P = 0.01) and RGR (P = 0.06) as females had fewer, but heavier ramets and mycorrhizal inoculation increased the number of ramets but decreased the average ramet mass (Table 1 and Fig. 1C, D). Mycorrhizal symbiosis increased shoot P concentration in both sexes from 0.09% to 0.22%, while there were no apparent effects by sex or water treatment on plant P nutrition (Table 1 and Fig. 1E, F). Differences due to plant genotype were only significant for ramet biomass (Table 1), which was also affected by the watering regime (Fig. 1D). Only a small proportion of individuals flowered during the experiment, and these data were not analyzed further. The analysis of chlorophyll fluorescence data revealed that only the watering treatment had a marginally near-significant effect (P = 0.06) on Fv/Fm (statistics not shown), as plants growing in the moderate-watering regime had higher value of Fv/Fm than plants growing in the low-watering regime (0.742 ± 0.006 vs. 0.718 ± 0.009), indicating higher stress in plants growing under low-watering conditions.
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Sexual differences in growth rates are common in dioecious plants. Generally, male plants grow faster than females (24 of 38 species reviewed by Delph, 1999). In our study, the two sexes of Antennaria dioica did not differ in biomass accumulation rate under the moderate-watering regime, but male plants had higher biomass when water was in short supply. The higher growth rate of males under drought agrees well with our field observations that male plants are more abundant in drier sites than females (S. Varga and M.-M. Kytöviita, unpublished manuscript). Males have been shown to occupy drier or less resource rich microhabitats also in other dioecious species (Bierzychudek and Eckhart, 1988). Antennaria dioica male plants had also higher clonal growth rate (greater number of ramets) as reported previously for male plants in many other dioecious species (Freeman et al., 1976; Escarré and Houssard, 1991; Fujitaka and Sakai, 2007; but see Connor, 1984) but only under a low-watering regime. Females overall had larger ramets at both watering regimes in our study, which may indicate that females require larger amounts of resources to reach sexual maturity than males as pointed out before (Delph, 1999).
We used an isolate of Glomus claroideum as the fungal symbiont in this experiment. Although plant benefit of the symbiosis under natural conditions depends on the whole microbial soil community (Koide and Li, 1991), this particular isolate of G. claroideum has been shown to provide large benefits to all plant species tested so far under our experimental conditions (Kytöviita et al., 2003; Kytöviita and Ruotsalainen, 2007; Pietikäinen and Kytöviita, 2007). As expected, symbiosis with G. claroideum provided significant growth and nutrient benefits also to A. dioica in this study. However, here we show for the first time that the sexes of dioecious species may gain a different benefit from the same mycorrhizal symbiont: symbiosis with the AM fungus was more beneficial for female plants, which were able to acquire larger amount of biomass under moderate water availability. Under the low-watering regime, the sexes gained similar benefit. From this, we can conclude that the sexes of Antennaria dioica have sex-specific benefits from the fungal symbiont and, in contrast to our hypothesis, the male plants, although faster growing under drought, do not gain more symbiosis-mediated benefits than females.
Both the fungal and plant partners are thought to generally gain benefits in the AM symbiosis. In our case, the amount of fungus in plant roots (frequency of fungal structures) and the amount of spores produced by the fungus may be considered as indicators of the benefit of the symbiosis to the fungus. In contrast to our initial hypothesis, we found no differences between the two sexes in fungal parameters and therefore conclude that both sexes seem to provide equal amounts of resources to their fungal root symbiont. We should point out here that only a few sinks of C were measured in this experiment (intraradical fungal structures and spore production). In AM, the external hyphae growing in the surrounding soil, their turnover, and their respiration also constitute a great part of the C cycle between the plant and the mycorrhizal symbiont (Gavito and Olsson, 2003; Heinemeyer et al., 2006), which should also be considered in resource allocation calculations. Interestingly, lowering the water supply tended to increase the number of fungal vesicles. In contrast, spore production was reduced in our system under low water supply. Drought is reported to affect vesicle and spore production in AM systems differently (Augé, 2001). This lack of a consistent pattern may be due to the different conditions used in the various studies and due to the complexity of the interactions between several symbiosis partners and abiotic factors (Johnson et al., 1997). Because vesicles act as storage organs, which probably allow the fungus to be temporarily independent of C acquisition from the host plant, it seems logical to expect a decrease in the number of vesicles as a response to the decrease in resource availability. However, because vesicles may be converted to spores in some AMF species under some conditions (Dodd et al., 2000), one may not exclude the possibility that the low water content in the soil could have delayed such conversion from vesicles to spores.
The effect of mycorrhizal symbiosis on plant clonal growth traits has rarely been studied. Growth rate in clonal plants include biomass increment as well as multiplication via production of new ramets. In the current study, mycorrhizal symbiosis increased the number of ramets in A. dioica as reported previously for Prunella vulgaris (Streitwolf-Engel et al., 1999). The higher number of ramets could be simply due to the larger biomass in the mycorrhizal plants. However, this seems not to be the case in A. dioica because the average size of ramets was significantly reduced in mycorrhizal symbiosis, indicating that the symbiosis stimulated the formation of new ramets more than biomass accumulation. It has been suggested that, through affecting host clonal growth traits, the AM fungi may affect host plant population sizes (Streitwolf-Engel et al., 2001). In our study, female plants produced fewer but heavier ramets. Because sexual reproduction is directly proportional to clonal size and thus to ramet number (Hartnett, 1990; Schmid et al., 1995), increments in the number of clonal growth units could be advantageous for male plants under conditions of low water availability. This possibility is supported by our field observations that male plants flower more than females in dry years (S. Varga and M.-M. Kytöviita, unpublished manuscript). It is known that AMF can enhance photosynthetic rates in host plants (Parádi et al., 2003). Our results of chlorophyll fluorescence data indicate that photosynthetic rate may be higher in well-watered plants, thus agreeing with the higher RGR observed in these plants, but AM inoculation had no effect on chlorophyll fluorescence measurements.
To our knowledge, this is the third study dealing with sex-specific mycorrhizal relationships in dimorphic plant species. Our present work agrees with that of Gehring and Whitham (1992), who reported similar AM colonization levels in both sexes of the dioecious Juniperus monosperma. Previously, we found that AM fungal colonization of the two sexes of the gynodioecious Geranium sylvaticum did not differ in the field (Varga et al., in press). In the present work, we found no difference in resource allocation to the mycorrhizal symbiont Glomus claroideum by two sexes of the host Antennaria dioica. Female plants benefited more from the mycorrhizal symbiosis in the tested prereproductive phase under well-watered conditions, but both female and male plants benefited equally when water level was lowered. Because reproduction incurs larger costs to females (Obeso, 2002) and because reproduction is known to alter resource allocation patterns in plants, the present results may not hold for the reproductive period. In the current study, we did not find any link between the symbiosis-mediated P acquisition and plant sex, so the mechanisms of the sex-specific responses to arbuscular mycorrhizas seem not to be linked to nutrition. It may also be possible that these effects are mediated by hormones; AMF are reported to influence plant hormonal status (Ludwig-Müller, 2000). Males of dioecious species may perform better than females in a low-resource environment because of inherent physiological differences to females, but these differences seemed not to have been influenced by mycorrhizal inoculation in A. dioica. To fully evaluate differences in resource allocation and costs of reproduction between the sexes of dioecious plants, we need to take into account mycorrhizal associations as mediators of mineral and carbohydrate metabolism.
FOOTNOTES
1 The authors thank M. Vestberg (Agrifood Finland) for the use of his Glomus claroideum isolate, the personnel at the Botanical Gardens of the University of Oulu for plant care, D. Carrasco for plant harvesting, T. Törmänen for the P analyses, and two anonymous referees for their comments and suggestions. This study was funded by Oulangan Rahasto, Societas Pro Fauna et Flora Fennica and Oskar Öflundin Säätiö. 
4 Author for correspondence (e-mail: Sandra.varga.estany{at}oulu.fi); Department of Biology, University of Oulu, P.O. Box 3000, FIN-90014, Oulu, Finland; phone: +358-8-553 1525; fax: +358-8-553 1061
LITERATURE CITED
Augé, R. M. 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11: 3–42.[CrossRef][Web of Science]
Azcón-Aguilar, C., AND J. M. Barea. 1992. Interactions between mycorrhizal fungi and other rhizosphere microorganisms. In M. J. Allen [ed.], Mycorrhizal functioning: An integrative plant–fungal process, 163–198. Chapman and Hall, New York, New York, USA.
Baas, R., A. van der Werf, AND H. Lambers. 1989. Root respiration and growth in Plantago majoras affected by vesicular-arbuscular mycorrhizal infection. Plant Physiology 91: 227–232.
Bierzychudek, P., AND V. Eckhart. 1988. Spatial segregation of the sexes of dioecious plants. American Naturalist 132: 34–43.[CrossRef][Web of Science]
Björkman, O., AND B. Demmig. 1987. Photon yield of O2 evolution and chlorophyll fluorescence at 77 K among vascular plants of diverse origins. Planta 170: 489–504.[CrossRef][Web of Science]
Connor, H. E. 1984. Breeding systems in New Zealand grasses. IX. Sex ratios in dioecious Spinifex sericeus. New Zealand Journal of Botany 22: 569–574.[Web of Science]
Dawson, T. E., J. K. Ward, AND J. R. Ehleringer. 2004. Temporal scaling of physiological responses from gas exchange to tree rings: A gender-specific study of Acer negundo (Boxelder) growing under different conditions. Functional Ecology 18: 212–222.[CrossRef]
Delph, L. F. 1999. Sexual dimorphism in live history. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 149–174. Springer-Verlag, Berlin, Germany.
Dodd, J. C., C. L. Boddington, A. Rodriguez, C. Gonzalez-Chavez, AND I. Mansur. 2000. Mycelium of arbuscular mycorrhizal fungi (AMF) from different genera: Form, function and detection. Plant and Soil 226: 131–151.[CrossRef][Web of Science]
Dudley, L. S. 2006. Ecological correlates of secondary sexual dimorphism in Salix glauca (Salicaceae). American Journal of Botany 93: 1775–1783.
Ellis, J. R., H. J. Larsen, AND M. G. Boosalis. 1985. Drought resistance of wheat plants inoculated with vesicular arbuscular mycorrhizas. Plant and Soil 86: 369–378.[CrossRef][Web of Science]
Eriksen, M., K. E. Bjureke, AND S. S. Dhillion. 2002. Mycorrhizal plants of traditionally managed boreal grasslands in Norway. Mycorrhiza 12: 117–123.[Web of Science][Medline]
Eriksson, O. 1997. Colonization dynamics and relative abundance of 3 plant species (Antennaria dioica, Hieracium pilosella and Hypochoeris maculata) in dry semi-natural grasslands. Ecography 20: 559–568.
Escarré, J., AND C. Houssard. 1991. Change in sex ratio in experimental populations of Rumex acetosa. Journal of Ecology 79: 379–387.[CrossRef][Web of Science]
Fears, T. R., J. Benichou, AND M. H. Gail. 1996. A reminder of the fallibility of the Wald statistic. American Statistician 50: 226–227.[CrossRef]
Freeman, D. C., L. G. Klikoff, AND K. T. Harper. 1976. Differential resource utilization by the sexes of dioecious plants. Science 193: 597–599.
Freeman, D. C., AND E. D. McArthur. 1982. A comparison of twig water stress between males and females of six species of desert shrubs. Forest Science 28: 304–308.[Web of Science]
Fujitaka, T., AND S. Sakai. 2007. Sexual dimorphism in clonal forms and ramet distribution patterns in Rumex acetosella (Polygonaceae). Ecological Research 22: 248–254.[CrossRef][Web of Science]
Gavito, M. E., AND P. A. Olsson. 2003. Allocation of plant carbon to foraging and storage in arbuscular mycorrhizal fungi. FEMS Microbiology Ecology 45: 181–187.[CrossRef][Medline]
Geber, M. A., T. E. Dawson, AND L. F. Delph [eds.], 1999. Gender and sexual dimorphism in flowering plants. Springer-Verlag, Berlin, Germany.
Gehring, C. A., AND T. G. Whitham. 1992. Reduced mycorrhizas on Juniperus monosperma with mistletoe: The influence of environmental stress and tree gender on a plant parasite and a plant–fungal mutualism. Oecologia 89: 298–303.[Web of Science]
Harley, L., AND E. L. Harley. 1987. A check-list of mycorrhiza in the British flora. New Phytologist 105: 1–102.[Web of Science]
Hartnett, D. C. 1990. Size-dependent allocation to sexual and vegetative reproduction in four clonal composites. Oecologia 84: 254–259.[Web of Science]
Heinemeyer, A., P. Ineson, N. Ostle, AND A. H. Fitter. 2006. Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. New Phytologist 171: 159–170.[CrossRef][Web of Science][Medline]
Houssard, C., J. Escarré, AND N. Vartanian. 1992. Water-stress effects on successional populations of the dioecious herb, Rumex acetosella L. New Phytologist 120: 551–559.[CrossRef][Web of Science]
Jabaji-Hare, S., A. Deschene, AND B. Kendrick. 1984. Lipid content and composition of vesicles of a vesicular-arbuscular mycorrhizal fungus. Mycologia 76: 1024–1030.[CrossRef][Web of Science]
Janos, D. P. 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17: 75–91.[CrossRef][Web of Science][Medline]
John, M. K. 1970. Colorimetric determination of phosphorus in soil and plant materials with ascorbic acid. Soil Science 109: 214–220.[Web of Science]
Johnson, N. C., J. H. Graham, AND F. A. Smith. 1997. Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytologist 135: 575–585.[CrossRef][Web of Science]
Kohorn, L. U. 1994. Shoot morphology and reproduction in jojoba—Advantages of sexual dimorphism. Ecology 75: 2384–2394.[CrossRef][Web of Science]
Koide, R. T., AND M. Li. 1991. Mycorrhizal fungi and the nutrient ecology of three old field annual plant species. Oecologia 85: 403–412.[CrossRef][Web of Science]
Kramer, P. J., AND J. S. Boyer [eds.], 1997. Water relations of plants and soils. Academic Press, San Diego, California, USA.
Kytöviita, M.-M., AND A. L. Ruotsalainen. 2007. Mycorrhizal benefit in two low arctic herbs increases with increasing temperature. American Journal of Botany 94: 1309–1315.
Kytöviita, M.-M., M. Vestberg, AND J. Tuomi. 2003. A test of mutual aid in common mycorrhizal network: Established vegetation negates mycorrhizal benefit in seedlings. Ecology 84: 898–906.[CrossRef][Web of Science]
Leigh, A., AND A. B. Nicotra. 2003. Sexual dimorphism in reproductive allocation and water use efficiency in Maireana pyramidata (Chenopodiaceae), a dioecious, semi-arid shrub. Australian Journal of Botany 51: 509–514.[CrossRef][Web of Science]
Lloyd, D. G., AND C. J. Webb. 1977. Secondary sex characters in plants. Botanical Review 43: 177–216.[CrossRef]
Ludwig-Müller, J. 2000. Hormonal balance in plants during colonization by mycorrhizal fungi. In Y. Kapulnik, and D. D. Douds [eds.], Arbuscular mycorrhizas: Physiology and function, 263–285. Kluwer, Dordrecht, Netherlands.
Maxwell, K., AND G. N. Johnson. 2000. Chlorophyll fluorescence—A practical guide. Journal of Experimental Botany 51: 659–668.
Mosse, B., D. P. Shibley, AND F. Le Tacon. 1981. Ecology of mycorrhizas and mycorrhizal fungi. Advances in Microbial Ecology 5: 137–210.[Web of Science]
Obeso, J. R. 2002. The cost of reproduction in plants. New Phytologist 155: 321–348.[CrossRef][Web of Science]
Parádi, I., Z. Bratek, AND F. Láng. 2003. Influence of arbuscular mycorrhiza and phosphorus supply on polyamine content, growth and photosynthesis of Plantago lanceolata. Biologia Plantarum 46: 563–569.[CrossRef][Web of Science]
Pietikäinen, A., AND M.-M. Kytöviita. 2007. Defoliation changes mycorrhizal benefit and competitive interactions between seedlings and adult plants. Journal of Ecology 95: 639–647.[CrossRef][Web of Science]
Porcel, R., AND J. M. Ruiz-Lozano. 2004. Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. Journal of Experimental Botany 55: 1743–1750.
Pugnaire, F. I., L. Serrano, AND J. Pardos. 1993. Constraints by water stress on plant growth. In M. Pessarakli [ed.], Handbook of plant and crop stress, 271–283. Marcel Dekker, New York, New York, USA.
Ruiz-Lozano, J. M., AND R. Azcón. 1995. Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiologia Plantarum 95: 472–478.[CrossRef]
Ruiz-Lozano, J. M., R. Azcón, AND M. Gómez. 1996. Alleviation of salt stress by arbuscular mycorrhizal Glomus species in Lactuca sativa plants. Physiologia Plantarum 98: 767–772.[CrossRef]
Schmid, B., F. A. Bazzaz, AND J. Weiner. 1995. Size dependency of sexual reproduction and of clonal growth in two perennial plants. Canadian Journal of Botany 73: 1831–1837.[CrossRef]
Schüßler, A., D. Schwarzott, AND C. Walker. 2001. A new fungal phylum, the Glomeromycota: Phylogeny and evolution. Mycological Research 105: 1413–1421.[CrossRef][Web of Science]
Simon, L., J. Bousquet, R. C. Levesque, AND M. Lalonde. 1993. Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363: 67–69.[CrossRef][Web of Science]
Sleeman, J. D., S. A. Dudley, J. R. Pannell, AND S. C. H. Barrett. 2002. Responses of carbon acquisition traits to irradiance and light quality in Mercurialis annua (Euphorbiaceae): Evidence for weak integration of plastic responses. American Journal of Botany 89: 1388–1400.
Smith, S. E., AND D. J. Read [eds.], 1997. Mycorrhizal symbiosis. Academic Press, San Diego, California, USA.
Smith, S. E., AND F. A. Smith. 1990. Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytologist 114: 1–38.[CrossRef][Web of Science]
Streitwolf-Engel, R., T. Boller, A. Wiemken, AND I. R. Sanders. 1999. Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. Journal of Ecology 85: 181–191.
Streiwolf-Engel, R., M. G. A. van der Heijden, A. Wiemken, AND I. R. Sanders. 2001. The ecological significance of arbuscular mycorrhizal fungal effects on clonal reproduction in plants. Ecology 82: 2846–2859.[Web of Science]
Varga, S., M.-M. Kytöviita, AND P. Siikamäki. Sexual differences in response to simulated herbivory in the gynodioecious herb Geranium sylvaticum. Plant Ecology: in press.
Ward, J. K., T. E. Dawson, AND J. R. Ehleringer. 2002. Responses of Acer negundo genders to interannual differences in water availability determined from carbon isotope ratios of tree ring cellulose. Tree Physiology 22: 339–346.[Abstract]
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