Journal of Arid Land

Volume 4 Issue 1 Article 6

3-5-2012

Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral in Gurbantunggut Desert

Tao ZHANG 1 College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China;

ChangYan TIAN 2 Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China;

Yu SUN 3 Institute of Crop Tillage and Cultivation, Heilongjiang Academy of Agricultural Sciences, Harbin 150030, China;

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Recommended Citation ZHANG, Tao; TIAN, ChangYan; and SUN, Yu (2012) "Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert," Journal of Arid Land: Vol. 4 : Iss. 1 , Article 6. DOI: 10.3724/SP.J.1227.2012.00042 Available at: https://egijournals.researchcommons.org/journal-of-arid-land/vol4/iss1/6

This Research Article is brought to you for free and open access by Journals of EGI. It has been accepted for inclusion in Journal of Arid Land by an authorized editor of Journals of EGI. For more information, please contact [email protected]. Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert

Cover Page Footnote This work was funded by the National Natural Science Foundation of China (30770341) and the International Fund for Agricultural Development (the WATERCOPE project, I-R-1284).

This research article is available in Journal of Arid Land: https://egijournals.researchcommons.org/journal-of-arid- land/vol4/iss1/6 Journal of Arid Land 2012, 4(1): 43−51 doi: 10.3724/SP.J.1227.2012.00042 Science Press jal.xjegi.com; www.chinasciencejournal.com

Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert

Tao ZHANG1, ChangYan TIAN2, Yu SUN3, DengSha BAI4, Gu FENG1∗

1 College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China; 2 Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China; 3 Institute of Crop Tillage and Cultivation, Heilongjiang Academy of Agricultural Sciences, Harbin 150030, China; 4 Institute of Nuclear and Biotechnology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China

Abstract: Previous studies documented that most desert plants can be colonized by arbuscular mycorrhizal (AM) fungi, however, little is known about how the dynamics of AM fungi are related to ephemerals in desert ecosystems. The dynamics of AM fungi with desert ephemerals were examined to determine the effects of host life stages on the development of AM fungi. Mean colonization of ephemeral annual plants was 45% lower than that of ephemeral perennial plants. The colonizations were much higher in the early part of the growing season than in later parts, peaking at flowering times. The phenology of AM fungi in systems varied among different ephem- erals. The density of AM fungal spores increased with the development of ephemeral annual plants, reached its maximum at flowering times, and then plateaued about 20 days after the aboveground senescence. A significant positive correlation was found between AM fungi spore density and biomass of ephemeral annual plants. The life cycles of AM fungi associated with desert ephemerals were very short, being about 60–70 days. Soil temperature and water content had no direct influence on the development of AM fungal spores. We concluded that the devel- opment of AM fungi was in response to desert ephemeral phenology and life history strategy.

Keywords: arbuscular mycorrhizal fungi; Gurbantunggut Desert; ephemeral annual plants; ephemeral perennial plants; dynamics; phenology; mycorrhizal colonization; spore density

Arbuscular mycorrhizal (AM) fungi are important shifting phenology between C3 and C4 coexistence components of virtually all terrestrial ecosystems and species. It has been reported that divergent phenolo- are especially critical in improving plant nutrient and gies may facilitate the coexistence of AM fungi in a water uptake under arid conditions (Allen, 1989; 2007; North Carolina grassland (Pringle and Bever, 2002). 2011). In some extreme environments, some plants Other researchers reported that soil type, tillage, fertil- can not survive without AM fungi (Pennisi, 2004). AM ity, pH and rainfall can influence the AM fungi diver- fungi also enhance plant competitive ability and de- sity and density (Hayman, 1982; Douds et al., 1995; termine community structure and ecosystem stability Clark, 1997; Gaidashova et al., 2010; Oehl et al., (van der Heijden et al., 1998; O'Connor et al., 2002; 2010). However, how AM fungi respond to environ- Hart et al., 2003). Despite the key role of AM in plant mental stress and life-history strategies of host plant is growth and ecosystem stabilization, the strategy of not clear. AM fungi in terms of survival and development in AM fungi are considered to be critical for the sur- wildland ecosystems is not well understood. vival of plants in arid environments (Allen and Allen, A number of studies have demonstrated that host 1988; Berliner et al., 1989; Cui and Nobel, 1992; Titus plant species can affect the community composition et al., 2002). Early studies found that most ephemeral and diversity of AM fungi (Johnson et al., 2004; Received 2011-07-18; accepted 2011-10-27 Hausmann, 2009). Allen et al. (1984) first reported *Corresponding author: Gu FENG (E-mail: [email protected]) 44 JOURNAL OF ARID LAND Vol. 4 plants formed AM in Gurbantunggut Desert (Shi et al., Ephedra distachya, a small shrub, distributes in inter- 2006; Tian et al., 2006), and that mycorrhizae can im- dune lands. Annual herbs are distributed understory of prove growth, promote P uptake，advance the flow- shrubs. In spring, ephemeral plants are dominant in the ering times and increase seed production of ephemer- community. als Erodium oxyrrhynchum and Plantago minuta (Sun The ‘ephemerals’ we used here include both annual et al., 2008). AM fungi are obligate biotrophs whose and perennial species，which have a short growing development depends on mutualistic association with season. Most ephemeral annual plants complete host plant . AM fungi spores complete a life span growth and reproduction in about 2 months from early (from spore germination to new mature sporulation) in spring (late March) to early summer (late May). As to about 100–120 days in pot culture (http:// invam.caf. ephemeral perennial plants, the aboveground parts wvu). But life spans of ephemeral plants are only usually senesce at the end of the growing season while about 2 months in Gurbantunggut Desert (Wang, the belowground structures (, corms, or tubers) 1993), and whether AM fungal spores can complete enter a period of dormancy until the next sprouting. their life cycles in such a short period of time is not The ephemerals are an important part of plant com- clear. Furthermore, the annual precipitation in Gur- munity in Gurbantunggut Desert. In early spring, the bantunggut Desert is 70–150 mm, while annual ephemerals can form synusia, and the mean cover of evaporation is more than 2,000 mm. The effects of ephemerals can reach 40.2% in May, with a mean these extreme environmental factors on development plant height of 10–20 cm (Zhang and Chen, 2002; of AM fungi are not well understood. A better under- Wang et al., 2003). Ephemeral plants play a key role standing of the growth and development of AM fungi in sand dune stabilization (Wang et al., 2003). Besides, and plants in field would help us to understand the the ephemerals are important pasture and supply much adaptation strategy of AM fungi to environmental fodder for livestock in early spring (Zhang, 2002). stress. 1.2 Collection of soil and plant samples We hypothesized that the development and phenol- ogy of ephemerals can determine the growth of AM Four important ephemeral plant species were investi- fungi. Specifically, AM fungi spores can complete gated in our experiment, including two ephemeral an- their life cycles for long term coevolution with nual plants Erodium oxyrrhynchum and Trigonella ephemeral plants. arcuata, two ephemeral perennial plants Gagea saccu- lifera and Ixiolirion tataricum. To test whether AM 1 Materials and methods fungi can transfer host from ephemeral annual plants to perennial plants after ephemerals finish their lives, 1.1 Study area one Artemisia songarica which grew Gurbantunggut Desert, a fixed and semi-fixed desert, nearby E. oxyrrhynchum and T. arcuata was selected. is located at the hinterland of the Junggar Basin The topsoil of ca. 1–2 cm was removed, and soil and (34°09′–49°08′N, 73°25′–96°24′E) in Xinjiang, north- plant samples were collected. Care was taken during western China. The annual accumulated temperature the collection of individual plants so that roots could varies between 3,000ºC and 3,500ºC. And the annual be positively identified as belonging to a particular precipitation is 70–150 mm with a mean of 143 mm, plant. The entire plants were dug out by trowel to en- which mainly distributes in spring and autumn. During sure that the roots remained connected to the shoots winter, the desert is usually covered by snow in more after sample collection. The samples were taken to the than 20 cm thickness. The annual evaporation in this laboratory for determination of AM root colonization. region is more than 2,000 mm (Wang et al., 2003). Soil samples (ca. 1,000 g) associated with the plants Soil moisture content in the topsoil (30 cm) is 2% to removed were collected. The soil samples were 5% in April and only 0.8% to 1.2% in May (Wang et air-dried before extraction, counting and identification al., 2004). Haloxylon persicum which grows on dunes of AM fungal spores. Soil water content, temperature is a constitutive species in the desert community. and precipitation were recorded (Table 1). No.1 Tao ZHANG et al.: Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert 45

1.3 Assessment of AM colonization density was counted (Shi et al., 2006). Fresh roots (ca. 0.2 g) were washed free of soil and 1.5 Observation of plant grow status cleared in 10% (w/v) KOH at 90°C in a water bath for Phenological status of these plants was recorded every 20–30 min. The root subsamples were cooled, washed, week. The total numbers of were counted every and cut into 0.5 to 1.0-cm-long segments and stained week. Shoots and roots were separated after harvesting with trypan blue according to the methods reviewed and oven dried (70°C for 48 h) prior to recording dry by Brundrett (2009). The mycorrhizal colonization in weights. root system was estimated using the method of Trou- 1.6 Statistical analysis velot et al. (1986). Presence or absence of mycorrhiza (F%), intensity of mycorrhizal colonization (m%), All data were analyzed using SPSS software version arbuscule abundance (A%) and vesicle abundance 16.0. Data for percentage of root length colonized by (V%) in the root system were recorded. the AM fungi were arcsin-transformed and spore den- sity counts were square root-transformed for statistical Table 1 Environmental factors in experimental site at different times analysis so as not to violate ANOVA assumptions. Atmosphere Date Soil temperature Relative Soil water content temperature (Day/Month) (ºC, 0–20 cm) humidity (%) (%, 0–20 cm) (ºC) 2 Results 23/3 5.40 6.19 74.00 5.23 30/3 13.89 12.47 33.00 4.11 2.1 Plant development 5/4 13.65 14.17 35.63 2.75 By observing the growth status of these ephemeral 10/4 15.65 16.55 44.92 4.50 plants, we found that the numbers of these plants 12/4 17.07 17.87 40.21 1.63 18/4 10.23 13.48 75.54 3.61 increased gradually at early times (Fig. 1), and then 19/4 9.74 12.36 71.54 0.68 decreased when the plant entered flowering times and 24/4 16.59 17.71 55.04 2.17 reproductive stage. But the aboveground biomass of 26/4 18.39 19.17 30.29 0.32 plants always increased from germination to harvest 2/5 18.13 20.24 42.33 4.79 time. Phenological phases of these plants were differ- 9/5 13.21 17.20 35.96 4.39 ent. The florescence of ephemeral perennial plants G. 15/5 21.60 24.57 37.08 2.82 sacculifera and I. tataricum was 30 days earlier than 16/5 20.00 23.24 37.63 2.82 that of E. oxyrrhynchum and T. arcuata. I. tataricum 22/5 17.66 21.16 55.46 1.13 1/6 23.35 27.31 39.38 1.06 and G. sacculifera entered flowering times at March 30 and April 12, respectively, and E. oxyrrhynchum 1.4 Extraction and counting of AM fungal spores and T. arcuata entered flowering at May 9 (Table 2). Spores or sporocarps were extracted from 20-ml 2.2 Mycorrhizal colonization air-dried subsamples of each soil sample in triplicate All plants observed were colonized by AM fungi but by wet sieving followed by flotation–centrifugation in the degree of colonization varied among plant species 50% sucrose. The finest sieve used was 53 μm in ap- (Fig. 2). The percentage of root length colonized var- erture. The spores were collected on a grid patterned ied from 7% to 85% and the mean colonization was (4 mm×4 mm) filter paper, washed three times with 42%. The colonization of E. oxyrrhynchum was much distilled water to spread them evenly over the entire lower than that of other ephemerals and the average grid, and counted using a dissecting microscope at ×30 colonization was only 18%. The degree of coloniza- magnification. A sporocarp was counted as one spore. tion in I. tataricum was highest which was up to 57%. The number of spores is expressed as the mean ± Comparing the degree of colonization from germina- standard error of three replicates. For observation and tion to harvest time, we found the mycorrhizal coloni- identification of spore characters, spores were mounted zation all increased at early times and reached highest on glass slides in polyvinyl alcohol-lactoglycerol at flowering times, and then decreased gradually. The (PVLG) and PVLG + Melzer’s reagent and then spore abundance of arbuscule and vesicle varied in the root 46 JOURNAL OF ARID LAND Vol. 4

Fig. 1 The dynamics of leaf number and shoot biomass of ephemeral plants. (a) Gagea sacculifera, (b) Ixiolirion tataricum, (c) Erodium oxyrrhynchum, (d) Trigonella arcuata. Different lowercase letters on the line indicate significant differences at P<0.05 among different times. Different capital letters marked on the gray bars indicate significant differences of shoot biomass among different times at P<0.05.

Table 2 Phenological dates of the four ephemerals germinated arcuata. The average spore densities of AM fungi in in spring the rhizosphere soil of E. oxyrrhynchum and T. ar- Seedling Flores- Fructes- Species Bud stage Withered stage cence cence cuata were 27 and 26, respectively (Fig. 3c, 3d). As to (Day/Month) AM fungi associated with the ephemeral annual plants G. sacculifera 19/3 27/3 29/3 12/4 9/5 E. oxyrrhynchum and T. arcuata, the spore density I. tataricum 23/3 12/4 19/4 26/4 22/5 increased gradually at vegetative stages and maxima E. oxyrrhynchum 3/4 24/4 9/5 17/5 27/5 appeared at flowering times on May 9, and then de- T. arcuata 3/4 22/4 9/5 22/5 31/5 clined. But the spore density of AM fungi in the soil associated with roots of I. tataricum remained a high systems of these ephemerals. Vesicle abundances in level and, in some cases, increased (up to 140) after the root systems of I. tataricum and E. oxyrrhynchum the aboveground parts completed their life cycles. The were much lower than that of G. sacculifera and T. spore density of AM fungi associated with A. songa- arcuata. Arbuscule abundance in the root systems of I. rica did not decline after the plant died, but increased tataricum and E. oxyrrhynchum were much higher (Fig. 3e). Among ephemeral annual plants and than that of G. sacculifera. ephemeral perennial plants, no significant correlations 2.3 Dynamics of AM fungi spore density were found between their soil water content, tempera- ture and AM fungi spore density, whereas significant The spore density varied among different species from differences were observed between their shoot bio- 19 to 203 per 20 g soil, with a mean of 86. Significant mass and atmosphere temperature and soil temperature differences were observed among soils collected from (Table 3). different plant species. The mean spore densities of AM fungi in soil, associated with ephemeral perennial 3 Discussion plants I. tataricum (up to 147) and G. sacculifera (up to 149) (Fig. 3a and 3b) were much higher than those Ephemeral plants are important floral elements widely with ephemeral annual plants E. oxyrrhynchum and T. distributed in all arid regions. These ephemerals play a No.1 Tao ZHANG et al.: Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert 47 key role in reducing the degree of desertification and prove water and nutrition uptake (van der Heijden et stabilizing soils as most ephemeral plants can grow al., 2006; Allen, 2007; 2011) and play a key role in well in very arid, infertile, and windy environments. plant survival and community stability of vegetation in Previous studies have focused on the distribution, bio- natural ecosystems (Hartnett and Wilson, 1999; van logical characteristics, and ecological functions of der Heijden, 2004). Although AM fungi are important spring ephemerals (Mao and Zhang, 1994; Zhang and to plants, they are obligate biotrophs, whose growth Chen, 2002; Wang et al., 2003; Qian et al., 2007). depends on host plant for the supply of carbohydrate. Many studies found desert herbaceous plants can be The development of AM fungi is controlled by host colonized by AM fungi (O'Connor et al., 2001; Shi et plant species (Johnson et al., 1992; Trepanier et al., al., 2006). In the present study, all of these ephemeral 2005; Heinemeyer et al., 2006). Some results reported plants were colonized by AM fungi. Hypha, arbuscule that the colonization of ephemeral annual plants was and vesicle were all observed in the root systems of lower than that of co-occurring perennials (Collier et ephemeral plants. The presence of vesicles and arbus- al., 2003; Shi et al., 2006). Allen (2001) reported that cules in roots of different ephemerals was different, mycorrhizal infection is related to the production of which was consistent with former results reported by new root tips, the penetration of such new roots, the Allen et al. (1984). lifespan of the fungus within the root, and the lifespan The survival and reproduction of organisms is a of the root itself. Rillig et al. (1998) reported that in- critical research topic. A better understanding of the fection intensity of mycorrhizae may also change in organism’s reproduction and succession pattern is es- response to many other treatments and environmental sential to biodiversity conservation. AM fungi im- variables. In our current results, the mycorrhizal colo-

Fig. 2 Mean colonization in root system of ephemeral plants at different times. (a) G. sacculifera, (b) I. tataricum, (c) E. oxyrrhynchum, (d) T. arcuata. F% indicates frequency of mycorrhizae in root system; A% arbuscule abundance in root system; V%, vesicle abundance in root system; and m%, intensity of mycorrhizal colonization in root system.

48 JOURNAL OF ARID LAND Vol. 4

nization and spore density associated with I. tataricum and G. sacculifera were much higher than these with E. oxyrrhynchum and T. arcuata. This might be re- lated to the characteristic of ephemeral plant roots. Most ephemeral perennial plants have fibrous root systems which are very thin and can be colonized eas- ily by AM fungi, while ephemeral annual plants have taproot systems with less effective colonization by AM fungi. Many studies found that host plant phenology can affect mycorrhizal colonization, but Rasmussen and Whigham (2002) found that the phenology of myco- trophic roots and patterns of mycorrhizal infection were not related to the leafy season. Our results showed that the mycorrhizal colonization, especially that with ephemeral annual plants, was influenced by phenological phase of ephemeral annual plants. The degrees of colonization were consistent with plant phenology. The maximum frequency of mycorrhizal colonization and infection occurred at flowering peri- ods, and then declined (Fig. 2c and 2d). These sug- gested that the host plant could supply much carbohy- drate to the AM fungi and improve the growth of AM fungi at flowering times. These results were consistent with former studies that indicated more carbohydrate is allocated to the symbiont during the reproductive stages of plants (Grigera et al., 2007). As to ephemeral perennial plants, the infection intensity and vesicle abundance did not reach highest at flowering periods and appeared maxima after the aboveground parts finished their life cycles (Fig. 2a, 2b). This result might indicate that the belowground parts of perennial plants can also supply carbohydrate to benefit the growth of AM fungi in root systems after above- ground parts complete their lives. It is well known that the development of AM fungi needs adequate time for energy accumulation for spore production. Many studies reported that it takes about 100–120 days from the spore germination to new mature spores production (Smith and Read, 2008). But here, the life span of ephemerals was only about 2 months in Gurbantunggut Desert (Wang, 1993). Our Fig. 3 Dynamics of spore density in rhizosphere soil of ephem- results found that the AM fungi spore density in- eral plants and perennial plants. (a) G. sacculifera, (b) I. tataricum creased with the growth of annual ephemeral plants (c) E. oxyrrhynchum, (d) T. arcuata, (e) A. songarica. Different lowercase letters marked on the fold-line indicate significant and stopped increasing after the annual ephemeral differences of colonization among different times at P<0.05. plants finished their lives, which might show that a

No.1 Tao ZHANG et al.: Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert 49

Table 3 Correlation between soil factors and AM fungi spore density and shoot biomass of ephemerals Atmosphere Soil Soil AM fungi AM fungi Shoot biomass Shoot biomass Correlations temperature temperature moisture spore density in spore density of ephemeral of ephemeral Atmosphere temperature 1 Soil temperature 0.947** 1 * Soil moisture −0.415* −0.396 1 AM fungi spore density in 0.203 0.296 0.071 1 ephemeral perennial plants AM fungi spore density in 0.048 0.162 0.267 0.602 1 ephemeral annual plants Shoot biomass of ephemeral 0.262 0.383 −0.265 0.071 0.543 1 perennial plants Shoot biomass of Ephemeral ** −0.509* 0.650 −0.375 −0.042 0.317 0.372 1 annual plants

Note: *and** indicate that correlations are significant at the 0.05 and 0.01 level, respectively. life cycle of AM fungi spore has completed. Whereas, have found that soil water and temperature can affect when the aboveground parts of perennial plants died, the mycorrhizae colonization, mycorrhizal production, the belowground parts were still alive or entered dor- and AM fungi community composition (Feil et al., mancy period. At this point the mycelium network can 1988; Auge, 2001; Lekberg and Koide, 2008; Yamato, transfer nutrients from dead roots to living plants 2009). We did not find a significant correlation be- (Jakobsen, 2004; Mikkelsen et al., 2008). We indeed tween soil temperature and water content and AM found after the aboveground parts died the AM fungi fungi spores density in rhizosphere soil (Table 3). spore density maintained a high level. The results Likely soil factors have indirect effects on AM fungi suggest that the living root system can continue to by influencing the growth of host plant. supply carbohydrate to AM fungi. Although there are 4 Conclusion many ephemeral annual plants in Gurbantunggut De- sert, some perennial plants and herbs are present. Be- We conclude that AM fungi have adapted to both en- sides, although there were no significant differences in vironmental factors and plant species in arid lands. AM fungi diversity and species richness during grow- Plant species composition and phenology are espe- ing season in Gurbantunggut Desert (Shi, 2006), the cially critical in regulating mycorrhizal colonization shifts of AM fungi species might be present. But the and the phenology of AM fungi in root systems. Soil possibility of these shifts can not be determined in our factors might affect AM fungi by influencing the present study; further work is then needed to identify growth of host ephemeral plants. the AM fungi community composition in root system and rhizosphere soil by using molecular methods. Acknowledgements AM fungi can improve soil condition which con- This work was funded by the National Natural Science Founda- tributes to plant growth. Soil factors also influence tion of China (30770341) and the International Fund for Agri- AM fungi diversity and development. Many studies cultural Development (the WATERCOPE project, I-R-1284).

References

Allen E B, Allen M F. 1988. Facilitation of succession by the processes and practices. Arid Land Research and Management, 3(2): nonmycotrophic colonizer Salsola-kali (Chenopodiaceae) on a harsh 229–241. site-effects of mycorrhizal fungi. American Journal of Botany, 75(2): Allen M F. 2001. Modeling arbuscular mycorrhizal infection: is % 257–266. infection an appropriate variable? Mycorrhiza, 10: 255-258. Allen M F, Allen E B, Stahl P D. 1984. Differential niche response of Allen M F. 2007. Mycorrhizal fungi: highways for water and nutrients in Bouteloua gracilis and Pascopyrum smithii to VA mycorrhizae. arid soils. Vadose Zone Journal, 6(2): 291–297. Bulletin of the Torrey Botanical Club, 111(3): 361–365. Allen M F. 2011. Linking water and nutrients through the vadose zone: a Allen M F. 1989. Mycorrhizae and rehabilitation of disturbed arid soils: fungal interface between the soil and plant systems. Journal of Arid 50 JOURNAL OF ARID LAND Vol. 4

Land, 3(3): 155–163. Jakobsen I. 2004. Hyphal fusion to plant species connections–giant Auge R M. 2001. Water relations, drought and vesicular-arbuscular mycelia and community nutrient flow. New Phytologist, 164(1): 4–7. mycorrhizal symbiosis. Mycorrhiza, 11: 3–42. Johnson D, Vandenkoornhuyse P J, Leake J R, et al. 2004. Plant Berliner R, Mitchell D T, Allsopp N. 1989. The vesicular-arbuscular communities affect arbuscular mycorrhizal fungal diversity and mycorrhizal infectivity of sandy soils in the south-western Cape, community composition in grassland microcosms. New Phytologist, South Africa. South African Journal of Botany, 55(1): 310–313. 161(2): 503–515. Brundrett M C. 2009. Mycorrhizal associations and other means of Johnson N C, Tilman D, Wedin D. 1992. Plant and soil controls on nutrition of vascular plants: understanding the global diversity of mycorrhizal fungal communities. Ecology, 73(6): 2034-2042. host plants by resolving conflicting information and developing Lekberg Y, Koide R T. 2008. Effect of soil moisture and temperature reliable means of diagnosis. Plant and Soil, 320(1–2): 37–77. during fallow on survival of contrasting isolates of arbuscular Clark R B. 1997. Arbuscular mycorrhizal adaptation, spore germination, mycorrhizal fungi. Botany-Botanique, 86(10): 1117–1124. root colonization, and host plant growth and mineral acquisition at Mao Z, Zhang D. 1994. The conspectus of ephemeral flora in northern low pH. Plant and Soil, 192(1): 15–22. Xinjiang. Arid Zone Research, 11(3): 1–26. Collier S C, Yarnes C T, Herman R P. 2003. Mycorrhizal dependency of Mikkelsen B L, Rosendahl S, Jakobsen I. 2008. Underground resource Chihuahuan Desert plants is influenced by life history strategy and allocation between individual networks of mycorrhizal fungi. New root morphology. Journal of Arid Environments, 55(2): 223–229. Phytologist, 180(4): 890–898. Cui M, Nobel P S. 1992. Nutrient status, water-uptake and gas-exchange O'Connor P J, Smith S E, Smith F A. 2001. Arbuscular mycorrhizal for three desert succulents infected with mycorrhizal fungi. New associations in the southern Simpson Desert. Australian Journal of Phytologist, 122(4): 643–649. Botany, 49(4): 493–499. Douds D D, Galvez L, Janke R R, et al. 1995. Effect of tillage and O'Connor P J, Smith S E, Smith E A. 2002. Arbuscular mycorrhizas farming system upon populations and distribution of vesicular- influence plant diversity and community structure in a semiarid arbuscular mycorrhizal fungi. Agriculture Ecosystems & Enviro- herbland. New Phytologist, 154(1): 209–218. nment, 52(2–3): 111–118. Oehl F, Laczko E, Bogenrieder A, Stahr K, et al. 2010. Soil type and land Feil W, Kottke I, Oberwinkler F. 1988. The effect of drought on use intensity determine the composition of arbuscular mycorrhizal mycorrhizal production and very fine root-system development of fungal communities. Soil Biology & Biochemistry, 42(5): 724–738 Norway spruce under natural and experimental conditions. Plant and Pennisi. 2004. The secret life of fungi. Science, 304: 1620–1622. Soil, 108(3): 221–231. Pringle A, Bever J D. 2002. Divergent phenologies may facilitate the Gaidashova S V, Van Asten P J A, Jefwa J M, et al. 2010. Arbuscular coexistence of arbuscular mycorrhizal fungi in a north carolina mycorrhizal fungi in the East African Highland banana cropping grassland. American Journal of Botany, 89(9): 1439–1446. systems as related to edapho-climatic conditions and management Qian Y B, Wu Z N, Zhang L Y, et al. 2007. Spatial patterns of ephemeral practices: case study of Rwanda. Fungal Ecology, 3(7): 225–233. plants in Gurbantunggut Desert. Chinese Science Bulletin, 52(22): Grigera M S, Drijber R A, Wienhold B J. 2007. Increased abundance of 3118–3127. arbuscular mycorrhizal fungi in soil coincides with the reproductive Rasmussen H N, Whigham D F. 2002. Phenology of roots and stages of maize. Soil Biology & Biochemistry, 39(8): 1401–1409. mycorrhiza in orchid species differing in phototrophic strategy. New Hart M M, Reader R J, Klironomos J N. 2003. Plant coexistence Phytologist, 154(3): 797–807. mediated by arbuscular mycorrhizal fungi. Trends in Ecology & Rillig M C, Allen M F, Klironomos J N, et al. 1998. Arbuscular Evolution, 18(4): 418–423. mycorrhizal percent root infection and infection intensity of Bromus

Hartnett D C, Wilson G W T. 1999. Mycorrhizae influence plant hordeaceus grown in elevated atmospheric CO2. Mycologia, 90(2): community structure and diversity in tallgrass prairie. Ecology, 80(4): 199–205. 1187–1195. Shi Z Y. 2006. Biodiversity and ecological function of arbuscular Hausmann N T, Hawkes C V. 2009. Plant neighborhood control of mycorrhizal fungi associated with spring ephemerals in the north of arbuscular mycorrhizal community composition. New Phytologist, Xinjiang. Ph.D dissertation, China Agricultural University, Beijing, 39. 183(4): 1188–1200. Shi Z Y, Feng G, Christie P, et al. 2006. Arbuscular mycorrhizal status of Hayman D S. 1982. Influence of soils and fertility on activity and spring ephemerals in the desert ecosystem of Junggar Basin, China. survival of vesicular-arbuscular mycorrhizal fungi. Phytopathology, Mycorrhiza, 16(4): 269–275. 72(8): 1119–1125. Smith S E, Read D J. 2008. Mycorrhizal Symbiosis 3rd ed: Boston: Heinemeyer A, Ineson P, Ostle N, et al. 2006. Respiration of the external Academic Press. mycelium in the arbuscular mycorrhizal symbiosis shows strong Sun Y, Li X L, Feng G. 2008. Effect of arbuscular mycorrhizal dependence on recent photosynthates and acclimation to temperature. colonization on ecological functional traits of ephemerals in the New Phytologist, 171(1): 159–170. Gurbantunggut Desert. Symbiosis, 46(3): 121–127. No.1 Tao ZHANG et al.: Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert 51

Tian C Y, Shi Z Y, Chen Z C, et al. 2006. Arbuscular mycorrhizal mycorrhizal contribution to plant productivity, plant nutrition and associations in the Gurbantunggut Desert. Chinese Science Bulletin, soil structure in experimental grassland. New Phytologist, 172(4): 51(Suppl.): 140–146. 739–752. Titus J H, Titus P J, Nowak R S, et al. 2002. Arbuscular mycorrhizae of Wang X Q, Jiang J, Lei J Q, et al. 2003. The distribution of ephemeral Mojave Desert plants. Western North American Naturalist, 62(3): vegetation on the longitudinal dune surface and its stabilization 327–334. significance in the Gurbantunggut Desert. Acta Geographica Sinica, Trepanier M, Becard G, Moutoglis P, et al. 2005. Dependence of 58(4): 598–605. arbuscular-mycorrhizal fungi on their plant host for palmitic acid Wang X Q, Jiang J, Lei J Q, et al. 2004. Relationship between spring synthesis. Applied and Environmental Microbiology, 71(9): ephemeral plants distribution and soil moisture on longitudinal dune 5341–5347. surface in Gurbantunggut Desert. Chinese Journal of Applied Trouvelot A, Kough J L, Gianinazzi-Pearson V. 1986. Mesure du taux de Ecology, 15: 556–560. mycorhization VA d’un systeme radiculaire. Recherchede methodes Wang Y. 1993. Phenological observation of the early spring ephemeral and d’estimation ayant une signification functionnelle. In: Gian- ephemeriod plant in Xinjiang. Arid Zone Research, 10(3): 34–39. inazzi-Pearson V, Gianinazzi S. Physiological and Genetic Aspects Yamato M, Ikeda S, Iwase K. 2009. Community of arbuscular of Mycorrhizae. Paris: INRA Press, 217–221. mycorrhizal fungi in drought-resistant plants, moringa spp., in van der Heijden M G A, Klironomos J N, Ursic M, et al. 1998. semiarid regions in Madagascar and Uganda. Mycoscience, 50(2): Mycorrhizal fungal diversity determines plant biodiversity, ecosy- 100–105. stem variability and productivity. Nature, 396(6706): 69–72. Zhang L. 2002. Ephemeral plants in Xinjiang(iii): significance of van der Heijden M G A. 2004. Arbuscular mycorrhizal fungi as support community and resource. Journal of Plant, 3: 4–5. systems for seedling establishment in grassland. Ecology Letters, Zhang L, Chen C. 2002. On the general characteristics of plant diversity 7(4): 293–303. of Gurbantunggut sandy desert. Acta Ecologica Sinica, 22: 1923– van der Heijden M G A, Streitwolf-Engel R, Riedl R, et al. 2006. The 1932.