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Biodiversity of arbuscular mycorrhizal fungi in China: a review.

Introduction

Arbuscular mycorrhizal (AM) fungi are extremely common symbioses in terrestrial ecosystems, associating with about 80% of plant families worldwide. They are recognized as an important, widespread component of most terrestrial ecosystems, benefiting plant establishment by enhancing plant nutrient acquisition, improving soil quality, and increasing resistance to environmental stresses[53], and also playing an important role in plant biodiversity, ecosystem variability and productivity. According to the latest taxonomy, AM fungi belong to the Glomeromycota phylum, including 4 families and 12 genera. To date, although only fewer than 200 species of AM fungi have been described [44], numerous studies on AM fungal diversity in different ecosystems worldwide have shown that AM fungi distribute globally [57].

China is situated in the eastern part of Asia, with a coastline of 18, 000 km and a total land area of 9.6 million km. Its territory extends over 50[degrees]of 2 latitude from north to south, embracing the equatorial belt, the tropics, the subtropics, the moderate temperate zone, and the cold temperate zone. From east to west, China extends over 62[degrees]of longitude with land covered by forests, grasslands, deserts, plains, hills, and mountains. China has a marked continental monsoonal climate characterized by great variety. Northerly winds prevail in winter, while southerly winds reign in summer. China has 94.97 million ha of cultivated land, 400 million ha of grasslands, and 133.7 million ha of forests. The diversity of plant species in China is extraordinary, about 30,000 or one eighth of the world total.

Studies on AM fungal biodiversity in China began in the 1980's. In 1984, Tang and Zang reported the first new AM fungus Glomus citricolum [54]. Thereafter, more and more survey work and classification of AM fungi within China were carried out. Over the past 20 years, more than 100 papers on AM fungal biodiversity have been published. This review aims to summarize the advances in AM fungal biodiversity, including species diversity, habitat diversity and host diversity within China.

AM fungal species diversity

A total of 122 AM fungi species within 11 genera have been reported in the rhizosphere of different plants in various environments of China, including 12 new species (Table 1). The most common and widely distributed genera is Glomus (64 species), and then Acaulospora (26 species) and Scutellospora (16 species).

AM fungal habitat diversity

It has been shown that, besides farmland s [14,42,83], fruit lands [28,34], vegetable lands [65], forest lands [11,24], grasslands [3,5,61,76],

AM fungi occurred widely in tropical rain forests [49,50,98,99], tropical virgin forests [19], tropical secondary forest [11], artificial forests [20,81], natural secondary forests [8], greenhouse vegetable land [35] , natural reserves [45,72], altiplano grassland [5].

AM fungi occurred in all kinds of landforms all over the China, such as mountains [52,83], plateaus [5,40,41], hills [13], plains [13], islands [35], basin [65]. However, AM fungal biodiversities differ from different soil climatic zones, varying with various environmental factors [87,88].

In recent years, AM fungal diversities in fragile ecosystems and polluted environments received more attraction, such as deserts [2,27,56], saline-alkaline soils [48,55,59,82], degraded grasslands [61], eroded soils [40,41], sewage irrigated soils [18], petroleum polluted soils [26], coal mine heaps [61], heavy metal polluted soils [32], mining disturbed soils [90], mine tailings [6], abandoned mine lands [32].

AM fungal host diversity

AM fungi are ubiquitous in natural ecosystems, associating with about 80% of terrestrial plant species worldwide [53]. Most plant phyla, including bryophyte, pteridophyte, gymnosperm and angiosperm, are all able to form mycorrhizae with AM fungi. In China, crops, wild plants, tropical plants, alpine plants, halophytes, xerophyte, hydrophyte, geophyte, parasitic plants, are all found to be mycorrhizal. Only a few families, such as Cyperaceae, Brassicaceae, Caryophyllaceae, Juncaceae, Chenopodiaceae and Amaranthaceae, are assumed never to form mycorrhizal associations or to do so rarely [23]. In recent years, mycorrhizae on plants of these families have been observed, such as Cyperaceae [38], Amaranthaceae [1,7,80], Caryophyllaceae [7], and Chenopodiaceae [36,59].

China has about 30,000 plant species, accounting for about one eighth of the world total. Chinese researchers have done a considerable amount of work on the mycorrhizal status of plant species in terrestrial ecosystems and have examined a total of nearly 800 plant species belonging to 150 families. These plants include food crops, economic crops, vegetables, fruits, ornamental plants, Chinese medical plants, wild weeds, trees, etc (Table 2). Interestingly, even some forest trees, such as Eucalyptus and Dipterocarpaceae, usually considered to be typically ectomycorrhizal, have been recently found to have AM colonization [20,49,50].

Future study

Although considerable research efforts have been carried out on AM fungal biodiversity, these studies are unsystematic and not enough and most are limited on regional scale or on specific host plants. China has a large area of land and diverse ecosystems with various environmental factors, thus AM fungal germplasms may be abundant. Unfortunately, so far, only 8 new AM fungal species have been reported in China. Obviously, maybe a large number of unknown AM fungal species need to be explored, which must be firstly strenghthened in the future.

Secondly, AM biodiversity in special habitats especially in extreme environments needs more attention. These AM species may have specific genes that allow them to resitant extreme environmental conditions, which may be of great value in future agriculture or environetal remediation such as bioremediation with mycorrhizae. The relative genes need to be cloned and identified.

Furthermore, AM fungal genetic diversity needs to be studied and effective molecular tools need to be developed. Most above-mentioned studied by Chinese researchers on the taxonomy and identification of AM fungi still are based on the morphology of their spores, but the morphological characters of spores are sometimes variable, which may lead to incorrect results. Effective molecular tools have recently been developed to identify AM fungi and a new monophyletic phylum, the Glomeromycota, for AM fungi has been established based on SSU rRNA gene sequences [47,58]. It is therefore important and urgent for Chinese scientists to manipulate these molecular tools in future studies on the biodiversity and ecology of AM fungi in China.

Acknowledgments

This work is supported by Talent Foundation of Henan University of Science and Technology (05-008) and the Scientific Research Foundation of Henan University of Science and Technology (2006ZY035).

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[100.]Zhou, C.Q., G.L. Wu and S.B. Huang, 1992. The Colonization of Vesicular-arbuscular Mycorrhiza on Fruit and Its Influencing Factors. China Fruit, 1: 22-24. (in Chinese)

Fa Yuan Wang, and Zhao Yong Shi

Agricultural College, Henan University of Science and Technology, Luoyang, Henan Province, 471003, P.R. China

Corresponding Author

Fa Yuan Wang, Agricultural College, Henan University of Science and Technology, Luoyang, Henan Province, 471003, P.R. China. E-mail: wfy1975@163.com; wfyuan1975@sohu.com
Table 1: AM fungi reported in China

AM fungus References

Acaulospora bireticulata Rothwell
 & Trappe Peng et al, 1990 [42]
Acaulospora capsicula Blaszk. Cai et al., 2007 [4]
Acaulospora cavernata Blaszk. Zhang et al., 2007 [94]
Acaulospora delicata Walker,
 Pfeiffer & Bloss Zhao et al., 2006 [95]
Acaulospora denticulata
 Sieverding & Toro Wu et al., 1995 [75]
Acaulospora dilatata Morton Zhang et al., 1998 [87]
Acaulospora elegans Trappe & Gerd. Hu, 1988 [24]
Acaulospora excavata Ingleby
 & Walker Zhang et al., 2001 [90]
Acaulospora foveata Trappe & Janos Wu and Chen, 1986 [69]
Acaulospora gedanensis Blaszk. Gao et al., 2006 [16]
Acaulospora koskei Blaszk. Zhang and Guo, 2005 [93]
Acaulospora lacunosa Morton Gai and Liu, 2000 [13]
Acaulospora laevis Gerd. & Trappe Wu and Chen,1986 [69]
Acaulospora longula Spain & Schenck Zhang and Wang, 1991 [83]
Acaulospora mellea Spain & Schenck Hu, 1988 [24]
Acaulospora morrowae Spain & Schenck Hu, 1988 [24]
Acaulospora myriocarpa Spain
 & Schenck Hu, 1988 [24]
Acaulospora nicolsonii Walker,
 Reed & Sanders Zhang et al., 2007 [94]
Acaulospora polonica Blaszk. Zhang et al., 2001 [90]
Acaulospora rehmii Sieverd. & Toro Shi et al., 2003 [49]
Acaulospora rugosa Morton Zhang et al., 1998 [87]
Acaulospora scrobiculata Trappe Wu and Chen, 1986 [69]
Acaulospora spinosa Walker & Trappe Hu, 1988 [24]
Acaulospora taiwania Hu * Hu, 1988 [24]
Acaulospora tuberculata Janos &
 Trappe Zhao and Du, 1997 [96]
Acaulospora undulata Sieverd. Zhang et al., 2001 [90]
Ambispora leptoticha Walker,
 Vestberg & Schuessler Hu, 1988 [24]
Archaeospora trappei (Ames & Linderman)
 Morton & Redecker emend Spain Wu and Chen, 1986 [69]
Diversispora spurca (Pfeiff., Walker
 & Bloss) Walker & Schussler Zhang et al., 2007 [94]
Diversispora versiforme (Karst) Berch Zhang and W ang, 1991 [83]
Entrophospora baltica Blaszk., Madej
 & Tadych Cai et al., 2007 [4]
Entrophospora infrequens (Hall) Ames
 & Schneid. Wu and Chen, 1986 [69]
Gigaspora decipiens Hall & Abbott Liu et al., 2002 [36]
Gigaspora gigantea (N icol. & Gerd.)
 Gerd. & Trappe Wu and Chen, 1986 [69]
Gigaspora margarita Becker & Hall Peng et al., 1990 [42]
Gigaspora ramisporophora Spain,
 Sieverd. & Schenck Cai et al., 2007 [4]
Glomus aggregatum Schenck & Smith Hu, 1988 [24]
Glomus albidum Walker & Rhodes Wang and Hu, 1989 [63]
Glomus ambisporum Smith & Schenck Wang and Hu, 1989 [63]
Glomus australe (Berk.) Berch Zhang et al., 2003 [92]
Glomus badium Oehl, Redecker
 & Sieverd. Zhang et al., 2007 [94]
Glomus brohultii Herrera, Ferrer
 & Sieverd. Bao et al., 2007 [3]
Glomus caledonium (Nicolson & Gerd.)
 Trappe & Gerd. Wu and Chen, 1986 [69]
Glomus canadense (Thaxter) Trappe
 & Gerd. Shi et al., 2004 [51]
Glomus citricolum Tang & Zang * Tang and Zang, 1984 [54]
Glomus claroideum Schenck & Sm. Peng et al., 1990 [42]
 emend Walker & Vestberg
Glomus clarum Nicolson & Schenck Hu, 1988 [24]
Glomus clavisporum (Trappe) Almeida
 & Schenck Wu and Chen, 1986 [69]
Glomus constrictum Trappe Fang et al., 1986 [10]
Glomus convolutum Gerd. & Trappe Zhang et al., 2003 [[92]
Glomus coremioides (Berk. & Broome)
 Redecker & Morton Wu and Chen, 1986 [69]
Glomus coronatum Giovann. Zhang et al., 2007 [94]
Glomus cunnighamia Hu * Hu, 1988 [24]
Glomus delhiense Mukerji, Blattacharjee
 & Tewari Liu et al., 2001 [37]
Glomus diaphanum Morton & Walker Peng et al., 1990 [42]
Glomus dimorphicum Boyetchko & Tewari Wang et al., 1998 [67]
Glomus dolichosporum Zhang & Wang * Zhang et al., 1997 [86]
Glomus eburneum Kenn., Stutz & Morton Wang et al., 2006 [64]
Glomus etunicatum Becker & Gerd. Wu and Chen, 1986 [69]
Glomus fasciculatum (Thaxter) Gerdemann
 & Trappe emend. Walker & Koske Wu and Chen, 1986 [69]
Glomus flavisporum (Lange & Lund)
 Trappe & Gerd. Gao et al., 2006 [16]
Glomus formosanum Wu & Chen * Wu and Chen, 1986 [69]
Glomus fulvum (Berk. & Broome) Trappe Wu et al., 2001 [73]
 & Gerd.
Glomus geosporum (Nicol. & Gerd.)
 Walker Wang and Hu, 1989 [63]
Glomus gibbosum Blaszk. Zhang et al., 2003 [92]
Glomus globiferum Koske & Walker Zhang et al., 2003 [92]
Glomus glomerulatum Sieverd. Liu et al., 2001 [37]
Glomus halonatum Rose & Trappe Ren et al., 2005 [45]
Glomus heterosprum Smith & Schenck Zhang et al., 2003 [92]
Glomus hoi Berch & Trappe Wang and Hu, 1989 [63]
Glomus hyderabadensis Swarapu, Kunwar,
 Prasad & Manohar Wang et al., 2006 [64]
Glomus intraradices Schenck & Smith Fang et al., 1986 [10]
Glomus invermaium Hall Gao et al., 2006 [16]
Glomus lamellosum Dalpe, Koske & Tews Zhang et al., 2007 [94]
Glomus liquidam baris (Wu & Chen)
 Almeida & Schenck * Wu and Chen, 1987 [70]
Glomus macrocarpum Tul. & Tul. Hu, 1988 [24]
Glomus luteum Kenn., Stutz & Morton Zhang and Guo, 2005 [93]
Glomus magnicaule Hall Shi et al., 2003 [49]
Glomus manihotis Howeler, Sieverd.
 & Schenck Wu et al., 1994 [74]
Glomus melanosporum Gerd. & Trappe Wang and Liu, 2002 [59]
Glomus microaggregatum Koske, Gemma
 & Olexia Zhang et al., 1996 [85]
Glomus microcarpum Tul. & Tul. Hu, 1988 [24]
Glomus monosporum Gerd. & Trappe Zhao, 1998 [97]
Glomus mosseae (Nicol. & Gerd.) Gerd.
 & Trappe Fang et al., 1986 [10]
Glomus multicaule Gerd. & Bakshi Zhao and Du, 1997 [96]
Glomus multiforum Tadych & Blaszk. Zhao et al., 2006 [95]
Glomus pakistanica Iqbal & Bushra Hu, 1988 [24]
Glomus pallidum Hall Peng et al., 1990 [42]
Glomus pansihalos Berch & Koske Wang and Liu, 2002 [59]
Glomus pustulatum Koske, Friese, Walker
 & Dalpe Wang and Liu, 2002 [59]
Glomus reticulatum Bhattacharjee
 & Mukerji Gai et al., 2000 [15]
Glomus rubiforme Gerdem ann & Trappe Wu and Chen, 1986 [69]
Glomus sinuosum Almeida & Schenck Wang et al., 1992 [62]
Glomus spinosum Hu * Hu, 2002 [25]
Glomus taiwanense (W u & Chen) Almeida
 & Schenck * Wu and Chen, 1987 [70]
Glomus tenebrosum (Thaxt.) Berch Wang and Liu, 2002 [59]
Glomus tortuosum Schenck & Smith Wu et al., 2000 [72]
Glomus verruculosum Blaszk. Li et al., 2004 [30]
Glomus viscosum Nicolson Li et al., 2004 [30]
Glomus zaozhuangianus Wang & Liu * Wang and Liu, 2002 [60]
Kuklospora colombiana Spain & Schenck Zhang et al., 2003 [92]
Kuklospora kentinensis Wu & Liu * Wu et al., 1995 [71]
Pacispora boliviana Oehl & Sieverd. Gao et al., 2006 [16]
Pacispora chimonobambusae (Wu & Liu)
 Walker, Vestberg & Schuessler * Wu et al., 1995 [71]
Pacispora scintillans Walker, Vestberg
 & Schuessler Hu, 1988 [24]
Paraglomus occltum (Walker) Morton
 & Redecker Peng et al., 1990 [42]
Scutellospora aurigloba (Hall) Walker
 & Sanders Peng et al., 1990 [42]
Scutellospora calospora (Nicolson &
 Gerd.) Walker & Sanders Hu, 1988 [24]
Scutellospora cerradensis Spain
 & Miranda Wang et al., 2006 [64]
Scutellospora coralloidea (Trappe, Gerd.
 & Ho) Walker & Sanders Pan et al., 1997 [41]
Scutellospora dipurpurescens Morton
 & Koske Zhao et al., 2006 [95]
Scutellospora erythropa (Koske & Walker)
 Walker & Sanders Pan et al., 1997b [41]
Scutellospora fulgida Koske & Walker Wang et al., 1998 [67]
Scutellospora gilmorei (Trappe & Gerd.)
 Walker & Sanders Hu, 1988 [24]
Scutellospora gregaria (Schenck & Nicol.)
 Walker & Sanders Zhao, 1998 [97]
Scutellospora heterogama (Nicol. & Gerd.)
 Walker & Sanders Wu et al., 1994 [74]
Scutellospora nigra (Redhead) Walker
 & Sanders Hu, 1988 [24]
Scutellospora pellucida (Nicol.
 & Schenck) Hu, 1988 [24]
Scutellospora persica (Koske & Walker)
 Walker & Sanders Zhao, 1998 [97]
Scutellospora reticulata (Koske, Miller
 & Walker) Walker & Sanders Wang et al., 1998 [67]
Scutellospora trirubiginopa Pan &
 Zhang * Pan et al., 1997 [40]
Scutellospora verrucosa (Koske
 & Walker) Walker & Sanders Yang et al., 2004 [78]

Note: The scientic names are amended according to the internet
information (http://www.lrz-muenchen.de/~schuessler/amphylo/); *
New species from China.

Table 2: Plant species reported to be AM in China

Food crops Arachis hypogaea L. Pisum satuvum L.
 [14,39,42,65, Avena nuda L. Sesam um indicum L.
 83,85,91] Eriogonum fasciculatum Setaria italica (L.)
 Benth. Beauv.
 Glycine max M errill. Sorghum vulgare Pers.
 Hordeum vulgare L. Triticum aestivum L.
 Ipomoea batatas (L.) Vigna rabiata (Linn.)
 Lam . Wilczek
 Manihot esculenta Crant. Vicia gemimiflora
 Oryza sativa L. Trautv.
 Zea mays L.

Economic crops Agave sisalana Perrine. Gossypium arboreum
 [10,39,42, Boehm eria nivea (L.) Linn.
 63,91] Camellia sinensis (L.) Helianthus annuus L.
 O . Kuntze. Morus alba L.
 Cannabis sativa L. Nicotiana tabacum L.
 Coffea arabica L. Piper nigrum L.
 Gaudich Hevea Saccharum sinense L.
 brasiliensis Mull.Arg

Fruits Actinidia chinensis Gingko biloba L.
 [4,34,39,54, Planch. Juglans regia L.
 66,74,83,84, Ananas comosus Litchi chinensis Sonn.
 85,100] (L.) Merr. Macadamia ternifolia
 Averrhoa caram bola L. F.Muell
 Canarium album Raeusch Malus pumila Mill.
 Carica papaya L. Mangifera indica L.
 Carya cathayensis Manilkara zapota
 Sargent. (Linn.) Van Royen.
 Castanea mollissima Morus alba L.
 Blum e. Musa sapientum L.
 Citrus aurantium L. Myrica rubra Sieb.
 Citrus grandis O sbeck. et Zucc.
 Citrus lim on Burm ann Pistacia vera L.
 Citrus sinensis O sbeck. Prunus arm eniaca L.
 Citrus sunki Hot. Prunus cerasus L.
 Cocos nucifera L. Prunus mum e Siebold
 Corylus heterophylla & Zucc.
 Fisher. Prunus persica L.
 Crataegus pinnatifolia Prunus salicina Lindl.
 Bunge. Psidium guajava L.
 Dim ocarpus longana Lour. Punica granatum L.
 Diospyros kaki Lf. var. Pyrus bretschneideri
 dom estica Rehd.
 Makino. Rubus occidentalis L.
 Eriobotrya japonica Vitis vinifera L.
 Lindley. Zizyphus jujuba Mill.
 Ficus carica L.
 Fortunella m argarita
 (Lour.) Swingle
 Fragaria x ananassa
 Duch.

Vegetables Allium cepa L. Lactuca sativa L.
 [33,39,42,43, Allium fistulosum L. Lnffa cylindrica Rom e.
 83,84,91] Allium fistulosum Linn. Lycopersicon
 Allium porrum L. esculentum Mill.
 Allium sativum Linn. Momordica charantia L.
 Allium tuberosum Rottl. Phaseolus vulgaris L.
 Am aranthus Phaseolus vulgaris Linn.
 mangostanus L. Pim pinella brachycarpa
 Apium graveolens L. Nakai.
 Asparagus Pisum sativum L.
 officinalis L. Solanum melongena L.
 Capsicum annuum L. Solanum tuberosum L.
 Citrullus lanatus Spinacia oleracea L.
 (Thunb.) Toona sinensis
 Matsum and Nakai (Juss.) Roem.
 Cucum is sativus L. Vigna sesquipedalis
 Daucus carota L. Koern
 Dioscorea batatas Vigna unguiculata
 Decne (L.) Walp.
 Ipom oea aquatica Zanthoxylum
 Forsk. schinifolium Zucc.
 Lablab purpureus (L.) Zingiber
 Sweet officinale Roscoe
 Zizania caduciflora
 Hand.

Flowers Aloe vera L. Lilium longiflorum
 [22,31,33, Cymbidium Thumb.
 39,81,84] ensifolium Sw. Lonicera japonica Thunb.
 Dendranthema Mimosa pudica L.
 morifolium Ram Myosotis sylvatica
 Gerbera Jam Ehrh.ex Hoffm.
 esonii Bolus Paeonia suffruticosa
 Gladiolus gandavensis Andrews.
 Van Houtte Petunia hybrida Vilm.
 Gynostemm a Rosa chinenses Jacq.
 pentaphylla (Thunb.) Rosa x hybrida Hort.
 Makino Saintpaulia ionantha
 Hamelia patins H .Wendl.
 Jasminum sam bac
 (L.) Ait.
 Leucaene leucocephala
 (Lam .) de Wit.

Medical plants Atractylodes macro- Panax notoginseng
 [17,29,39,46, cephala Koidz. (BurK1) F1H1Chen
 67,68,77, Datura stramonium L. Panax quiquefolium L.
 79,84] Gentiana scabra Bge. Phellodendren am urense
 Lonicera japonica Rupr.
 Thunb. Platycodon grandiflorus
 Lycium chinensis (Jacq.) A. DC.
 Mill. Salvia miltiorrhiza
 Mentha haplocalyx Bunge
 Briq. Schizonepeta tenuifolia
 Panax ginseng Briq.
 CA Mey Scutellaria
 laterifolia L.

Forage grasses Medicago sativa L. Aneurolepidium chinense
 [3,5,39, Trifolium repens L (Trin) Kitag.
 76,84] Trifolium pretense L. Festuca rubra L.
 Leymus chinensis
 (Trin.) Tzvel.

Wild weeds Aeluropus littoralis Eulalia specisa
 [1,7,13,15, var. sinensis Debx. (Debeaux)Kuntze
 36,59,84] Agrostis Imperata cylindrica
 stolonifera L. var. major (Nees)
 Alopecurus C.E. Hubb.
 aequalis Sobol. Kummerowia striata
 Artemisia (Thunb.) Schindl.
 lavandulaefolia DC. Orostachys fimbriatus
 Arthraxon hispidus (Turcz.)Berger
 (Thunb.)Makino Papaver nudicaule L.
 Belam canda chinensis Plantago asiatica L.
 (L.) DC. Poa pratensis L.
 Brom us rem otiflorus Polypogon fugax Nees
 (steud.) Ohwi ex Steud.
 Cirsium setosum Puccinellia distans
 (W illd.) M B. (L.) Parl.
 Dendranthema indicum Setaria viridis
 (L.) Des Moul. (L.)Beauv.
 Digitaria ciliaris Vitex negundo Linn.
 (Retz.) Koel. var. heterophylla
 Digitaria sanguinalis (Franch)
 (L.) Scop.
 Eleusine indica (L.)
 Gaertn
 Eragrostis pilosa
 (L.)Beauv.
 Erigeron acris L.

Forest trees Abies fargesii Franch Eucalypt us L.
 [1,9,12,19,20, Acacia L. Fagaceae
 21,24,49,50, Alnus L. Phoebe L.
 69,72,83,86] Betula alnoides Hamlit Poplus L
 Burretiodendron Quercus L.
 hsienmu Chun et How Schim a superba
 Cunninghamia lanceo- Gardner & Champ.
 lata (Lam b.) Hook. Sophora L.
 Cupressus L. Taiwania cryptomerioides
 Dipterocarpaceae Hayata
 Ulmus pumila L.
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Title Annotation:Original Article
Author:Wang, Fa Yuan; Shi, Zhao Yong
Publication:Advances in Environmental Biology
Article Type:Report
Date:Jan 1, 2008
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