Genetic variation and population structure of the mushroom Pleurotus ferulae in China inferred from nuclear DNA analysis

doi:10.1016/S2095-3119(16)61383-7

摘要/Abstract

Abstract: To investigate the genetic diversity of an edible fungus Pleurotus ferulae, a total of 89 wild samples collected from six geographical locations in the Xinjiang Uygur Autonomous Region of China and two geographical locations in Italy, were analyzed using three DNA fragments including the translation elongation factor (EF1α), the second largest subunit of the RNA polymerase II (RPB2) and the largest subunit of the RNA polymerase II (RPB1). The results indicated relatively abundant genetic variability in the wild resources of P. ferulae. The analysis of molecular variance (AMOVA) showed that the vast majority of the genetic variation was found within geographical populations. Both the Chinese populations and the Italian populations of P. ferulae displayed a limited genetic differentiation. The degree of differentiation between the Chinese populations and the Italian populations was obviously higher than that between the populations from the same region, and moreover the genetic differentiation among all the tested populations was correlated to the geographical distance. The phylogeny analyses confirmed that samples from China and Italy belonged to another genetic group separated from Pleurotus eryngii. They were closely related to each other but were clustered according to their geographical origins, which implied the Chinese populations were highly differentiated from the Italian populations because of distance isolation, and the two populations from different regions might be still in the process of allopatric divergence.

Key words: genetic variation , population structure , genetic differentiation

ZHAO Meng-ran, HUANG Chen-yang, WU Xiang-li, CHEN Qiang, QU Ji-bin, LI Yan-chun, GAO Wei, ZHANG Jin-xia. [J]. Journal of Integrative Agriculture, 2016, 15(10): 2237-2246.

ZHAO Meng-ran, HUANG Chen-yang, WU Xiang-li, CHEN Qiang, QU Ji-bin, LI Yan-chun, GAO Wei, ZHANG Jin-xia. Genetic variation and population structure of the mushroom Pleurotus ferulae in China inferred from nuclear DNA analysis[J]. Journal of Integrative Agriculture, 2016, 15(10): 2237-2246.

参考文献

Akyuz M, Kirbag S. 2009. Antimicrobial activity of Pleurotus eryngii var. ferulae grown on various agro-wastes. EurAsian Journal of Biosciences, 3, 58–63.

Akyuz M, Kirbag S. 2010. Effect of various agro-residues on nutritive value of Pleurotus eryngii (DC. ex Fr.) Quél. var. ferulae Lanzi. Journal of Agricultural Sciences, 16, 83–88.

Akyuz M, Yildiz A. 2008. Evaluation of cellulosic wastes for the cultivation of Pleurotus eryngii (DC. ex Fr.) Quél. African Journal of Biotechnology, 7, 1494–1499.

Alam N, Yoon K N, Lee J S, Cho H J, Lee T S. 2012. Consequence of the antioxidant activities and tyrosinase inhibitory effects of various extracts from the fruiting bodies of Pleurotus ferulae. Saudi Journal of Biological Sciences, 19, 111–118.

Bergemann S E, Smith M A, Parrent J L, Gilbert G S, Garbelotto M. 2009. Genetic population structure and distribution of a fungal polypore, Datronia caperata (Polyporaceae), in mangrove forests of Central America. Journal of Biogeography, 36, 266–279.

Bertolino S, Vizzini A, Wauters L A, Tosi G. 2004. Consumption of hypogeous and epigeous fungi by the red squirrel (Sciurus vulgaris) in subalpine conifer forests. Forest Ecology and Management, 202, 227–233.

Boisselier-Dubayle M C, Perreau-Bertrand J, Lambourdiere J. 1996. Genetic variablility in wild populations of Mycena rosea. Mycological Research, 100, 753–758.

Brewer M T, Milgroom M G. 2010. Phylogeography and population structure of the grape powdery mildew fungus, Erysiphe necator, from diverse Vitis species. BMC Evolutionary Biology, 10, 268–281.

Cao Y, Zhang Y, Yu Z F, Mi F, Liu C L, Tang X Z, Long Y X, He X X, Wang P F, Xu J P. 2013. Structure, gene flow, and recombination among geographic populations of a Russula virescens Ally from southwestern China. PLOS ONE, 8, e73174.

Chen Z C. 1986. Preliminary research on the domestication of Pleurotus ferulae. Edible Fungi of China, 2, 16–17. (in Chinese)

Cogliati M, Zani A, Rickerts V, McCormick I, Desnos-Ollivier M, Velegraki A, Escandon P, Ichikawa T, Ikeda R, Bienvenu A L, Tintelnot K, Tore O, Akcaglar S, Lockhart S, Tortorano A M, Varma A. 2016. Multilocus sequence typing analysis reveals that Cryptococcus neoformans var. neoformans is a recombinant population. Fungal Genetics and Biology, 87, 22–29.

Cozzolino S, Cafasso D, Pellegrino G, Musacchio A, Widmer A. 2003. Fine-scale phylogeographical analysis of Mediterranean Anacamptis palustris (Orchidaceae) populations based on chloroplast minisatellite and microsatellite variation. Molecular Ecology, 12, 2783–2792.

Ding Z, Chen Y, Xu Z, Peng L, Xu G, Gu Z, Zhang L, Shi G, Zhang K. 2013. Production and characterization of laccase from Pleurotus ferulae in submerged fermentation. Annals of Microbiology, 64, 121–129.

Douhan G W, Vincenot L, Gryta H, Selosse M A. 2011. Population genetics of ectomycorrhizal fungi: From current knowledge to emerging directions. Fungal Biology, 115, 569–597.

Excoffier L, Laval G, Schneider S. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolution Bioinformatics Online, 1, 47–50.

Feng B, Zhao Q, Xu J P, Qin J, Yang Z L. 2016. Drainage isolation and climate change-driven population expansion shape the genetic structures of Tuber indicum complex in the Hengduan Mountains region. Scientific Reports, 6, 1-10.

Gascon C, Malcolm J R, Patton J L, da Silva M N, Bogart J P, Lougheed S C, Peres C A, Neckel S, Boag P T. 2000. Riverine barriers and the geographic distribution of Amazonian species. Proceedings of the National Academy of Sciences of the United States of America, 97, 13672–13677.

Geml J, Kauff F, Brochmann C, Taylor D L. 2010. Surviving climate changes: High genetic diversity and transoceanic gene flow in two arctic-alpine lichens, Flavocetraria cucullata and F. nivalis (Parmeliaceae, Ascomycota). Journal of Biogeography, 37, 1529–1542.

De Gioia T, Sisto D, Rana G L, Figliuolo G. 2005. Genetic structure of the Pleurotus eryngii species-complex. Mycological Research, 109, 71–80.

Halling R E, Osmundson T W, Neves M A. 2008. Pacific boletes: implications for biogeographic relationships. Mycological Research, 112, 437–447.

Hibbett D S. 2001. Shiitake mushrooms and molecular clocks: historical biogeography of Lentinula. Mycological Research, 28, 231–241.

James T Y, Porter D, Hamrick J L, Vilgalys R. 1999. Evidence for limited iIntercontinental gene flow in the cosmopolitan mushroom, Schizophyllum commune. Evolution, 53, 1665–1677.

Jargeat P, Martos F, Carriconde F, Gryta H, Moreau P A, Gardes M. 2010. Phylogenetic species delimitation in ectomycorrhizal fungi and implications for barcoding: The case of the Tricholoma scalpturatum complex (Basidiomycota). Molecular Ecology, 19, 5216–5230.

Kauserud H, Svegarden I B, Saetre G P, Knudsen H, Stensrud O, Schmidt O, Doi S, Sugiyama T, Hogberg N. 2007. Asian origin and rapid global spread of the destructive dry rot fungus Serpula lacrymans. Molecular Ecology, 16, 3350–3360.

Kirbag S, Akyüz M. 2008. Evaluation of agricultural wastes for the cultivation of Pleurotus eryngii var ferulae (DC. ex Fr.) Quél. African Journal of Biotechnology, 7, 3660–3664.

Lewinsohn D, Nevo E, Wasser S P, Hadar Y, Beharav A. 2001. Genetic diversity in populations of the Pleurotus eryngii complex in Israel. Mycological Research, 105, 941–951.

Lian C L, Narimatsu M, Nara K, Hogetsu T. 2006. Tricholoma matsutake in a natural Pinus densiflora forest: Correspondence between above- and below-ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytologist, 171, 825–836.

Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.

Li M C, Liang J F, Li Y C, Feng B, Yang Z L, James T Y, Xu J P. 2010. Genetic diversity of Dahongjun, the commercially important “Big Red Mushroom” from southern China. PLoS ONE, 5, e10684.

Mang S M, Figliuolo G. 2010. Species delimitation in Pleurotus eryngii species-complex inferred from ITS and EF-1α gene sequences. Mycology, 1, 269–280.

Moncalvo J M, Buchanan P K. 2008. Molecular evidence for long distance dispersal across the Southern Hemisphere in the Ganoderma applanatum-australe species complex (Basidiomycota). Mycological Research, 112, 425–436.

Mou C J, Cao Y Q. 1986. The mushroom of Pleurotus ferulae in Xinjiang and its domesticated and cultural traits. Edible Fungi, 5, 4–5. (in Chinese)

Nevo E. 1998. Molecular evolution and ecological stress at global, regional and local scales: The Israeli perspective. The Journal of Experimental Zoology, 282, 95–119.

Nevo E, Beiles A. 1988. Genetic parallelism of protein polymorphism in nature: Ecological test of the neutral theory of molecular evolution. Biological Journal of the Linnean Society, 35, 229–245.

Nielsen R, Slatkin M. 2000. Likelihood analysis of ongoing gene flow and historical association. Evolution, 54, 44–50.

Pildain M B, Coetzee M P A, Rajchenberg M, Petersen R H, Wingfield M J, Wingfield B D. 2009. Molecular phylogeny of Armillaria from the Patagonian Andes. Mycological Progress, 8, 181–194.

Posada D, Crandall K A. 1998. Modeltest: Testing the model of DNA substitution. Bioinformatics, 14, 817–818.

Rodriguez Estrada A E, Jimenez-Gasco Mdel M, Royse D J. 2010. Pleurotus eryngii species complex: Sequence analysis and phylogeny based on partial EF1α and RPB2 genes. Fungal Biology, 114, 421–428.

Ro H S, Kim S S, Ryu J S, Jeon C O, Lee T S, Lee H S. 2007. Comparative studies on the diversity of the edible mushroom Pleurotus eryngii: ITS sequence analysis, RAPD fingerprinting, and physiological characteristics. Mycological Research, 111, 710–715.

Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

Rosendahl S, McGee P, Morton J B. 2009. Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Molecular Ecology, 18, 4316–4329.

Saville B J, Yoell H, Anderson J B. 1996. Genetic exchange and recombination in populations of the root-infecting fungus Armillaria gallica. Molecular Ecology, 5, 485–497.

Schoch C L, Sung G H, Lopez-Giraldez F, Townsend J P, Miadlikowska J, Hofstetter V, Robbertse B, Matheny P B, Kauff F, Wang Z, Gueidan C, Andrie R M, Trippe K, Ciufetti L M, Wynns A, Fraker E, Hodkinson B P, Bonito G, Groenewald J Z, Arzanlou M, et al. 2009. The Ascomycota tree of life: A phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Society of Systematic Biologists, 58, 224–239.

Stephens M, Donnelly P. 2003. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetic, 73, 1162–1169.

Swofford D L. 2002. PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods), 4th ed. Sinauer Associates, Sunderland, MA, USA. pp. 12-26

Taylor E B, Boughman J W, Groenenboom M, Sniatynski M, Schluter D, Gow J L. 2006. Speciation in reverse: Morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Molecular Ecology, 15, 343–355.

Urbanelli S, Della Rosa V, Fanelli C, Fabbri A A, Reverberi M. 2003. Genetic diversity and population structure of the Italian fungi belonging to the taxa Pleurotus eryngii (DC.:Fr.) Quél and P. ferulae (DC.:Fr.) Quél. Heredity, 90, 253–259.

Urbanelli S, Fanelli C, Fabbri A A, Della Rosa V, Maddau L, Marras F M R. 2002. Molecular genetic analysis of two taxa of the Pleurotus eryngii complex: Pleurotus eryngii (DC.:Fr.) Quél. var. eryngii and P. ferulae (DC.:Fr.) Quél. var. ferulae. Biological Journal of the Linnean Society, 75, 125–136.

Vincenot L, Nara K, Sthultz C, Labbe J, Dubois M P, Tedersoo L, Martin F, Selosse M A. 2012. Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete Laccaria amethystina complex. Molecular Ecology, 21, 281–299.

Xu J P. 2006. Fudamental of fungal molecular population genetic analyses. Current Issues in Molecular Biology, 8, 75–90.

Zervakis G I, Moncalvo J M, Vilgalys R. 2004. Molecular phylogeny, biogeography and speciation of the mushroom species Pleurotus cystidiosus and allied taxa. Microbiology, 150, 715–726.

Zervakis G I, Venturella G, Papadopoulou K. 2001. Genetic polymorphism and taxonomic infrastructure of the Pleurotus eryngii species-complex as determined by RAPD analysis, isozyme profiles and ecomorphological characters. Microbiology, 147, 3183–3194.

Zhang J X, Huang C Y, Ng T B, Wang H X. 2006. Genetic polymorphism of ferula mushroom growing on Ferula sinkiangensis. Applied Genetics and Molecular Biotechnology, 71, 304–309.

Zhao M R, Huang C Y, Chen Q, Wu X L, Qu J B, Zhang J X. 2013. Genetic variability and population structure of the mushroom Pleurotus eryngii var. tuoliensis. PLOS ONE, 8, e83253.

Zheng W, Zou L, Han Z Q. 2015. Genetic analysis of the populations of Japanese anchovy Engraulis japonicus from the Yellow Sea and East China Sea based on mitochondrial cytochrome b sequence. Biochemical Systematics and Ecology, 58, 169–177.