两种乳牛肝菌属菌根食用菌与马尾松的共生特征
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摘要
菌根食用菌(ediblemycorrhizalfungi,EMF)是兼具生态价值和经济价值的大型真菌,其对林木健康、森林生态系统的稳定性及林下经济的发展至关重要。本研究以贵州地区马尾松Pinus massoniana林2种乳牛肝菌属Suillus EMF为研究对象,研究了其子实体及其与马尾松形成的菌根的形态特征,调查了其子实体的发生规律及其与温度和降雨的关系。研究结果表明:粘盖乳牛肝菌S.bovinus和褐环乳牛肝菌S.luteus可同时在马尾松林发生。粘盖乳牛肝菌和褐环乳牛肝菌与马尾松形成的菌根均呈珊瑚状,其中粘盖乳牛肝菌形成的菌根表面光滑无根外菌丝但具有根外菌索,褐环乳牛肝菌形成的菌根具有密集的根外菌丝但无根外菌索。粘盖乳牛肝菌和褐环乳牛肝菌子实体具有较长的发生期、产量较大,且具有错峰发生的特点。相对于降雨,温度是这2种乳牛肝菌子实体发生的主要限制因素。
Edible mycorrhizal fungi(EMF) are valuable forest resources, in terms of their ecological functions as symbiont of forest trees and the economic value of their edible basidiomata. They are supposed to play important roles in sustaining forest tree and ecosystem health, and contributing to economic development. In this study, basidiomata and mycorrhizas of two Suillus species associated with Pinus massoniana were morphologically observed, and a three-year field survey was conducted to clarify the phenology of the formation of basidiomata. It was proved that S. bovinus and S. luteus coexisted in forest of P. massoniana in Guizhou Province. The ectomycorrhizas of the two fungi formed in P. massoniana roots are usually coralloid in shape with dichotomous branches. The mycorrhizas formed by S. bovinus had smooth surface without emanating hyphae but with rhizomorph, while those formed by S. luteus had densely emanating hyphae but had no rhizomorph. The basidiomata formed by the two fungi have long fruiting season, considerable production, and staggered occurrence of fruiting peak. Compared with the precipitation, the temperature seemed to be more important in determining basidioma production.
Edible mycorrhizal fungi(EMF) are valuable forest resources, in terms of their ecological functions as symbiont of forest trees and the economic value of their edible basidiomata. They are supposed to play important roles in sustaining forest tree and ecosystem health, and contributing to economic development. In this study, basidiomata and mycorrhizas of two Suillus species associated with Pinus massoniana were morphologically observed, and a three-year field survey was conducted to clarify the phenology of the formation of basidiomata. It was proved that S. bovinus and S. luteus coexisted in forest of P. massoniana in Guizhou Province. The ectomycorrhizas of the two fungi formed in P. massoniana roots are usually coralloid in shape with dichotomous branches. The mycorrhizas formed by S. bovinus had smooth surface without emanating hyphae but with rhizomorph, while those formed by S. luteus had densely emanating hyphae but had no rhizomorph. The basidiomata formed by the two fungi have long fruiting season, considerable production, and staggered occurrence of fruiting peak. Compared with the precipitation, the temperature seemed to be more important in determining basidioma production.
引文
Agerer R,1991.Characterization of ectomycorrhiza.In:Norris JR,Read DJ,Varma AK(eds.)Methods in microbiology.Academic Press,New York.25-73
Agerer R,2001.Exploration types of ectomycorrhizae.Mycorrhiza,11:107-114
Bai SL,Yan W,Ma RH,Wang TN,2001.Investigation of ECMfungi resources in Mt.Daqing and Mt.Manhan.Journal of Mountain Science,19(1):44-47(in Chinese)
Boddy L,Büntgen U,Egli S,Gange AC,Heegaard E,Kirk PM,Mohammad A,Kauserud H,2014.Climate variation effects on fungal fruiting.Fungal Ecology,10:20-33
Bonet JA,de-Miguel S,Martínez de Aragón J,Pukkala T,PalahíM,2012.Immediate effect of thinning on the yield of Lactarius group deliciosus in Pinus pinaster forests in Northeastern Spain.Forest Ecology Management,265:211-217
Buyck B,Zoller S.Hofstetter V,2018.Walking the thin line…ten years later:the dilemma of above-versus below-ground features to support phylogenies in the Russulaceae(Basidiomycota).Fungal Diversity,89:267-292
Chen LQ,1989.Studies on symbiotic mycorrhiza fungi with Masson pine.Forest Research,2(4):357-362(in Chinese)
Dahlberg A,Finlay RD,1999.Suillus.In:Cairney JWG,Chambers SM(eds.)Ectomycorrhizal fungi key genera in profile.Springer,Berlin,Heidelberg.1-369
Dai YC,Zhou LW,Yang ZL,Wen HA,Bau T,Li TH,2010.Arevised checklist of edible fungi in China.Mycosystema,29(1):1-21
Egli S,Ayer F,Peter M,Eilmann B,Rigling A,2010.Is forest mushroom productivity driven by tree growth?Results from a thinning experiment.Annals of Forest Science,67(5):509
Godbout C,Fortin JA,1985.Synthesized ectomycorrhizae of aspen:fungal genus level structural characterization.Canadian Journal of Botany,63:252-262
Gu XR,Ni YL,Jiang YN,Jia H,He XH,2018.Effect of Laccaria bicolor inoculation on contents of inorganic phosphorus and labile aluminum in the rhizosphere soil of Pinus massoniana saplings.Pedologica,55(5):1179-1189(in Chinese)
Hernández-Rodríguez M,de-Miguel S,Pukkala T,Oria-de-Rueda JA,Martín-Pinto P,2015.Climate-sensitive models for mushroom yields and diversity in Cistus ladanifer scrublands.Agricultural and Forest Meteorology,213:173-182
Jiang QB,Zhong CL,Chen Y,Zhang Y,Chen Z,2016.Study on inoculating Russula fungi to Pinus massoniana seedling.Journal of Central South University of Forestry&Technology,36(8):6-9,38(in Chinese)
Karavani A,De Cáceres M,Martínez de Aragón J,Bonet JA,de-Miguel S,2018.Effect of climatic and soil moisture conditions on mushroom productivity and related ecosystem services in Mediterranean pine stands facing climate change.Agricultural and Forest Meteorology,28:432-440
Kong F,Liu Y,Hu W,Shen P,Zhou C,Wang L,2000.Biochemical responses of the mycorrhizae in Pinus massoniana to combined effects of Al,Ca and low pH.Chemosphere,40(3):311-318
Li J,2010.Studies on the macrofungus resources in Taihang Mountain of Hebei Province and antioxidant activity of four kinds of mushrooms.Master Thesis,Hebei Normal University,Shijiazhuang.1-108(in Chinese)
Li M,Ding GJ,Sun XG,Luo XM,Zhang RB,2016.Plant diversity and soil enzyme activity in 4 typical communities of Pinus massoniana of Guizhou.Journal of Forest Environment,36(4):434-441(in Chinese)
Liu F,2009.Optimization of the growth conditions by submerged fermentation and exploration of health drink of Suillus bovinus.Master Thesis,Anhui Agricultural University,Hefei.1-37(in Chinese)
Liu XD,2002.Coloratlas of the wild macrofungi in China 1.China Forestry Publishing House,Beijing.1-228(in Chinese)
Liu XD,2004.Coloratlas of the wild macrofungi in China 2.China Forestry Publishing House,Beijing.1-262(in Chinese)
Luan ZQ,Liang LK,Gong XQ,Liu CL,You CR,Chu Y,2016.Study on optimization of Suillus bovinus under tissue culture conditions.Journal of Biology,33(2):106-109,128(in Chinese)
Mao XL,2009.Macromycetes of China.Scientific Press,Beijing.1-816(in Chinese)
Martínez-Pe?a F,de-Miguel S,Pukkala T,Boet JA,Ortega-Martínez P,Aldea J,Martínez de Aragónd J,2012.Yield models for ectomycorrhizal mushrooms in Pinus sylvestris forests with special focus on Boletus edulis and Lactarius group deliciosus.Forest Ecology and Management,282:63-69
Mleczko P,Ronikier M,2007.Features of ectomycorrhizae confirm molecular phylogenetics of Suillus(Boletales)rather than carpophore-based systematics:insights from studies on Suillus variegatus,S.plorans and related species.Nova Hedwigia,84(1-2):1-20
Murat C,Mello A,AbbàS,Vizzini A,Bonfante P,2008.Edible mycorrhizal fungi:identification,life cycle and morphogenesis.In:Varma A(ed.)Mycorrhiza.Berlin,Heidelberg.707-732
Pang L,Zhou ZC,Zhang Y,Feng ZP,2016.Effects of atmospheric N sedimentation on growth and P efficiency of Pinus massoniana mycorrhizal seedlings under low Pstress.Journal of Plant Nutrition and Fertilizer,22(1):225-235(in Chinese)
Roberts P,Evans SE,2013.The book of fungi.The Ivy Press,London.1-656
Ruiz-Díez B,Rincón AM,de Felipe MR,Fernández-Pascual M,2006.Molecular characterization and evaluation of mycorrhizal capacity of Suillus isolates from Central Spain for the selection of fungal inoculants.Mycorrhiza,16:465-474
Wang M,Yuan L,Zhou Z,Yang H,Huang J,2012.Efflux of oxalate and uptake of nitrogen,phosphorus and potassium by ectomycorrhizal fungal isolates in vitro in response to aluminum stress.Scientia Silvae Sinicae,48(2):82-88
Watling R,Hills AE,Turnbull E,2005.British fungus flora:agarics and boleti.Volume 1.Boletes and their allies.Royal Botanic Garden,Edinburgh.1-173
White TJ,Bruns T,Lee S,Taylor J,1990.Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics.In:Innis MA,Gelfand DH,Sninsky JJ,White TJ(eds.)PCR protocols:a guide to methods and applications.Academic Press,San Diego.315-322
Yamada A,Ogura T,Ohmasa M,2001.Cultivation of mushrooms of edible ectomycorrhizal fungi associated with Pinus densiflora by in vitro mycorrhizal synthesis.Mycorrhiza,11:67-81
Yin D,Deng X,Ilan Chet,Song R,2014.Physiological responses of Pinus sylvestris var.mongolica seedlings to the interaction between Suillus luteus and Trichoderma virens.Current Microbiology,69:334-342
Yin DC,Qi JY,Song RQ,2018.The effect of compound inoculation of Suillus luteus and Trichoderma virens on the interannual changes of the bioactivity of Pinus sylvestris var.mongolica rhizosphere.Chinese Journal of Ecology,37(9):2637-2641(in Chinese)
Yu H,Chen Z,Shang H,Cao JX,2017.Effects of ectomycorrhizal fungi on seedlings of Pinus massoniana under simulated acid rain.Acta Ecologica Sinica,37(6):5418-5427(in Chinese)
Yuan MS,Sun PQ,2013.Color atlas of large fungi in China.Sichuan Science and Technology Press,Sichuan.1-564(in Chinese)
Zhou ZX,2001.Chinese Masson pine.China Forestry Press,Beijing.1-200(in Chinese)
白淑兰,闫伟,马荣华,王铁牛,2001.大青山、蛮汗山外生菌根真菌资源调查.山地学报,19(1):44-47
陈连庆,1989.马尾松共生菌根真菌调查研究.林业科学研究,2(4):357-362
戴玉成,周丽伟,杨祝良,文华安,图力古尔,李泰辉,2010.中国食用菌名录.菌物学报,29(1):1-21
辜夕容,倪亚兰,江亚男,贾豪,何新华,2018.接种双色蜡蘑对马尾松根际土壤无机磷和活性铝含量的影响.土壤学报,55(5):1179-1189
姜清彬,仲崇禄,陈羽,张勇,陈珍,2016.红菇菌根食用菌接种马尾松苗期的共生效应研究.中南林业科技大学学报,36(8):6-9,38
李洁,2010.河北省太行山区野生高等真菌资源调查及四种子实体抗氧化活性研究.河北师范大学硕士论文,石家庄.1-108
李敏,丁贵杰,孙学广,罗晓蔓,张仁波,2016.贵州马尾松群落植物多样性与土壤酶活性.森林与环境学报,36(4):434-441
刘芳,2009.乳牛肝菌液态发酵生长条件的优化及其保健饮品开发的探索.安徽农业大学硕士论文,合肥.1-37
刘旭东,2002.中国野生大型真菌彩色图鉴1.北京:中国林业出版社.1-228
刘旭东,2004.中国野生大型真菌彩色图鉴2.北京:中国林业出版社.1-262
栾竹青,梁丽琨,龚雪琴,刘传林,由翠荣,初洋,2016.组培条件下乳牛肝菌培养基的优化研究.生物学杂志,33(2):106-109,128
卯晓岚,2009.中国蕈菌.北京:科学出版社.1-816
庞丽,周志春,张一,丰忠平,2016.大气氮沉降提高低磷土壤条件下马尾松菌根共生和磷效率的原因.植物营养与肥料学报,22(1):225-235
尹大川,祁金玉,宋瑞清,2018.复合接种褐环乳牛肝菌与绿木霉对樟子松根际土壤生物活性年际变化的影响.生态学杂志,37(9):2637-2641
于浩,陈展,尚鹏,曹吉鑫.2017.野外模拟酸雨胁迫下接种外生菌根真菌对马尾松幼苗的缓解作用.生态学报,37(16):5418-5427
袁明生,孙佩琼,2013.中国大型真菌彩色图谱.四川:四川科学技术出版社.1-564
周政贤,2001.中国马尾松.北京:中国林业出版社.1-200
Agerer R,2001.Exploration types of ectomycorrhizae.Mycorrhiza,11:107-114
Bai SL,Yan W,Ma RH,Wang TN,2001.Investigation of ECMfungi resources in Mt.Daqing and Mt.Manhan.Journal of Mountain Science,19(1):44-47(in Chinese)
Boddy L,Büntgen U,Egli S,Gange AC,Heegaard E,Kirk PM,Mohammad A,Kauserud H,2014.Climate variation effects on fungal fruiting.Fungal Ecology,10:20-33
Bonet JA,de-Miguel S,Martínez de Aragón J,Pukkala T,PalahíM,2012.Immediate effect of thinning on the yield of Lactarius group deliciosus in Pinus pinaster forests in Northeastern Spain.Forest Ecology Management,265:211-217
Buyck B,Zoller S.Hofstetter V,2018.Walking the thin line…ten years later:the dilemma of above-versus below-ground features to support phylogenies in the Russulaceae(Basidiomycota).Fungal Diversity,89:267-292
Chen LQ,1989.Studies on symbiotic mycorrhiza fungi with Masson pine.Forest Research,2(4):357-362(in Chinese)
Dahlberg A,Finlay RD,1999.Suillus.In:Cairney JWG,Chambers SM(eds.)Ectomycorrhizal fungi key genera in profile.Springer,Berlin,Heidelberg.1-369
Dai YC,Zhou LW,Yang ZL,Wen HA,Bau T,Li TH,2010.Arevised checklist of edible fungi in China.Mycosystema,29(1):1-21
Egli S,Ayer F,Peter M,Eilmann B,Rigling A,2010.Is forest mushroom productivity driven by tree growth?Results from a thinning experiment.Annals of Forest Science,67(5):509
Godbout C,Fortin JA,1985.Synthesized ectomycorrhizae of aspen:fungal genus level structural characterization.Canadian Journal of Botany,63:252-262
Gu XR,Ni YL,Jiang YN,Jia H,He XH,2018.Effect of Laccaria bicolor inoculation on contents of inorganic phosphorus and labile aluminum in the rhizosphere soil of Pinus massoniana saplings.Pedologica,55(5):1179-1189(in Chinese)
Hernández-Rodríguez M,de-Miguel S,Pukkala T,Oria-de-Rueda JA,Martín-Pinto P,2015.Climate-sensitive models for mushroom yields and diversity in Cistus ladanifer scrublands.Agricultural and Forest Meteorology,213:173-182
Jiang QB,Zhong CL,Chen Y,Zhang Y,Chen Z,2016.Study on inoculating Russula fungi to Pinus massoniana seedling.Journal of Central South University of Forestry&Technology,36(8):6-9,38(in Chinese)
Karavani A,De Cáceres M,Martínez de Aragón J,Bonet JA,de-Miguel S,2018.Effect of climatic and soil moisture conditions on mushroom productivity and related ecosystem services in Mediterranean pine stands facing climate change.Agricultural and Forest Meteorology,28:432-440
Kong F,Liu Y,Hu W,Shen P,Zhou C,Wang L,2000.Biochemical responses of the mycorrhizae in Pinus massoniana to combined effects of Al,Ca and low pH.Chemosphere,40(3):311-318
Li J,2010.Studies on the macrofungus resources in Taihang Mountain of Hebei Province and antioxidant activity of four kinds of mushrooms.Master Thesis,Hebei Normal University,Shijiazhuang.1-108(in Chinese)
Li M,Ding GJ,Sun XG,Luo XM,Zhang RB,2016.Plant diversity and soil enzyme activity in 4 typical communities of Pinus massoniana of Guizhou.Journal of Forest Environment,36(4):434-441(in Chinese)
Liu F,2009.Optimization of the growth conditions by submerged fermentation and exploration of health drink of Suillus bovinus.Master Thesis,Anhui Agricultural University,Hefei.1-37(in Chinese)
Liu XD,2002.Coloratlas of the wild macrofungi in China 1.China Forestry Publishing House,Beijing.1-228(in Chinese)
Liu XD,2004.Coloratlas of the wild macrofungi in China 2.China Forestry Publishing House,Beijing.1-262(in Chinese)
Luan ZQ,Liang LK,Gong XQ,Liu CL,You CR,Chu Y,2016.Study on optimization of Suillus bovinus under tissue culture conditions.Journal of Biology,33(2):106-109,128(in Chinese)
Mao XL,2009.Macromycetes of China.Scientific Press,Beijing.1-816(in Chinese)
Martínez-Pe?a F,de-Miguel S,Pukkala T,Boet JA,Ortega-Martínez P,Aldea J,Martínez de Aragónd J,2012.Yield models for ectomycorrhizal mushrooms in Pinus sylvestris forests with special focus on Boletus edulis and Lactarius group deliciosus.Forest Ecology and Management,282:63-69
Mleczko P,Ronikier M,2007.Features of ectomycorrhizae confirm molecular phylogenetics of Suillus(Boletales)rather than carpophore-based systematics:insights from studies on Suillus variegatus,S.plorans and related species.Nova Hedwigia,84(1-2):1-20
Murat C,Mello A,AbbàS,Vizzini A,Bonfante P,2008.Edible mycorrhizal fungi:identification,life cycle and morphogenesis.In:Varma A(ed.)Mycorrhiza.Berlin,Heidelberg.707-732
Pang L,Zhou ZC,Zhang Y,Feng ZP,2016.Effects of atmospheric N sedimentation on growth and P efficiency of Pinus massoniana mycorrhizal seedlings under low Pstress.Journal of Plant Nutrition and Fertilizer,22(1):225-235(in Chinese)
Roberts P,Evans SE,2013.The book of fungi.The Ivy Press,London.1-656
Ruiz-Díez B,Rincón AM,de Felipe MR,Fernández-Pascual M,2006.Molecular characterization and evaluation of mycorrhizal capacity of Suillus isolates from Central Spain for the selection of fungal inoculants.Mycorrhiza,16:465-474
Wang M,Yuan L,Zhou Z,Yang H,Huang J,2012.Efflux of oxalate and uptake of nitrogen,phosphorus and potassium by ectomycorrhizal fungal isolates in vitro in response to aluminum stress.Scientia Silvae Sinicae,48(2):82-88
Watling R,Hills AE,Turnbull E,2005.British fungus flora:agarics and boleti.Volume 1.Boletes and their allies.Royal Botanic Garden,Edinburgh.1-173
White TJ,Bruns T,Lee S,Taylor J,1990.Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics.In:Innis MA,Gelfand DH,Sninsky JJ,White TJ(eds.)PCR protocols:a guide to methods and applications.Academic Press,San Diego.315-322
Yamada A,Ogura T,Ohmasa M,2001.Cultivation of mushrooms of edible ectomycorrhizal fungi associated with Pinus densiflora by in vitro mycorrhizal synthesis.Mycorrhiza,11:67-81
Yin D,Deng X,Ilan Chet,Song R,2014.Physiological responses of Pinus sylvestris var.mongolica seedlings to the interaction between Suillus luteus and Trichoderma virens.Current Microbiology,69:334-342
Yin DC,Qi JY,Song RQ,2018.The effect of compound inoculation of Suillus luteus and Trichoderma virens on the interannual changes of the bioactivity of Pinus sylvestris var.mongolica rhizosphere.Chinese Journal of Ecology,37(9):2637-2641(in Chinese)
Yu H,Chen Z,Shang H,Cao JX,2017.Effects of ectomycorrhizal fungi on seedlings of Pinus massoniana under simulated acid rain.Acta Ecologica Sinica,37(6):5418-5427(in Chinese)
Yuan MS,Sun PQ,2013.Color atlas of large fungi in China.Sichuan Science and Technology Press,Sichuan.1-564(in Chinese)
Zhou ZX,2001.Chinese Masson pine.China Forestry Press,Beijing.1-200(in Chinese)
白淑兰,闫伟,马荣华,王铁牛,2001.大青山、蛮汗山外生菌根真菌资源调查.山地学报,19(1):44-47
陈连庆,1989.马尾松共生菌根真菌调查研究.林业科学研究,2(4):357-362
戴玉成,周丽伟,杨祝良,文华安,图力古尔,李泰辉,2010.中国食用菌名录.菌物学报,29(1):1-21
辜夕容,倪亚兰,江亚男,贾豪,何新华,2018.接种双色蜡蘑对马尾松根际土壤无机磷和活性铝含量的影响.土壤学报,55(5):1179-1189
姜清彬,仲崇禄,陈羽,张勇,陈珍,2016.红菇菌根食用菌接种马尾松苗期的共生效应研究.中南林业科技大学学报,36(8):6-9,38
李洁,2010.河北省太行山区野生高等真菌资源调查及四种子实体抗氧化活性研究.河北师范大学硕士论文,石家庄.1-108
李敏,丁贵杰,孙学广,罗晓蔓,张仁波,2016.贵州马尾松群落植物多样性与土壤酶活性.森林与环境学报,36(4):434-441
刘芳,2009.乳牛肝菌液态发酵生长条件的优化及其保健饮品开发的探索.安徽农业大学硕士论文,合肥.1-37
刘旭东,2002.中国野生大型真菌彩色图鉴1.北京:中国林业出版社.1-228
刘旭东,2004.中国野生大型真菌彩色图鉴2.北京:中国林业出版社.1-262
栾竹青,梁丽琨,龚雪琴,刘传林,由翠荣,初洋,2016.组培条件下乳牛肝菌培养基的优化研究.生物学杂志,33(2):106-109,128
卯晓岚,2009.中国蕈菌.北京:科学出版社.1-816
庞丽,周志春,张一,丰忠平,2016.大气氮沉降提高低磷土壤条件下马尾松菌根共生和磷效率的原因.植物营养与肥料学报,22(1):225-235
尹大川,祁金玉,宋瑞清,2018.复合接种褐环乳牛肝菌与绿木霉对樟子松根际土壤生物活性年际变化的影响.生态学杂志,37(9):2637-2641
于浩,陈展,尚鹏,曹吉鑫.2017.野外模拟酸雨胁迫下接种外生菌根真菌对马尾松幼苗的缓解作用.生态学报,37(16):5418-5427
袁明生,孙佩琼,2013.中国大型真菌彩色图谱.四川:四川科学技术出版社.1-564
周政贤,2001.中国马尾松.北京:中国林业出版社.1-200