Deciphering interfungal relationships in the 410-million-yr-old Rhynie chert: an intricate interaction between two mycelial fungi

详细信息    查看全文

• 作者：Michael Krings (1) (2) (3)
  Thomas N. Taylor (3)
  
  1. Department f眉r Geo- und Umweltwissenschaften ; Pal盲ontologie und Geobiologie ; Ludwig-Maximilians-Universit盲t ; Richard-Wagner-Stra脽e 10 ; 80333 ; Munich ; Germany
  2. Bayerische Staatssammlung f眉r Pal盲ontologie und Geologie ; Richard-Wagner-Stra脽e 10 ; 80333 ; Munich ; Germany
  3. Department of Ecology and Evolutionary Biology ; and Natural History Museum and Biodiversity Research Institute ; University of Kansas ; Lawrence ; KS ; 66045 ; USA
  
• 关键词：Early Devonian ; Fossil fungi ; Glomeromycota ; Hyphal investment ; Mycoparasitism
• 刊名：Symbiosis
• 出版年：2014
• 出版时间：October 2014
• 年：2014
• 卷：64
• 期：2
• 页码：53-61
• 全文大小：1,353 KB
• 参考文献：1. B艂aszkowski J (1995) / Glomus corymbiforme, a new species in Glomales from Poland. Mycologia 87:732鈥?37 10.2307/3760819" target="_blank" title="It opens in new window">CrossRef
  2. Boyetchko SM, Tewari JP (1991) Parasitism of spores of the vesicular-arbuscular mycorrhizal fungus, / Glomus dimorphicum. Phytoprotection 72:27鈥?2 10.7202/706000ar" target="_blank" title="It opens in new window">CrossRef
  3. Bucholtz F (1912) Beitr盲ge zur Kenntnis der Gattung / Endogone Link. Beih Bot Centralbl Abt II 29:147鈥?24
  4. Channing A, Edwards D, Sturtevant S (2004) A geothermally influenced wetland containing unconsolidated geochemical sediments. Can J Earth Sci 41:809鈥?27 10.1139/e04-034" target="_blank" title="It opens in new window">CrossRef
  5. Combes C (2001) Parasitism. The ecology and evolution of intimate interactions. University of Chicago Press, Chicago
  6. Daniels BA, Menge JA (1980) Hyperparasitization of vesicular-arbuscular mycorrhizal fungi. Phytopathology 70:584鈥?88 10.1094/Phyto-70-584" target="_blank" title="It opens in new window">CrossRef
  7. Dotzler N, Krings M, Taylor TN, Agerer R (2006) Germination shields in / Scutellospora (Glomeromycota: Diversisporales, Gigasporaceae) from the 400 million-year-old Rhynie chert. Mycol Prog 5:178鈥?84 10.1007/s11557-006-0511-z" target="_blank" title="It opens in new window">CrossRef
  8. Dotzler N, Walker C, Krings M, Hass H, Kerp H, Taylor TN, Agerer R (2009) Acaulosporoid glomeromycotan spores with a germination shield from the 400-million-year-old Rhynie chert. Mycol Prog 8:9鈥?8 10.1007/s11557-008-0573-1" target="_blank" title="It opens in new window">CrossRef
  9. Godfrey RM (1957) Studies of British species of / Endogone. II. Fungal parasites. Trans British Mycol Soc 40:136鈥?44 10.1016/S0007-1536(57)80072-2" target="_blank" title="It opens in new window">CrossRef
  10. Hass H, Taylor TN, Remy W (1994) Fungi from the Lower Devonian Rhynie chert: mycoparasitism. Amer J Bot 81:29鈥?7 10.2307/2445559" target="_blank" title="It opens in new window">CrossRef
  11. Hijri M, Redecker D, MacDonald-Comber Petetot JA, Voigt K, W枚stemeyer J, Sanders IR (2002) Identification and isolation of two ascomycete fungi from spores of the arbuscular mycorrhizal fungus / Scutellospora castanea. Appl Environ Microbiol 68:4567鈥?573 10.1128/AEM.68.9.4567-4573.2002" target="_blank" title="It opens in new window">CrossRef
  12. Jeffries P, Young TWK (1994) Interfungal parasitic relationships. CAB International, Wallingford
  13. Karatygin IV, Snigirevskaya NS, Demchenko KN (2006) Species of the genus / Glomites as plant mycobionts in Early Devonian ecosystems. Paleontol J 40:572鈥?79 10.1134/S0031030106050121" target="_blank" title="It opens in new window">CrossRef
  14. Kidston R, Lang WH (1921) On Old Red Sandstone plants showing structure, from the Rhynie Chert bed, Aberdeenshire. Part V. The Thallophyta occurring in the peat-bed; the succession of the plants throughout a vertical section of the bed, and the conditions of accumulation and preservation of the deposit. Trans Roy Soc Edinburgh 52:855鈥?02 10.1017/S0080456800016045" target="_blank" title="It opens in new window">CrossRef
  15. Krings M, Taylor TN (2013) / Zwergimyces vestitus (Kidston et W.H. Lang) nov. comb., a fungal reproductive unit enveloped in a hyphal mantle from the Lower Devonian Rhynie chert. Rev Palaeobot Palynol 190:15鈥?9 10.1016/j.revpalbo.2012.11.008" target="_blank" title="It opens in new window">CrossRef
  16. Krings M, Taylor TN (2014a) A mantled fungal reproductive unit from the Lower Devonian Rhynie chert that demonstrates Carboniferous 鈥渟porocarp鈥?morphology and development. N Jb Geol Pal盲ontol Abh 273:197鈥?05 10.1127/0077-7749/2014/0423" target="_blank" title="It opens in new window">CrossRef
  17. Krings M, Taylor TN (2014b) An unusual fossil microfungus with suggested affinities to the Chytridiomycota from the Lower Devonian Rhynie chert. Nova Hedw 99:403鈥?12 10.1127/0029-5035/2014/0205" target="_blank" title="It opens in new window">CrossRef
  18. Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007a) An alternative mode of early land plant colonization by putative endomycorrhizal fungi. Plant Signal Behav 2:125鈥?26 10.4161/psb.2.2.3970" target="_blank" title="It opens in new window">CrossRef
  19. Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007b) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174:648鈥?57 10.1111/j.1469-8137.2007.02008.x" target="_blank" title="It opens in new window">CrossRef
  20. Krings M, Dotzler N, Taylor TN (2009) / Globicultrix nugax nov. gen. et nov. spec. (Chytridiomycota), an intrusive microfungus in fungal spores from the Rhynie chert. Zitteliana A 48/49:165鈥?70
  21. Krings M, Dotzler N, Longcore JE, Taylor TN (2010) An unusual microfungus in a fungal spore from the Lower Devonian Rhynie chert. Palaeontology 53:753鈥?59 10.1111/j.1475-4983.2010.00959.x" target="_blank" title="It opens in new window">CrossRef
  22. Krings M, Taylor TN, Dotzler N (2013) Fossil evidence of the zygomycetous fungi. Persoonia 30:1鈥?0 10.3767/003158513X664819" target="_blank" title="It opens in new window">CrossRef
  23. Krings M, Taylor TN, Taylor EL, Kerp H, Dotzler N (2014) First record of a fungal 鈥渟porocarp鈥?from the Lower Devonian Rhynie chert. Palaeobiodivers Palaeoenviron 94:221鈥?27 10.1007/s12549-013-0135-7" target="_blank" title="It opens in new window">CrossRef
  24. Lee PJ, Koske RE (1994) / Gigaspora gigantea: parasitism of spores by fungi and actinomycetes. Mycol Res 98:458鈥?66 10.1016/S0953-7562(09)81205-7" target="_blank" title="It opens in new window">CrossRef
  25. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746鈥?748 10.1126/science.1143082" target="_blank" title="It opens in new window">CrossRef
  26. Malen莽on MC (1947) 脡tudes de parasitisme mycopathologique. Rev Mycol 7:27鈥?2
  27. Mark DF, Rice CM, Fallick AE, Trewin NH, Lee MR, Boyce A, Lee JKW (2011) ⁴⁰Ar/³⁹Ar dating of hydrothermal activity, biota and gold mineralization in the Rhynie hot-spring system, Aberdeenshire, Scotland. Geochim Cosmochim Acta 75:555鈥?69 10.1016/j.gca.2010.10.014" target="_blank" title="It opens in new window">CrossRef
  28. Mark DF, Rice CM, Trewin NH (2013) Discussion on 鈥楢 high-precision U鈥揚b age constraint on the Rhynie Chert Konservat-Lagerst盲tte: time scale and other implications鈥? / Journal, Vol. 168, 863鈥?72. J Geol Soc London 170:701鈥?03 10.1144/jgs2011-110" target="_blank" title="It opens in new window">CrossRef
  29. Ouellette OPGB [Ed.] (1994) Histological studies of host penetration and colonization by endophytic fungi. American Phytopathological Society Press, St Paul MN
  30. Parry SF, Noble SR, Crowley QG, Wellman CH (2011) A high-precision U-Pb age constraint on the Rhynie chert Konservat-Lagerst盲tte: time scale and other implications. J Geol Soc London 168:863鈥?72 10.1144/0016-76492010-043" target="_blank" title="It opens in new window">CrossRef
  31. Parry SF, Noble SR, Crowley QG, Wellman CH (2013) Reply to Discussion on 鈥楢 high-precision U鈥揚b age constraint on the Rhynie Chert Konservat-Lagerst盲tte: time scale and other implications鈥? / Journal, Vol. 168, 863鈥?72. J Geol Soc London 170:703鈥?06 10.1144/jgs2012-089" target="_blank" title="It opens in new window">CrossRef
  32. Paulitz TC, Menge JA (1986) The effects of a mycoparasite on the mycorrhizal fungus / Glomus deserticola. Phytopathology 76:351鈥?54 10.1094/Phyto-76-351" target="_blank" title="It opens in new window">CrossRef
  33. Petitberghien P (1956) Les champignons hypog茅s de la region de Dijon. Bull sci Bourgogne 16:115鈥?55
  34. Powell CL, Trewin NH, Edwards D (2000) Palaeoecology and plant succession in a borehole through the Rhynie cherts, Lower Old Red Sandstone, Scotland. In: Friend PF, Williams BPJ (eds) New perspectives on the Old Red Sandstone (Geol Soc London Spec Publ 180). Geological Society Publishing House, Bath, UK, pp 439鈥?57
  35. Purin S, Rillig MC (2008) Parasitism of arbuscular mycorrhizal fungi: reviewing the evidence. FEMS Microbiol Lett 279:8鈥?4 10.1111/j.1574-6968.2007.01007.x" target="_blank" title="It opens in new window">CrossRef
  36. Remy W, Hass H (1996) New information on gametophytes and sporophytes of / Aglaophyton major and inferences about possible environmental adaptations. Rev Palaeobot Palynol 90:175鈥?93 10.1016/0034-6667(95)00082-8" target="_blank" title="It opens in new window">CrossRef
  37. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci U S A 91:11841鈥?1843 10.1073/pnas.91.25.11841" target="_blank" title="It opens in new window">CrossRef
  38. Rice CA, Ashcroft WA (2004) The geology of the northern half of the Rhynie basin, Aberdeenshire, Scotland. Trans Roy Soc Edinburgh Earth Sci 94:299鈥?08
  39. Rice CM, Trewin NH, Anderson LI (2002) Geological setting of the Early Devonian Rhynie cherts, Aberdeenshire, Scotland: an early terrestrial hot spring system. J Geol Soc London 159:203鈥?14 10.1144/0016-764900-181" target="_blank" title="It opens in new window">CrossRef
  40. Rousseau A, Benhamou N, Chet I, Pich茅 Y (1996) Mycoparasitism of the extramatrical phase of / Glomus intraradices by / Trichoderma harzianum. Phytopathology 86:434鈥?43 10.1094/Phyto-86-434" target="_blank" title="It opens in new window">CrossRef
  41. Strullu-Derrien C, Kenrick P, Pressel P, Duckett JG, Rioult JP, Strullu DG (2014) Fungal associations in / Horneophyton ligneri from the Rhynie Chert ( / c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant鈥揻ungus symbioses. New Phytol 203:964鈥?79 10.1111/nph.12805" target="_blank" title="It opens in new window">CrossRef
  42. Sylvia DM, Schenck NC (1983a) Germination of chlamydospores of three / Glomus species as affected by soil matric potential and fungal contamination. Mycologia 75:30鈥?5 10.2307/3792920" target="_blank" title="It opens in new window">CrossRef
  43. Sylvia DM, Schenck NC (1983b) Soil fungicides for controlling chytridiaceous mycoparasites of / Gigaspora margarita and / Glomus fasciculatum. Appl Environ Microbiol 45:1306鈥?309
  44. Taber RA (1982) / Gigaspora spores and associated hyperparasites in weed seeds in soil. Mycologia 74:1026鈥?031 10.2307/3792734" target="_blank" title="It opens in new window">CrossRef
  45. Taylor TN, Remy W, Hass H (1992) Fungi from the Lower Devonian Rhynie chert: Chytridiomycetes. Amer J Bot 79:1233鈥?241 10.2307/2445050" target="_blank" title="It opens in new window">CrossRef
  46. Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia 87:560鈥?73 10.2307/3760776" target="_blank" title="It opens in new window">CrossRef
  47. Taylor TN, Klavins SD, Krings M, Taylor EL, Kerp H, Hass H (2004) Fungi from the Rhynie chert: a view from the dark side. Trans Roy Soc Edinburgh Earth Sci 94:457鈥?73
  48. Taylor TN, Hass H, Kerp H (2005) Life history biology of early land plants: deciphering the gametophyte phase. Proc Natl Acad Sci U S A 102:5892鈥?897 10.1073/pnas.0501985102" target="_blank" title="It opens in new window">CrossRef
  49. Wakefield WS, Powell MS, Letcher PM, Barr DJS, Churchill PF (2010) A molecular phylogenetic evaluation of the Spizellomycetales. Mycologia 102:596鈥?04 10.3852/09-120" target="_blank" title="It opens in new window">CrossRef
  50. Wellman CH (2006) Spore assemblages from the Lower Devonian 鈥楲ower Old Red Sandstone鈥?deposits of the Rhynie outlier, Scotland. Trans Roy Soc Edinburgh Earth Sci 97:167鈥?11 10.1017/S0263593300001449" target="_blank" title="It opens in new window">CrossRef
  51. Wellman CH, Kerp H, Hass H (2006) Spores of the Rhynie chert plant / Aglaophyton ( / Rhynia) / major (Kidston & Lang) Edwards 1986. Rev Palaeobot Palynol 142:229鈥?50 10.1016/j.revpalbo.2006.04.009" target="_blank" title="It opens in new window">CrossRef
  52. Yao YJ, Pegler DN, Young TWK (1996) Genera of Endogonales. Royal Botanic Gardens, Kew
  
• 刊物主题：Evolutionary Biology; Developmental Biology; Microbiology; Plant Sciences; Ecology;
• 出版者：Springer Netherlands
• ISSN：1878-7665

文摘

The oldest fossil evidence of interfungal relationships comes from the Lower Devonian Rhynie chert. However, comprehensive specimens displaying consistent patterns of such associations are rare. In this paper we describe a new interfungal interaction from the Rhynie chert that occurs between two mycelial fungi within a degrading land plant axis. One of the partners (fungus 1, probably a glomeromycete) is represented by aseptate hyphae that extend through the space of what was the cortical intercellular system of the plant and produce thin-walled vesicles and/or spores. Intimately associated with fungus 1 is a second fungus (fungus 2, systematic affinities unknown) comprised of delicate, septate hyphae. Many vesicles/spores of fungus 1 are surrounded by a mantle-like hyphal investment formed by fungus 2. Because fungus 2 invades the vesicles/spores of fungus 1 and forms extensive hyphal wefts in the lumen, we interpret fungus 2 as a parasite, albeit not necessarily a pathogen, of fungus 1. This discovery contributes to our knowledge of the diversity of fungi and the intricate interfungal relationships that existed in early continental ecosystems.