Evolution of Nematode-trapping Cells of Predatory Fungi of the Orbiliaceae Based on Evidence from RRNA-encoding DNA and Multiprotein Sequences

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2007 May 15

PMID 17494736

Citations 69

Authors

Ying Yang

Ence Yang

Zhiqiang An

Xingzhong Liu

Affiliations

Soon will be listed here.

Abstract

Among fungi, the basic life strategies are saprophytism, parasitism, and predation. Fungi in Orbiliaceae (Ascomycota) prey on animals by means of specialized trapping structures. Five types of trapping devices are recognized, but their evolutionary origins and divergence are not well understood. Based on comprehensive phylogenetic analysis of nucleotide sequences of three protein-coding genes (RNA polymerase II subunit gene, rpb2; elongation factor 1-alpha gene, ef1-alpha; and ss tubulin gene, bt) and ribosomal DNA in the internal transcribed spacer region, we have demonstrated that the initial trapping structure evolved along two lineages yielding two distinct trapping mechanisms: one developed into constricting rings and the other developed into adhesive traps. Among adhesive trapping devices, the adhesive network separated from the others early and evolved at a steady and gentle speed. The adhesive knob evolved through stalk elongation, with a final development of nonconstricting rings. Our data suggest that the derived adhesive traps are at a highly differentiated stage. The development of trapping devices is felicitous proof of adaptive evolution.

Citing Articles

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References

Heckman D, Geiser D, Eidell B, STAUFFER R, Kardos N, Hedges S . Molecular evidence for the early colonization of land by fungi and plants. Science. 2001; 293(5532):1129-33. DOI: 10.1126/science.1061457. View

Padovan A, Sanson G, Brunstein A, Briones M . Fungi evolution revisited: application of the penalized likelihood method to a Bayesian fungal phylogeny provides a new perspective on phylogenetic relationships and divergence dates of Ascomycota groups. J Mol Evol. 2005; 60(6):726-35. DOI: 10.1007/s00239-004-0164-y. View

ODonnell K, Kistler H, Cigelnik E, Ploetz R . Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci U S A. 1998; 95(5):2044-9. PMC: 19243. DOI: 10.1073/pnas.95.5.2044. View

Berbee M, Carmean D, Winka K . Ribosomal DNA and resolution of branching order among the ascomycota: how many nucleotides are enough?. Mol Phylogenet Evol. 2001; 17(3):337-44. DOI: 10.1006/mpev.2000.0835. View

PRAMER D . NEMATODE- TRAPPING FUNGI. AN INTRIGUING GROUP OF CARNIVOROUS PLANTS INHABIT THE MICROBIAL WORLD. Science. 1964; 144(3617):382-8. DOI: 10.1126/science.144.3617.382. View

Douzery E, Snell E, Bapteste E, Delsuc F, Philippe H . The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?. Proc Natl Acad Sci U S A. 2004; 101(43):15386-91. PMC: 524432. DOI: 10.1073/pnas.0403984101. View

Liu Y, Hall B . Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Natl Acad Sci U S A. 2004; 101(13):4507-12. PMC: 384777. DOI: 10.1073/pnas.0400938101. View

Glass N, Donaldson G . Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol. 1995; 61(4):1323-30. PMC: 167388. DOI: 10.1128/aem.61.4.1323-1330.1995. View

Posada D, Crandall K . MODELTEST: testing the model of DNA substitution. Bioinformatics. 1999; 14(9):817-8. DOI: 10.1093/bioinformatics/14.9.817. View

10.

Higgins M, PRAMER D . Fungal Morphogenesis: Ring Formation and Closure by Arthrobotrys dactyloides. Science. 1967; 155(3760):345-6. DOI: 10.1126/science.155.3760.345. View

11.

PRAMER D, STOLL N . Nemin: a morphogenic substance causing trap formation by predaceous fungi. Science. 1959; 129(3354):966-7. DOI: 10.1126/science.129.3354.966. View

12.

Sanderson M . Molecular data from 27 proteins do not support a Precambrian origin of land plants. Am J Bot. 2011; 90(6):954-6. DOI: 10.3732/ajb.90.6.954. View

13.

Liu Y, Whelen S, Hall B . Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol. 1999; 16(12):1799-808. DOI: 10.1093/oxfordjournals.molbev.a026092. View

14.

Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D . The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1998; 25(24):4876-82. PMC: 147148. DOI: 10.1093/nar/25.24.4876. View

15.

Hibbett D, Binder M . Evolution of complex fruiting-body morphologies in homobasidiomycetes. Proc Biol Sci. 2002; 269(1504):1963-9. PMC: 1691125. DOI: 10.1098/rspb.2002.2123. View

16.

Ahren D, Ursing B, Tunlid A . Phylogeny of nematode-trapping fungi based on 18S rDNA sequences. FEMS Microbiol Lett. 1998; 158(2):179-84. DOI: 10.1111/j.1574-6968.1998.tb12817.x. View

17.

Li Y, Hyde K, Jeewon R, Cai L, Vijaykrishna D, Zhang K . Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes. Mycologia. 2006; 97(5):1034-46. DOI: 10.3852/mycologia.97.5.1034. View

18.

Maddison W, Maddison D . Interactive analysis of phylogeny and character evolution using the computer program MacClade. Folia Primatol (Basel). 1989; 53(1-4):190-202. DOI: 10.1159/000156416. View