Innovation and constraint leading to complex multicellularity in the Ascomycota

Nature Communications

Volumn 8, Issue , 2017, Pages

  Nguyen, Tu Anh ^a   Cissé, Ousmane H ^b   Yun Wong, Jie ^a   Zheng, Peng ^a   Hewitt, David ^c   Nowrousian, Minou ^d   Stajich, Jason E ^b   Jedd, Gregory ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ACADEMY OF NATURAL SCIENCES OF DREXEL UNIVERSITY   (United States)

^d RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIVERGENCE; EVOLUTION; GENE EXPRESSION; GENOME; GENOMICS; INNOVATION; PHYLOGENETICS; YEAST;

BUDDING; CELL ORGANELLE; FISSION YEAST; FUNCTIONAL GENOMICS; GENETIC VARIABILITY; GENOME; MACHINE; PEZIZOMYCOTINA; ASCOMYCETES; BIODIVERSITY; BIOLOGY; CYTOLOGY; FUNGAL GENOME; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; PHYSIOLOGY; SEQUENCE ALIGNMENT; TRANSPORT AT THE CELLULAR LEVEL; WHOLE GENOME SEQUENCING;

ANIMALIA; ASCOMYCOTA; FUNGI; NEOLECTA; NEOLECTA IRREGULARIS; PEZIZOMYCOTINA; SCHIZOSACCHAROMYCETACEAE;

FUNGAL DNA; FUNGAL PROTEIN;

ASCOMYCOTA; BIODIVERSITY; BIOLOGICAL TRANSPORT; COMPUTATIONAL BIOLOGY; DNA, FUNGAL; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENOME, FUNGAL; PHYLOGENY; SEQUENCE ALIGNMENT; WHOLE GENOME SEQUENCING;

EID: 85011967259     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14444     Document Type: Article

References (88)

1. King, N. The unicellular ancestry of animal development. Dev. Cell 7, 313-325 (2004).
2. Rokas, A. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 42, 235-251 (2008).
3. Knoll, A. H. The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci. 39, 217-239 (2011).
4. Nichols, S. a, Dirks, W., Pearse, J. S. & King, N. Early evolution of animal cell signaling and adhesion genes. Proc. Natl Acad. Sci. U. S. A. 103, 12451-12456 (2006).
5. Segawa, Y. et al. Functional development of Src tyrosine kinases during evolution from a unicellular ancestor to multicellular animals. Proc. Natl Acad. Sci. USA 103, 12021-12026 (2006).
6. Adamska, M., Matus, D. Q., Adamski, M., Rokhsar, D. S. & Martindale, M. Q. The evolutionary origin of hedgehog proteins. Curr. Biol. 17, 836-837 (2007).
7. King, N. et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783-788 (2008).
8. Sebé-Pedrós, A., De Mendoza, A., Lang, B. F., Degnan, B. M. & Ruiz-Trillo, I. Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol. Biol. Evol. 28, 1241-1254 (2011).
9. Fairclough, S. R. et al. Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol. 14, R15 (2013).
10. de Mendoza, A. et al. Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages. Proc. Natl Acad. Sci. USA 110, E4858-E4866 (2013).
11. Suga, H. et al. The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat. Commun. 4, 2325 (2013).
12. Anderson, D. P. et al. Evolution of an ancient protein function involved in organized multicellularity in animals. Elife 5, e10147 (2016).
13. Tanabe, Y. et al. Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc. Natl Acad. Sci. USA 102, 2436-2441 (2005).
14. Floyd, S. K. & Bowman, J. L. The ancestral developmental tool kit of land plants. Int. J. Plant Sci. Spec. Issue Discern. Homol. Gene Expr. 168, 1-35 (2007).
15. Lee, J. H., Lin, H., Joo, S. & Goodenough, U. Early sexual origins of homeoprotein heterodimerization and evolution of the plant KNOX/BELL family. Cell 133, 829-840 (2008).
16. Rensing, S. A. et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69 (2008).
17. Hori, K. et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5, 3978 (2014).
18. Bloemendal, S. et al. A homologue of the human STRIPAK complex controls sexual development in fungi. Mol. Microbiol. 84, 310-323 (2012).
19. Bayram, Ö. et al. VelB / VeA / LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320, 1504-1506 (2008).
20. Teichert, I., Nowrousian, M., PÖggeler, S. & Kück, U. in Advances in Genetics. (eds Friedmann, T., Dunlap, J. C. & Goodwin, S. F. ) 87, 199-244 (Elsevier, 2014).
21. Balus?ka, F., Volkmann, D. & Barlow, P. W. Cell-Cell Channels (Springer Science & Business Media, 2007).
22. Jedd, G. Fungal evo-devo: organelles and multicellular complexity. Trends Cell Biol. 21, 12-19 (2011).
23. Jedd, G. & Chua, N. H. A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat. Cell Biol. 2, 226-231 (2000).
24. Lai, J. et al. Intrinsically disordered proteins aggregate at fungal cell-to-cell channels and regulate intercellular connectivity. Proc. Natl Acad. Sci. 109, 15781-15786 (2012).
25. Trinci, A. P. J. & Collinge, A. J. Structure and plugging of septa of wild type and spreading colonial mutants of Neurospora crassa. Arch. Mikrobiol. 91, 355-364 (1973).
26. Kimbrough, J. W. in Septal Ultrastructure and Ascomycete Systematics, 127-141 (New York Plenum Press, 1994).
27. van Peer, A. F. et al. The septal pore cap is an organelle that functions in vegetative growth and mushroom formation of the wood-rot fungus Schizophyllum commune. Environ. Microbiol. 12, 833-844 (2010).
28. Sudbery, P. E. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9, 737-748 (2011).
29. Furuya, K. & Niki, H. The DNA damage checkpoint regulates a transition between yeast and hyphal growth in Schizosaccharomyces japonicus. Mol. Cell Biol. 30, 2909-2917 (2010).
30. Kramer, C. L. Morphological development and nuclear behavior in the genus Taphrina. Mycologia 52, 295-320 (1960).
31. Redhead, S. A. The genus Neolecta (Neolectaceae fam. nov., Lecanorales, Ascomycetes) in Canada. Can. J. Bot. 55, 301-306 (1977).
32. Landvik, S., Eriksson, O. E. & Berbee, M. L. Neolecta: a fungal dinosaur? Evidence from b-tubulin amino acid sequences. Mycologia 93, 1151-1163 (2001).
33. Sugiyama, J., Hosaka, K. & Suh, S. Early diverging Ascomycota: phylogenetic divergence and related evolutionary enigmas. Mycologia 98, 996-1005 (2006).
34. Healy, R. A., Kumar, T. K. A., Hewitt, D. A. & McLaughlin, D. J. Functional and phylogenetic implications of septal pore ultrastructure in the ascoma of Neolecta vitellina. Mycologia 105, 802-813 (2013).
35. Parra, G., Bradnam, K. & Korf, I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061-1067 (2007).
36. Arvas, M. et al. Comparison of protein coding gene contents of the fungal phyla Pezizomycotina and Saccharomycotina. BMC Genomics 8, 325 (2007).
37. Liu, F. et al. Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J. Cell Biol. 180, 325-339 (2008).
38. Ng, S. K., Liu, F., Lai, J., Low, W. & Jedd, G. A tether for Woronin body inheritance is associated with evolutionary variation in organelle positioning. PLoS Genet. 5, e1000521 (2009).
39. PÖggeler, S., Nowrousian, M. & Kück, U. in The Mycota: A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research (eds Kües, U. & Fischer, R. ) 325-348 (Springer Science & Business Media, 2006).
40. Pandey, A., Roca, M. G., Read, N. D. & Glass, N. L. Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot. Cell 3, 348-358 (2004).
41. Flei-ner, A. et al. The so locus is required for vegetative cell fusion and postfertilization events in Neurospora crassa. Eukaryot. Cell 4, 920-930 (2005).
42. Engh, I. et al. The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies. Eukaryot. Cell 6, 831-843 (2007).
43. Idnurm, A., Verma, S. & Corrochano, L. M. A glimpse into the basis of vision in the kingdom Mycota. Fungal Genet. Biol. 47, 881-892 (2010).
44. Blackstone, N. W. Redox control and the evolution of multicellularity. Bioessays 22, 947-953 (2000).
45. Sebé-Pedrós, A., Grau-Bové, X., Richards, T. A. & Ruiz-Trillo, I. Evolution and classification of myosins, a paneukaryotic whole-genome approach. Genome Biol. Evol. 6, 290-305 (2014).
46. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
47. Eddy, S. R. Profile hidden Markov models. Bioinformatics 14, 755-763 (1998).
48. Vallee, R. B., McKenney, R. J. & Ori-McKenney, K. M. Multiple modes of cytoplasmic dynein regulation. Nat. Cell Biol. 14, 224-230 (2012).
49. Heider, M. R. & Munson, M. Exorcising the exocyst complex. Traffic 13, 898-907 (2012).
50. Feyder, S., De Craene, J.-O., Bär, S., Bertazzi, D. & Friant, S. Membrane trafficking in the yeast Saccharomyces cerevisiae model. Int. J. Mol. Sci. 0067, 1509-1525 (2015).
51. Culver-Hanlon, T. L., Lex, S. a, Stephens, A. D., Quintyne, N. J. & King, S. J. A microtubule-binding domain in dynactin increases dynein processivity by skating along microtubules. Nat. Cell Biol. 8, 264-270 (2006).
52. Yao, X., Zhang, J., Zhou, H., Wang, E. & Xiang, X. In vivo roles of the basic domain of dynactin p150 in microtubule plus-end tracking and dynein function. Traffic 13, 375-387 (2012).
53. Kardon, J. R., Reck-Peterson, S. L. & Vale, R. D. Regulation of the processivity and intracellular localization of Saccharomyces cerevisiae dynein by dynactin. Proc. Natl Acad. Sci. USA 106, 5669-5674 (2009).
54. Kiel, J. A. K. W., Veenhuis, M. & van der Klei, I. J. PEX genes in fungal genomes: common, rare or redundant. Traffic 7, 1291-1303 (2006).
55. Schmidt, F. et al. Insights into peroxisome function from the structure of PEX3 in complex with a soluble fragment of PEX19. J. Biol. Chem. 285, 25410-25417 (2010).
56. Schueller, N. et al. The peroxisomal receptor Pex19p forms a helical mPTS recognition domain. EMBO J. 29, 2491-2500 (2010).
57. Chen, Y. et al. Hydrophobic handoff for direct delivery of peroxisome tailanchored proteins. Nat. Commun. 5, 5790 (2014).
58. Yagita, Y., Hiromasa, T. & Fujiki, Y. Tail-anchored PEX26 targets peroxisomes via a PEX19-dependent and TRC40-independent class I pathway. J. Cell Biol. 200, 651-666 (2013).
59. Lam, S. K., Yoda, N. & Schekman, R. A vesicle carrier that mediates peroxisome protein traffic from the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 107, 21523-21528 (2010).
60. Schossig, A. et al. Mutations in ROGDI cause Kohlschütter-TÖnz syndrome. Am. J. Hum. Genet. 90, 701-707 (2012).
61. Page, L. J., Sowerby, P. J., Lui, W. W. Y. & Robinson, M. S. g-Synergin: an EH domain-containing protein that interacts with g-adaptin. J. Cell Biol. 146, 993-1004 (1999).
62. Küssel-Andermann, P. et al. Vezatin, a novel transmembrane protein, bridges myosin VIIA to the cadherin-catenins complex. EMBO J. 19, 6020-6029 (2000).
63. Yao, X., Arst, H. N., Wang, X. & Xiang, X. Discovery of a vezatin-like protein for dynein-mediated early endosome transport. Mol. Biol. Cell 26, 3816-3827 (2015).
64. Riquelme, M. & Sanchez-Leon, E. The Spitzenkorper: a choreographer of fungal growth and morphogenesis. Curr. Opin. Microbiol. 20, 27-33 (2014).
65. Peraza-Reyes, L. & Berteaux-Lecellier, V. Peroxisomes and sexual development in fungi. Front. Physiol. 4, 244 (2013).
66. Nyathi, Y. & Baker, A. Plant peroxisomes as a source of signalling molecules. Biochim. Biophys. Acta-Mol. Cell Res. 1763, 1478-1495 (2006).
67. Dixit, E. et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141, 668-681 (2010).
68. Pagliarini, D. J. et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123 (2008).
69. Nagy, L. G. et al. Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts. Nat. Commun. 5, 4471 (2014).
70. Stern, D. L. The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751-764 (2013).
71. Banks, J. A. et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960-963 (2011).
72. Sanderfoot, A. Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol. 144, 6-17 (2007).
73. Kloepper, T. H., Kienle, C. N. & Fasshauer, D. SNAREing the basis of multicellularity: consequences of protein family expansion during evolution. Mol. Biol. Evol. 25, 2055-2068 (2008).
74. Grove, S. N. & Bracker, C. E. Protoplasmic organization of hyphal tips among fungi: vesicles and Spitzenkorper. J. Bacteriol. 104, 989-1009 (1970).
75. Priebe, S., Linde, J., Albrecht, D., Guthke, R. & Brakhage, A. A. FungiFun: a web-based application for functional categorization of fungal genes and proteins. Fungal Genet. Biol. 48, 353-358 (2011).
76. Hofmann, K. & Stoffel, W. TMbase: a database of membrane spanning protein segments. Biol. Chem. 374, 166 (1993).
77. Gould, S. J., Keller, G. A., Hosken, N., Wilkinson, J. & Subramani, S. A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108, 1657-1664 (1989).
78. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
79. Capella-Gutiérrez, S., Silla-Martnez, J. M. & Gabaldón, T. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973 (2009).
80. Guindon, S. et al. New algorithms and methods to estimate maximumlikelihood phylogenies: assessing the performance of PhyML 3. 0. Syst. Biol. 59, 307-321 (2010).
81. Henikoff, S. & Henikoff, J. G. Amino acid substitution matrices from protein blocks. Proc. Natl Acad. Sci. USA 89, 10915-10919 (1992).
82. Savitzky, A. & Golay, M. J. E. Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 36, 1627-1639 (1964).
83. Colot, H. V et al. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl Acad. Sci. USA 103, 10352-10357 (2006).
84. Lai, J. et al. Marker fusion tagging, a new method for production of chromosomally encoded fusion proteins. Eukaryot. Cell 9, 827-830 2010
85. Margolin, B. S., Freitag, M. & Selker, E. U. Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa by electroporation. Fungal Genet. Newsl. 44, 34-36 (1997).
86. Lacaze, I., Lalucque, H., Siegmund, U., Silar, P. & Brun, S. Identification of NoxD/Pro41 as the homologue of the p22phox NADPH oxidase subunit in fungi. Mol. Microbiol. 95, 1006-1024 (2015).
87. Urnavicius, L. et al. The structure of the dynactin complex and its interaction with dynein. Science 347, 1441-1446 (2015).
88. Kyte, J. & Doolittle, R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132 (1982).