Dyneins Across Eukaryotes: A Comparative Genomic Analysis

Abstract

Dyneins are large minus‐end‐directed microtubule motors. Each dynein contains at least one dynein heavy chain (DHC) and a variable number of intermediate chains (IC), light intermediate chains (LIC) and light chains (LC). Here, we used genome sequence data from 24 diverse eukaryotes to assess the distribution of DHCs, ICs, LICs and LCs across Eukaryota. Phylogenetic inference identified nine DHC families (two cytoplasmic and seven axonemal) and six IC families (one cytoplasmic). We confirm that dyneins have been lost from higher plants and show that this is most likely because of a single loss of cytoplasmic dynein 1 from the ancestor of Rhodophyta and Viridiplantae, followed by lineage‐specific losses of other families. Independent losses in Entamoeba mean that at least three extant eukaryotic lineages are entirely devoid of dyneins. Cytoplasmic dynein 2 is associated with intraflagellar transport (IFT), but in two chromalveolate organisms, we find an IFT footprint without the retrograde motor. The distribution of one family of outer‐arm dyneins accounts for 2‐headed or 3‐headed outer‐arm ultrastructures observed in different organisms. One diatom species builds motile axonemes without any inner‐arm dyneins (IAD), and the unexpected conservation of IAD I1 in non‐flagellate algae and LC8 (DYNLL1/2) in all lineages reveals a surprising fluidity to dynein function.

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References 95

1. 1.

   Hirokawa N, Noda Y, Okada Y. Kinesin and dynein superfamily proteins in organelle transport and cell division. Curr Opin Cell Biol. 1998;10:60-73.

   Not in our library10.1016/s0955-0674(98)80087-2

2. 2.

   Gibbons IR. The role of dynein in microtubule-based motility. Cell Struct Funct. 1996;21:331-342.

   Not in our library10.1247/csf.21.331

3. 3.

   Holzbaur ELF, Vallee RB. Dyneins: molecular structure and cellular function. Annu Rev Cell Biol. 1994;10:339-372.

   Not in our library10.1146/annurev.cb.10.110194.002011

4. 4.

   Kon T, Nishiura M, Ohkura R, Toyoshima YY, Sutoh K. Distinct functions of nucleotide-binding/hydrolysis sites in the four AAA modules of cytoplasmic dynein. Biochemistry. 2004;43:11266-11274.

   Not in our library10.1021/bi048985a

5. 5.

   Gibbons IR, LeeEiford A, Mocz G, Phillipson CA, Tang WJY, Gibbons BH. Photosensitized cleavage of dynein heavy chains: cleavage at the V1 site by irradiation at 365nm in the presence of ATP and vanadate. J Biol Chem. 1987;262:2780-2786.

   Not in our library

6. 6.

   Oiwa K, Sakakibara H. Recent progress in dynein structure and mechanism. Curr Opin Cell Biol. 2005;17:98-103.

   Not in our library10.1016/j.ceb.2004.12.006

7. 7.

   Koonce MP, Samso M. Of rings and levers: the dynein motor comes of age. Trends Cell Biol. 2004;14:612-619.

   Not in our library10.1016/j.tcb.2004.09.013

8. 8.

   King SM, Schliwa M. Dynein motors: structure, mechanochemistry and regulation. Molecular Motors. 2002;45-78.

   Not in our library

9. 9.

   Simpson AGB, Roger AJ. The real ‘kingdoms’ of eukaryotes. Curr Biol. 2004;14:R693-R696.

   Not in our library10.1016/j.cub.2004.08.038

10. 10.

    Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409:860-921.

    Not in our library10.1038/35057062

11. 11.

    Aparicio S, Chapman J, Stupka E, Putnam N, Chia J, Dehal P, Christoffels A, Rash S, Hoon S, Smit A, Gelpke MDS, Roach J, Oh T, Ho IY, Wong M, et al. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science. 2002;297:1301-1310.

    Not in our library10.1126/science.1072104

12. 12.

    Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, et al. The genome sequence of Drosophila melanogaster. Science. 2000;287:2185-2195.

    Not in our library10.1126/science.287.5461.2185

13. 13.

    Genome sequence of the nematode C. elegans: a platform for investigating biology. Science. 1998;282:2012-2018.

    Not in our library10.1126/science.282.5396.2012

14. 14.

    Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, et al. Life with 6000 genes. Science. 1996;274:546-567.

    Not in our library10.1126/science.274.5287.546

15. 15.

    Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, Sgouros J, Peat N, Hayles J, Baker S, Basham D, Bowman S, Brooks K, Brown D, Brown S, et al. The genome sequence of Schizosaccharomyces pombe. Nature. 2002;415:871-880.

    Not in our library10.1038/nature724

16. 16.

    Loftus B, Anderson I, Davies R, Alsmark UCM, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, et al. The genome of the protist parasite Entamoeba histolytica. Nature. 2005;433:865-868.

    Not in our library10.1038/nature03291

17. 17.

    Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, et al. The genome of the social amoeba Dictyostelium discoideum. Nature. 2005;435:43-57.

    Not in our library10.1038/nature03481

18. 18.

    Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Bohme W, Hannick L, Aslett MA, Shallom J, Marcello L, et al. The genome of the African trypanosome Trypanosoma brucei. Science. 2005;309:416-422.

    Not in our library10.1126/science.1112642

19. 19.

    Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, Anupama A, Apostolou Z, Attipoe P, Bason N, Bauser C, et al. The genome of the kinetoplastid parasite Leishmania major. Science. 2005;309:436-442.

    Not in our library10.1126/science.1112680

20. 20.
    Macronuclear Genome Sequence of the Ciliate Tetrahymena thermophila, a Model Eukaryote · 2006

    No notice
21. 21.

    Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science. 2004;306:79-86.

    Not in our library10.1126/science.1101156

22. 22.

    Tyler BM, Tripathy S, Zhang XM, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CMB, Dorrance AE, Dou DL, Dickerman AW, et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science. 2006;313:1261-1266.

    Not in our library10.1126/science.1128796

23. 23.

    Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 2002;419:498-511.

    Not in our library10.1038/nature01097

24. 24.

    Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng MQ, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, et al. Complete genome sequence of the apicomplexan Cryptosporidium parvum. Science. 2004;304:441-445.

    Not in our library10.1126/science.1094786

25. 25.

    Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, et al. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature. 2004;428:653-657.

    Not in our library10.1038/nature02398

26. 26.

    Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408:796-815.

    Not in our library10.1038/35048692

27. 27.

    Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, et al. The genome of black cottonwood, Populus trichocarpa. Science. 2006;313:1596-1604.

    Not in our library10.1126/science.1128691

28. 28.

    Yu J, Hu SN, Wang J, Wong GKS, Li SG, Liu B, Deng YJ, Dai L, Zhou Y, Zhang XQ, Cao ML, Liu J, Sun JD, Tang JB, Chen YJ, et al. A draft sequence of the rice genome (Oryza sativa L. ssp indica). Science. 2002;296:79-92.

    Not in our library10.1126/science.1068037

29. 29.

    Asai DJ, Wilkes DE. The dynein heavy chain family. J Euk Microbiol. 2004;51:23-29.

    Not in our library10.1111/j.1550-7408.2004.tb00157.x

30. 30.

    Morris RL, Hoffman MP, Obar RA, McCafferty SS, Gibbons IR, Leone AD, Cool J, Allgood EL, Musante AM, Judkins KM, Rossetti BJ, Rawson AP, Burgess DR. Analysis of cytoskeletal and motility proteins in the sea urchin genome assembly. Dev Biol. 2006;300:219-237.

    Not in our library10.1016/j.ydbio.2006.08.052

31. 31.

    Ogawa K, Kamiya R, Wilkerson CG, Witman GB. Interspecies conservation of outer arm dynein intermediate chain sequences defines two intermediate chain subclasses. Mol Biol Cell. 1995;6:685-696.

    Not in our library10.1091/mbc.6.6.685

32. 32.

    Wilkerson CG, King SM, Koutoulis A, Pazour GJ, Witman GB. The 78,000 Mr intermediate chain of Chlamydomonas outer arm dynein is a WD-repeat protein required for arm assembly. J Cell Biol. 1995;129:169-178.

    Not in our library10.1083/jcb.129.1.169

33. 33.

    Takada S, Kamiya R. Reconstitution of Chlamydomonas outer dynein arms from alpha-beta-subunit and gamma-subunit: requirement of a 3rd factor. J Cell Biol. 1994;126:737-745.

    Not in our library10.1083/jcb.126.3.737

34. 34.

    Mitchell DR, Kang Y. Reversion analysis of dynein intermediate chain function. J Cell Sci. 1993;105:1069-1078.

    Not in our library10.1242/jcs.105.4.1069

35. 35.

    Mitchell DR, Kang Y. Identification of oda6 as a Chlamydomonas dynein mutant by rescue with the wild-type gene. J Cell Biol. 1991;113:835-842.

    Not in our library10.1083/jcb.113.4.835

36. 36.

    Hendrickson TW, Perrone CA, Griffin P, Wuichet K, Mueller J, Yang PF, Porter ME, Sale WS. IC138 is a WD-repeat dynein intermediate chain required for light chain assembly and regulation of flagellar bending. Mol Biol Cell. 2004;15:5431-5442.

    Not in our library10.1091/mbc.e04-08-0694

37. 37.

    Perrone CA, Yang PF, O’Toole E, Sale WS, Porter ME. The Chlamydomonas IDA7 locus encodes a 140-kDa dynein intermediate chain required to assemble the I1 inner arm complex. Mol Biol Cell. 1998;9:3351-3365.

    Not in our library10.1091/mbc.9.12.3351

38. 38.

    Yang P, Sale WS. Cloning and characterization of the 140 kD intermediate chain gene of inner dynein arm I1 in Chlamydomonas. Mol Biol Cell. 1996;7:3305-3305.

    Not in our library

39. 39.

    DiBella LM, Gorbatyuk O, Sakato M, Wakabayashi K, Patel-King RS, Pazour GJ, Witman GB, King SM. Differential light chain assembly influences outer arm dynein motor function. Mol Biol Cell. 2005;16:5661-5674.

    Not in our library10.1091/mbc.e05-08-0732

40. 40.

    Lawrence CJ, Morris NR, Meagher RB, Dawe RK. Dyneins have run their course in plant lineage. Traffic. 2001;2:362-363.

    Not in our library10.1034/j.1600-0854.2001.25020508.x

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