Dyneins

From Purdue Genomics Database Facility

12 March 2008

Cross section of a flagellum showing the typical 9 (outer doublet) +2 (inner) arrangement of microtubules, modified from http://www.ncbi.nlm.nih.gov/books/bv.fcgi?rid=mcb.figgrp.5481.

There are 7 dynein genes in Selaginella moellendorffii, 8 in Physcomitrella, and 14 in Chlamydomonas (Wickstead and Gull, 2007). As expected, there are none in angiosperms, which lack flagellated sperm. Six of the Selaginella loci have two alleles; the best allelic variant is noted in the model notes (these dynein genes are big and a couple of them probably have errors).

Interestingly, Selaginella and Physcomitrella lack the outer dynein arm genes (i.e., OAD alpha and beta), and do not have the cytoplasmic dynein genes DYNC1H1 abd DYNC2H1. Chlamydomonas has three of these four genes (DYNC1H1 is missing in Chlamydomonas).

Note (Marek Elias, 28.6.2008): Both Selaginella and Physcomitrella lack also light intermediate chains of the two cytoplasmic dyneins (DYNC1IL1 and DYNC2LI1), whereas Chlamydomonas retains the light intermediate chain of the cytoplasmic dynein 2 (DYNC2LI1, Chlre3 ID 130394, GenBank AAO12154.1). Selaginella, Physco and Chlamy have the inner dynein arm genes (IAD3-5) and IADalpha and beta. Naming of the dynein genes is based on Wickstead and Gall (2007). I thought having no outer dynein arms was a novel finding until I read a 1985 paper titled "Widespread absence of outer dynein arms in the spermatozoids of lower plants" by Hyams and Campbell (1985). In this paper the authors show that the flagella of Marsilea, Pteridium, Lygodium, Anemia, Equisteum--all ferns--and the liverwort Marchantia have inner but no outer dynein arms. In looking at micrographs of Selaginella krausianna sperm from Renzaglia et al. (1999), outer dynein arms are also absent in Selaginella.

The significance of not having outer dynein arms is not clear. Hyams speculated that the lack of outer arms could affect the beat/waveform of the flagella as well as reduce beat frequency (Hyams and Campbell, 1985). Such changes could help the sperm find and swim through the neck of the archegonium--an unnecessary task for Chlamy.

When did plants lose the outer dynein arm? A study of Nitella spermatogenesis by Turner (1968) shows EMs of the sperm flagella. Turner noted that the dynein arms were missing, but said "This apparent lack of arms may be due to inadequate preservation under the particular conditions of fixation employed". It appears that the outer dynein arms were lost before (during?) the evolution of the Charales, or, put another way, before plants colonized land.

The only seed plants that have flagellated sperm are Ginko and cycads. In looking at micrographs of Ginko (Li et al., 1989) and Zamia (Norstog, 1967) flagella, these also appear to lack the outer dynein arm.

One trend in the evolution of flagellated plant sperm is the increase in number of flagella per sperm. Selaginella and Lycopodium sperm have 2 flagella, ferns have hundreds while Zamia can have 12,000 flagella. Why/how seed plants lost all flagella is unknown, but an interesting question.

Other reasons why these genes/proteins might be interesting:

1) Assuming that these flagella proteins are only needed for a specific cell type, it will be very interesting to see if/how these genes are co-regulated (do they have common cis-acting elements?). Swimming sperm can be obtained from S. moellendorffii shortly after adding microspores to water so this can be tested.

2) Are these proteins only involved in sperm movement? Do they have roles in the sporophyte? Can they serve as MTOCs during cell division (probably not, as cytoplasmic dyneins are absent in Selaginella)?

OTHER FLAGELLA PROTEINS

The flagella genes absent in Physco and Selmo and angiosperms yet present in Chlamydomonas and human are listed, as are the conserved flagella genes (most are single copy) that are present only in organisms having cilia or flagella. This list was generated by using all of the Chlamydomonas flagella genes identified by proteomics (Pazour et al. 2005) to query the Physcomitrella and Selaginella JGI databases, and the nr database. In this case, I was interested in finding all of the genes that were present in organisms having flagella and absent in the angiosperms

Flagella genes missing in Selmo, Physco and angiosperms but present in Chlamy and human: IFT20 IFT72/74 IFT81 IFT139 IFT140 IFT144 BBS4

Also in this category (Marek Elias, 28.6.2008): ARL6 (=BBS3), IFT27 (=RABL4 in human, under the name FAP156 in Pazour et al.)

Present in Chlamy, Physco, Selmo, human; absent in angiosperms: DIP13 FAP118 FAP155 FAP167/IFT80 FAP184 FAP189 FAP198 FAP22/quilin FAP250 FAP253 FAP267 FAP32 FAP50 FAP57 FAP61 FAP65 FAP66 FAP73 FAP80/IFT122A HP3 HY3 hyp protein IA1-IC140 IA-IC28 IFT139 IFT140 IFT52 IFT121/IFT1A IFT172A IFT57/CPC1 IFT88 IQCA1 IQCA2 Parkin PF16/SPAG6 RIB72 RSP3 RSP4 RSP6 RSP9 TCTEX2b/FAP2

Also in this category (Marek Elias, 28.6.2008): ARL3 (under the name ARLC2 in Pazour et al.) = Selmo1 ID 449874 (449879), Phypa1 ID 225335

Note (Marek Elias, 28.6.2008): Other proteins not found in the study by Pazour et al. but known to be flagellar from other studies should be checked, too! For example:

- all subunits of the BBSome (see Nachury et al., Cell 2007, 129:1201-1213), including BBS1, BBS2, BBS4 (already noted by Jody), BBS5, BBS7, BBS8, amd BBS9, seem missing from both Selaginella and Physcomitrella (as well as angiosperms)

REFERENCES:

Hyams JS, Campbell CJ (1985) Widespread absence of outer dynein arms in the spermatozoids of lower plants. Cell Biology International Reports 9: 841-848

Li Y, Wang FH, Knox RB (1989) Ultrastructural analysis of the flagellar apparatus in sperm cells of Ginko biloba. Protoplasma 149: 57-63

Norstog K (1967) Fine sturcture of the spermatozoid of Zamia with special reference to the flagellar apparatus. Amer. J. Bot. 54: 831-840

Pazour GJ, Agrin N, Leszyk J, Witman GB. (2005). Proteomic analysis of a eukaryotic cilium. J Cell Biol. 170:103-113.

Renzaglia KS, Bernhard DL, Garbary DJ (1999) Developmental ultrastructure of the male gamete of Selaginella. Int. J. Plant Sci. 160

Turner FR (1968) An ultrastructural study of plant spermatogenesis. Spermatogenesis in Nitella. J. Cell Biol. 37:370-393

Wickstead B, Gull K (2007) Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8: 1708-1721