Assembly of a phased diploid Candida albicans genome facilitates allele-specific measurements and provides a simple model for repeat and indel structure

Genome Biology

Volumn 14, Issue 9, 2013, Pages

  Muzzey, Dale ^a   Schwartz, Katja ^b   Weissman, Jonathan S ^a   Sherlock, Gavin ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Haplotype; Homopolymer; Indel; Microsatellite; Phasing; Repeat

Indexed keywords

ALLELE; ARTICLE; CANDIDA ALBICANS; CHROMOSOME; CONTROLLED STUDY; DIPLOIDY; FUNGAL CHROMOSOME; FUNGAL GENOME; FUNGAL STRAIN; GENE CONSTRUCT; GENE EXPRESSION; GENE POOL; HOMOZYGOSITY; INDEL MUTATION; MOLECULAR EVOLUTION; MUTATION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMORPHIC LOCUS; PROMOTER REGION; SENSITIVITY AND SPECIFICITY; SINGLE NUCLEOTIDE POLYMORPHISM; WILD TYPE; BIOLOGICAL MODEL; CHROMOSOME MAP; GENETICS; HAPLOTYPE; HETEROZYGOTE; HIGH THROUGHPUT SEQUENCING; HOMOZYGOTE;

CANDIDA ALBICANS; EUKARYOTA;

MICROSATELLITE DNA;

ALLELES; CANDIDA ALBICANS; CHROMOSOME MAPPING; CHROMOSOMES, FUNGAL; DIPLOIDY; GENOME, FUNGAL; HAPLOTYPES; HETEROZYGOTE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMOZYGOTE; INDEL MUTATION; MICROSATELLITE REPEATS; MODELS, GENETIC;

EID: 84883626672     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-9-r97     Document Type: Article

References (42)

1. Browning SR, Browning BL. Haplotype phasing: existing methods and new developments. Nat Rev Genet 2011, 12:703-714. 3217888, 21921926.
2. Lin S, Chakravarti A, Cutler DJ. Haplotype and missing data inference in nuclear families. Genome Res 2004, 14:1624-1632. 10.1101/gr.2204604, 509272, 15256514.
3. Li X, Li J. Haplotype reconstruction in large pedigrees with untyped individuals through IBD inference. J Comput Biol 2011, 18:1411-1421. 10.1089/cmb.2011.0167, 3216110, 21923410.
4. Ma L, Xiao Y, Huang H, Wang Q, Rao W, Feng Y, Zhang K, Song Q. Direct determination of molecular haplotypes by chromosome microdissection. Nat Methods 2010, 7:299-301. 10.1038/nmeth.1443, 2871314, 20305652.
5. Fan HC, Wang J, Potanina A, Quake SR. Whole-genome molecular haplotyping of single cells. Nat Biotechnol 2011, 29:51-57. 10.1038/nbt.1739, 21170043.
6. Peters BA, Kermani BG, Sparks AB, Alferov O, Hong P, Alexeev A, Jiang Y, Dahl F, Tang YT, Haas J, Robasky K, Zaranek AW, Lee J-H, Ball MP, Peterson JE, Perazich H, Yeung G, Liu J, Chen L, Kennemer MI, Pothuraju K, Konvicka K, Tsoupko-Sitnikov M, Pant KP, Ebert JC, Nilsen GB, Baccash J, Halpern AL, Church GM, Drmanac R. Accurate whole-genome sequencing and haplotyping from 10 to 20 human cells. Nature 2012, 487:190-195. 10.1038/nature11236, 3397394, 22785314.
7. Kaper F, Swamy S, Klotzle B, Munchel S, Cottrell J, Bibikova M, Chuang H-Y, Kruglyak S, Ronaghi M, Eberle MA, Fan J-B. Whole-genome haplotyping by dilution, amplification, and sequencing. Proc Natl Acad Sci U S A 2013, 110:5552-5557. 10.1073/pnas.1218696110, 3619281, 23509297.
8. Kitzman JO, Mackenzie AP, Adey A, Hiatt JB, Patwardhan RP, Sudmant PH, Ng SB, Alkan C, Qiu R, Eichler EE, Shendure J. Haplotype-resolved genome sequencing of a Gujarati Indian individual. Nat Biotechnol 2011, 29:59-63. 10.1038/nbt.1740, 3116788, 21170042.
9. Suk E-K, McEwen GK, Duitama J, Nowick K, Schulz S, Palczewski S, Schreiber S, Holloway DT, McLaughlin S, Peckham H, Lee C, Huebsch T, Hoehe MR. A comprehensively molecular haplotype-resolved genome of a European individual. Genome Res 2011, 21:1672-1685. 10.1101/gr.125047.111, 3202284, 21813624.
10. Voskoboynik A, Neff NF, Sahoo D, Newman AM, Pushkarev D, Koh W, Passarelli B, Fan HC, Mantalas GL, Palmeri KJ, Ishizuka KJ, Gissi C, Griggio F, Ben-Shlomo R, Corey DM, Penland L, White RA, Weissman IL, Quake SR. The genome sequence of the colonial chordate, Botryllus schlosseri. Elife 2013, 2:e00569. 10.7554/eLife.00569, 3699833, 23840927.
11. Bennett RJ, Johnson AD. Mating in Candida albicans and the search for a sexual cycle. Annu Rev Microbiol 2005, 59:233-255. 10.1146/annurev.micro.59.030804.121310, 15910278.
12. Bennett RJ, Johnson AD. Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J 2003, 22:2505-2515. 10.1093/emboj/cdg235, 155993, 12743044.
13. Forche A, Alby K, Schaefer D, Johnson AD, Berman J, Bennett RJ. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol 2008, 6:e110. 10.1371/journal.pbio.0060110, 2365976, 18462019.
14. Hickman MA, Zeng G, Forche A, Hirakawa MP, Abbey D, Harrison BD, Wang Y-M, Su C-H, Bennett RJ, Wang Y, Berman J. The " obligate diploid" Candida albicans forms mating-competent haploids. Nature 2013, 494:55-59. 10.1038/nature11865, 3583542, 23364695.
15. Butler G, Rasmussen MD, Lin MF, Santos MAS, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy JL, Agrafioti I, Arnaud MB, Bates S, Brown AJP, Brunke S, Costanzo MC, Fitzpatrick DA, de Groot PWJ, Harris D, Hoyer LL, Hube B, Klis FM, Kodira C, Lennard N, Logue ME, Martin R, Neiman AM, Nikolaou E, Quail MA, Quinn J, et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 2009, 459:657-662. 10.1038/nature08064, 2834264, 19465905.
16. Jones T, Federspiel NA, Chibana H, Dungan J, Kalman S, Magee BB, Newport G, Thorstenson YR, Agabian N, Magee PT, Davis RW, Scherer S. The diploid genome sequence of Candida albicans. Proc Natl Acad Sci U S A 2004, 101:7329-7334. 10.1073/pnas.0401648101, 409918, 15123810.
17. van het Hoog M, Rast TJ, Martchenko M, Grindle S, Dignard D, Hogues H, Cuomo C, Berriman M, Scherer S, Magee BB, Whiteway M, Chibana H, Nantel A, Magee PT. Assembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes. Genome Biol 2007, 8:R52. 10.1186/gb-2007-8-4-r52, 1896002, 17419877.
18. Abbey D, Hickman M, Gresham D, Berman J. High-Resolution SNP/CGH microarrays reveal the accumulation of loss of heterozygosity in commonly used Candida albicans strains. G3 (Bethesda) 2011, 1:523-530.
19. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
20. Hoyer LL. The ALS gene family of Candida albicans. Trends Microbiol 2001, 9:176-180. 10.1016/S0966-842X(01)01984-9, 11286882.
21. Bruno VM, Wang Z, Marjani SL, Euskirchen GM, Martin J, Sherlock G, Snyder M. Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res 2010, 20:1451-1458. 10.1101/gr.109553.110, 2945194, 20810668.
22. Gregg C, Zhang J, Weissbourd B, Luo S, Schroth GP, Haig D, Dulac C. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 2010, 329:643-648. 10.1126/science.1190830, 3005244, 20616232.
23. DeVeale B, van der Kooy D, Babak T. Critical evaluation of imprinted gene expression by RNA-Seq: a new perspective. PLoS Genet 2012, 8:e1002600. 10.1371/journal.pgen.1002600, 3315459, 22479196.
24. Kelsey G, Bartolomei MS. Imprinted genes .. and the number is?. PLoS Genet 2012, 8:e1002601. 10.1371/journal.pgen.1002601, 3315456, 22479197.
25. Chang Y-F, Imam JS, Wilkinson MF. The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 2007, 76:51-74. 10.1146/annurev.biochem.76.050106.093909, 17352659.
26. Segal E, Widom J. Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 2009, 19:65-71. 10.1016/j.sbi.2009.01.004, 2673466, 19208466.
27. Raveh-Sadka T, Levo M, Shabi U, Shany B, Keren L, Lotan-Pompan M, Zeevi D, Sharon E, Weinberger A, Segal E. Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast. Nat Genet 2012, 44:743-750. 10.1038/ng.2305, 22634752.
28. Zanders S, Ma X, Roychoudhury A, Hernandez RD, Demogines A, Barker B, Gu Z, Bustamante CD, Alani E. Detection of heterozygous mutations in the genome of mismatch repair defective diploid yeast using a Bayesian approach. Genetics 2010, 186:493-503. 10.1534/genetics.110.120105, 2954485, 20660644.
29. Gragg H, Harfe BD, Jinks-Robertson S. Base composition of mononucleotide runs affects DNA polymerase slippage and removal of frameshift intermediates by mismatch repair in Saccharomyces cerevisiae. Mol Cell Biol 2002, 22:8756-8762. 10.1128/MCB.22.24.8756-8762.2002, 139878, 12446792.
30. Koren A, Tsai H-J, Tirosh I, Burrack LS, Barkai N, Berman J. Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet 2010, 6:e1001068. 10.1371/journal.pgen.1001068, 2924309, 20808889.
31. Tirosh I, Reikhav S, Levy AA, Barkai N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science 2009, 324:659-662. 10.1126/science.1169766, 19407207.
32. Khan Z, Bloom JS, Amini S, Singh M, Perlman DH, Caudy AA, Kruglyak L. Quantitative measurement of allele-specific protein expression in a diploid yeast hybrid by LC-MS. Mol Syst Biol 2012, 8:602. 3435501, 22893000.
33. Zhang X, Borevitz JO. Global analysis of allele-specific expression in Arabidopsis thaliana. Genetics 2009, 182:943-954. 10.1534/genetics.109.103499, 2728882, 19474198.
34. Tran HT, Keen JD, Kricker M, Resnick MA, Gordenin DA. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol Cell Biol 1997, 17:2859-2865. 232138, 9111358.
35. Kelkar YD, Strubczewski N, Hile SE, Chiaromonte F, Eckert KA, Makova KD. What is a microsatellite: a computational and experimental definition based upon repeat mutational behavior at A/T and GT/AC repeats. Genome Biol Evol 2010, 2:620-635. 10.1093/gbe/evq046, 2940325, 20668018.
36. Kelkar YD, Tyekucheva S, Chiaromonte F, Makova KD. The genome-wide determinants of human and chimpanzee microsatellite evolution. Genome Res 2008, 18:30-38. 2134767, 18032720.
37. Lang GI, Murray AW. Estimating the per-base-pair mutation rate in the yeast Saccharomyces cerevisiae. Genetics 2008, 178:67-82. 10.1534/genetics.107.071506, 2206112, 18202359.
38. Legrand M, Forche A, Selmecki A, Chan C, Kirkpatrick DT, Berman J. Haplotype mapping of a diploid non-meiotic organism using existing and induced aneuploidies. PLoS Genet 2008, 4:e1. 10.1371/journal.pgen.0040001, 2174976, 18179283.
39. Schwartz K, Wenger JW, Dunn B, Sherlock G. APJ1 and GRE3 homologs work in concert to allow growth in xylose in a natural Saccharomyces sensu stricto hybrid yeast. Genetics 2012, 191:621-632. 10.1534/genetics.112.140053, 3374322, 22426884.
40. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760. 10.1093/bioinformatics/btp324, 2705234, 19451168.
41. Peltz SW, Brown AH, Jacobson A. mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans-acting factor. Genes Dev 1993, 7:1737-1754. 10.1101/gad.7.9.1737, 8370523.
42. Viterbi A. Error bounds for convolutional codes and an asymptotically optimum decoding algorithm. Information Theory 1967, 13:260-269.