Does the Mode of Plastid Inheritance Influence Plastid Genome Architecture?

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Crosby, Kate ^a   Smith, David Roy ^b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PLASTID DNA; UNCLASSIFIED DRUG;

APICOMPLEXA; ARTICLE; DNA STRUCTURE; EXTRACHROMOSOMAL INHERITANCE; GENOME SIZE; GREEN ALGA; INHERITANCE; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASTID GENOME; RED ALGA; SPECIES DIFFERENCE; STRAMENOPILE; TAXONOMY; UNINDEXED SEQUENCE;

APICOMPLEXA; BIOLOGICAL EVOLUTION; CHLOROPHYTA; DNA, PLANT; DNA, PROTOZOAN; GENOME SIZE; GENOME, PLASTID; INHERITANCE PATTERNS; PHYLOGENY; PLANTS; PLASTIDS; RHODOPHYTA; STRAMENOPILES;

EID: 84866935331     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046260     Document Type: Article

References (93)

1. Palmer JD, (2003) The symbiotic birth and spread of plastids: how many times and whodunit? Journal of Phycology 39: 4-12.
2. Keeling PJ, (2004) Diversity and evolutionary history of plastids and their hosts. Am J Bot 91: 1481-1493 doi:10.3732/ajb.91.10.1481.
3. Archibald JM, (2009) The Puzzle of Plastid Evolution. Current Biology 19: R81-R88 doi:10.1016/j.cub.2008.11.067.
4. Green BR, (2011) Chloroplast genomes of photosynthetic eukaryotes. The Plant Journal 66: 34-44 doi:10.1111/j.1365-313X.2011.04541.x.
5. Lynch M (2007) The Origins of Genome Architecture. Sunderland, MA: Sinauer Associates.
6. Lynch M, Conery JS, (2003) The origins of genome complexity. Science 302: 1401-1404 doi:10.1126/science.1089370.
7. Moens P, Gregory TR, Witt JDS, (2008) Population size and genome size in fishes: a closer look. Génome 51: 309-313 doi:10.1139/G08-003.
8. Whitney KD, Garland T, (2010) Did Genetic Drift Drive Increases in Genome Complexity? PLoS Genet 6: e1001080 doi:10.1371/journal.pgen.1001080.t001.
9. Birky CW Jr, (2001) The inheritance of genes in mitcohondria and chloroplast: Laws, Mechanisms, and Models. Annu Rev Genet 35: 125-148 doi:10.1146/annurev.genet.35.102401.090231.
10. Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am J Bot: 1443-1458.
11. Harris SA, Ingram R (1991) Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon: 393-412.
12. Reboud X, Zeyl C, (1994) Organelle inheritance in plants. Heredity 72: 132-140 doi:10.1038/hdy.1994.19.
13. Zimmermann J, Jahn R, Gemeinholzer B, (2011) Barcoding diatoms: evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols. Org Divers Evol 11: 173-192 doi:10.1007/s13127-011-0050-6.
14. Latta RG, Mitton JB, (1997) A comparison of population differentiation across four classes of gene marker in limber pine (Pinus flexilis James). Genetics 146: 1153-1163.
15. Hansen AK, Escobar LK, Gilbert LE, Jansen RK, (2007) Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies. Am J Bot 94: 42-46 doi:10.3732/ajb.94.1.42.
16. Felsenstein J, (1985) Phylogenies and the Comparative Methods. Am Nat 125: 1-15.
17. Garland T Jr, Harvey P, Ives A (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology.
18. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, (2009) GenBank. Nucl Acids Res 37: D26-D31 doi:10.1093/nar/gkn723.
19. Sayers EW, Barrett T, Benson DA, Bryant SH, Canese K, et al. (2009) Database resources of the National Center for Biotechnology Information. Nucl Acids Res 37: D5-D15 doi:10.1093/nar/gkn741.
20. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, et al. (2011) Geneious v5.4. Available:http://www.geneious.com/.
21. Purvis A, Rambaut A, (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput Appl Biosci 11: 247-251.
22. Orme D (2011) The caper package: comparative analysis of phylogenetics and evolution in R.
23. Fritz S, Purvis A, (2010) Selectivity in Mammalian Extinction Risk and Threat Types: a New Measure of Phylogenetic Signal Strength in Binary Traits. Conservation Biology 24: 1042-1051 doi:10.1111/j.1523-1739.2010.01455.x.
24. Lynch M, Koskella B, Schaack S, (2006) Mutation Pressure and the Evolution of Organelle Genomic Architecture. Science 311: 1727-1730 doi:10.1126/science.1118884.
25. Frankham R, Lees K, Montgomery ME, England PR, Lowe EH, et al. (1999) Do population size bottlenecks reduce evolutionary potential? Animal Conservation 2: 255-260.
26. Baack EJ, Whitney KD, Rieseberg LH, (2005) Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytol 167: 623-630 doi:10.1111/j.1469-8137.2005.01433.x.
27. Chumley TW, (2006) The Complete Chloroplast Genome Sequence of Pelargonium×hortorum: Organization and Evolution of the Largest and Most Highly Rearranged Chloroplast Genome of Land Plants. Molecular Biology and Evolution 23: 2175-2190 doi:10.1093/molbev/msl089.
28. Cosmides LM, Tooby J, (1981) Cytoplasmic inheritance and intragenomic conflict. J Theor Biol 89: 83-129.
29. Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, et al. (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci USA 91: 9794-9798.
30. Braukmann TWA, Kuzmina M, Stefanović S, (2009) Loss of all plastid ndh genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny. Curr Genet 55: 323-337 doi:10.1007/s00294-009-0249-7.
31. Zhong B, Yonezawa T, Zhong Y, Hasegawa M, (2010) The Position of Gnetales among Seed Plants: Overcoming Pitfalls of Chloroplast Phylogenomics. Molecular Biology and Evolution 27: 2855-2863 doi:10.1093/molbev/msq170.
32. Carmichael JS, Friedman WE, (1995) Double Fertilization in Gnetum gnemon: The Relationship between the Cell Cycle and Sexual Reproduction. Plant Cell 7: 1975-1988 doi:10.1105/tpc.7.12.1975.
33. Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot: 383-404.
34. Whittle C-A, Johnston MO, (2002) Male-driven evolution of mitochondrial and chloroplastidial DNA sequences in plants. Molecular Biology and Evolution 19: 938-949.
35. Whittle C-A, Johnston MO, (2003) Male-biased transmission of deleterious mutations to the progeny in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 4055-4059 doi:10.1073/pnas.0730639100.
36. Whittle C-A, Malik MR, Krochko JE, (2007) Gender-specific selection on codon usage in plant genomes. BMC Genomics 8: 169 doi:10.1186/1471-2164-8-169.
37. Kumari M, Clarke HJ, Francs-Small des CC, Small I, Khan TN, et al. (2011) Albinism does not correlate with biparental inheritance of plastid DNA in interspecific hybrids in Cicer species. Plant Science 180: 628-633 doi:10.1016/j.plantsci.2011.01.003.
38. Peters AF, Scornet D, Müller DG, Kloareg B, Cock JM, (2004) Inheritance of organelles in artificial hybrids of the isogamous multicellular chromist alga Ectocarpus siliculosus(Phaeophyceae). European Journal of Phycology 39: 235-242 doi:10.1080/09670260410001683241.
39. Motomura T, Nagasato C, Kimura K, (2010) Cytoplasmic inheritance of organelles in brown algae. J Plant Res 123: 185-192 doi:10.1007/s10265-010-0313-x.
40. Renzaglia K, Dengate S, Schmitt S, Duckett J, (2002) Novel features of Equisetum arvense spermatozoids: insights into pteridophyte evolution. New Phytol 154: 159-174.
41. Zanmin H, Shiyi H, Jinzhong Z (1996) Paternal inheritance of plastid DNA in genus Pharbitis. Acta Botanica Sinica 38.
42. Hu Z-M, Hu S-Y (1995) Study on organelle DNA within the generative cell and sperm cells in Pharbitis. Acta Botanica Sinica: 1-6.
43. Matsushima R, Hu Y, Toyoda K, Sodmergen, Sakamoto W, (2008) The Model Plant Medicago truncatula Exhibits Biparental Plastid Inheritance. Plant and Cell Physiology 49: 81-91 doi:10.1093/pcp/pcm170.
44. Corriveau JL, Coleman AW, (1990) Plastid inheritance in Oenothera: paternal input may influence transmission patterns. Curr Genet 17: 327-330.
45. Baur E, (1909) Das Wesen und die Erblichkeit sver- haltnisse der "Varietates albomarginatae hort" von Pelargonium zonale. Z Indukt Abstammungs-Ver- erbungsl 1: 330-351.
46. Schmit V, Jardin P, Baudoin J, Debouck D, (1993) Use of chloroplast DNA polymorphisms for the phylogenetic study of seven Phaseolus taxa including P. vulgaris and P. coccineus. TAG Theoretical and Applied Genetics 87: 506-516.
47. Corriveau JL, Polans NO, Coleman AW, (1989) Cultivar variability for the presence of plastid DNA in pollen of Pisum sativum L.: implications for plastid transmission. Curr Genet 16: 47-51.
48. Bogdanova VS, Galieva ER, Kosterin OE, (2008) Genetic analysis of nuclear-cytoplasmic incompatibility in pea associated with cytoplasm of an accession of wild subspecies Pisum sativum subsp. elatius (Bieb.) Schmahl. Theoret Appl Genetics 118: 801-809 doi:10.1007/s00122-008-0940-y.
49. Bogdanova VS, Galieva ER, Yadrikhinskiy AK, Kosterin OE (2012) Inheritance and genetic mapping of two nuclear genes involved in nuclear-cytoplasmic incompatibility in peas (Pisum sativum L.). Theoret Appl Genetics. doi:10.1007/s00122-012-1804-z.
50. Renzaglia KS, Johnson TH, Gates HD, Whittier DP, (2001) Architecture of the sperm cell of Psilotum. Am J Bot 88: 1151-1163.
51. Renzaglia KS, Bernhard DL, Garbary DJ, (1999) Developmental Ultrastructure of the Male Gamete of Selaginella. Int J Plant Sci 160: 14-28 doi:10.1086/314103.
52. Zhang Q, Liu Y, (2003) Sodmergen (2003) Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant and Cell Physiology 44: 941-951.
53. Ruf S, Hermann M, Berger IJ, Carrer H, Bock R, (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat Biotechnol 19: 870-875 doi:10.1038/nbt0901-870.
54. Azhagiri AK, Maliga P, (2007) Exceptional paternal inheritance of plastids in Arabidopsis suggests that low-frequency leakage of plastids via pollen may be universal in plants. The Plant Journal 52: 817-823 doi:10.1111/j.1365-313X.2007.03278.x.
55. Kuroiwa T, Hori T, (1986) Preferential digestion of male chloroplast nuclei and mitochondrial nuclei during gametogenesis of Bryopsis maxima Okamura. Protoplasma 133: 85-87 doi:10.1007/BF01293191.
56. Droogenbroeck B, Maertens I, Haegeman A, Kyndt T, O'Brien C, et al. (2005) Maternal inheritance of cytoplasmic organelles in intergeneric hybrids of Carica papaya L. and Vasconcellea spp. (Caricaceae Dumort., Brassicales). Euphytica 143: 161-168 doi:10.1007/s10681-005-3156-0.
57. Sun GH, Uyeda TQP, Kuroiwa T, (1988) Destruction of organelle nuclei during spermatogenesis in Chara corallina examined by staining with DAPI and anti-DNA antibody. Protoplasma 144: 185-188.
58. Gastony GJ, Yatskievych G (1992) Maternal inheritance of the chloroplast and mitochondrial genomes in cheilanthoid ferns. Am J Bot: 716-722.
59. Havey M, McCreight J, Rhodes B, Taurick G, (1998) Differential transmission of the Cucumis organellar genomes. TAG Theoretical and Applied Genetics 97: 122-128.
60. Zhong Z-R, Li N, Qian D, Jin J-H, Chen T, (2011) Maternal inheritance of plastids and mitochondria in Cycas L. (Cycadaceae). Mol Genet Genomics 286: 411-416 doi:10.1007/s00438-011-0653-9.
61. Boblenz K, Nothnagel T, Metzlaff M, (1990) Paternal inheritance of plastids in the genus Daucus. Molecular and General Genetics 220: 489-491.
62. Vivek BS, Ngo QA, Simon PW, (1999) Evidence for maternal inheritance of the chloroplast genome in cultivated carrot (Daucus carota L. ssp. sativus). Theoret Appl Genetics 98: 669-672 doi:10.1007/s001220051119.
63. Ferguson DJP, Campbell SA, Henriquez FL, Phan L, Mui E, et al. (2007) Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in Eimeria tenella. Int J Parasitol 37: 33-51 doi:10.1016/j.ijpara.2006.10.003.
64. McKinnon GE, Vaillancourt RE, Tilyard PA, Potts BM, (2001) Maternal inheritance of the chloroplast genome in Eucalyptus globulus and interspecific hybrids. Genome 44: 831-835 doi:10.1139/gen-44-5-831.
65. Reinhard A, Reavey P, Lin J, Zhang H, (2009) Chloroplast DNA inheritance, ancestry, and sequencing in Fragaria. Acta Horticulturae 859: 221-228.
66. Brawley SH, Wetherbee R, Quatrano RS, (1976) Fine-structural studies of the gametes and embryo of Fucus vesiculosus L. (Phaeophyta). II. The cytoplasm of the egg and young zygote. J Cell Sci 20: 255-271.
67. Lee C, (1955) Fertilization in Ginkgo biloba. Botanical Gazette 117: 79-100.
68. Kumar S, Dhingra A, Daniell H, (2004) Stable transformation of the cotton plastid genome and maternal inheritance of transgenes. Plant Mol Biol 56: 203-216 doi:10.1007/s11103-004-2907-y.
69. Bouzon Z, Miguens F (2000) Male gametogenesis in the red algae Gracilaria and Gracilariopsis (Rhodophyta, Gracilariales). Cryptogamie Algologie 21.
70. Wills DM, Hester ML, Liu A, Burke JM, (2005) Chloroplast SSR polymorphisms in the Compositae and the mode of organellar inheritance in Helianthus annuus. Theoret Appl Genetics 110: 941-947 doi:10.1007/s00122-004-1914-3.
71. Mogensen H, Rusche ML, (1985) Quantitative ultrastructural analysis of barley sperm. Protoplasma 128: 1-13.
72. Mogensen HL, (1988) Exclusion of male mitochondria and plastids during syngamy in barley as a basis for maternal inheritance. Proc Natl Acad Sci USA 85: 2594-2597.
73. Pacini E, Taylor P, Singh M, Knox R, (1992) Development of plastids in pollen and tapetum of rye-grass, Lolium perenne L. Annals of Botany. 70: 179-188.
74. Huang CY, Ayliffe MA, Timmis JN, (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422: 72-76 doi:10.1038/nature01435.
75. Amane M, Lumaret R, Hany V, Ouazzani N, Debain C, et al. (1999) Chloroplast-DNA variation in cultivated and wild olive (Olea europaea L.). TAG Theoretical and Applied Genetics 99: 133-139.
76. Caha C, Lee DJ, Martínez-Reyna J, Vogel K, (2001) Meiotic stability, chloroplast DNA polymorphisms, and morphological traits of upland× lowland switchgrass reciprocal hybrids. Crop Science 41: 1579-1583.
77. Mejnartowicz M, (1991) Inheritance of chloroplast DNA in Populus. TAG Theoretical and Applied Genetics 82: 477-480.
78. Niwa K, Kobiyama A, (2010) Interspecific hybridization in the haploid blade-forming marine crop Porphyra (Bangiales, Rhodophyta): occurrence of allopolyploidy in surviving F1 gametophytic blades. Journal of Phycology 46: 693-702.
79. Olson MS, McCauley DE, (2000) Linkage disequilibrium and phylogenetic congruence between chloroplast and mitochondrial haplotypes in Silene vulgaris. Proceedings of the Royal Society B: Biological Sciences 267: 1801-1808 doi:10.1098/rspb.2000.1213.
80. Ferguson DJP, Henriquez FL, Kirisits MJ, Muench SP, Prigge ST, et al. (2005) Maternal inheritance and stage-specific variation of the apicoplast in Toxoplasma gondii during development in the intermediate and definitive host. Eukaryotic Cell 4: 814-826 doi:10.1128/EC.4.4.814-826.2005.
81. Adams CR, Stamer KA, Miller JK, McNally JG, Kirk MM, et al. (1990) Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet 18: 141-153.
82. Conde MF, Pring D, Levings C III, (1979) Maternal inheritance of organelle DNA's in Zea mays-Zea perennis reciprocal crosses. Journal of Heredity 70: 2-4.
83. Chen J, Tauer C, Huang Y, (2002) Paternal chloroplast inheritance patterns in pine hybrids detected with trnL-trnF intergenic region polymorphism. Theoret Appl Genetics 104: 1307-1311 doi:10.1007/s00122-002-0893-5.
84. Guo F, Hu S-Y, Yuan Z, Zee S-Y, Han Y, (2005) Paternal cytoplasmic transmission in Chinese pine (Pinus tabulaeformis). Protoplasma 225: 5-14 doi:10.1007/s00709-005-0088-4.
85. Neale DB, Wheeler NC, Allard RW (1986) Paternal inheritance of chloroplast DNA in Douglas-fir. http://dxdoiorg/101139/x86-205.
86. Neale D, Sederoff R, (1989) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. TAG Theoretical and Applied Genetics 77: 212-216.
87. Dong J, Wagner D, Yanchuk A, Carlson M, Magnussen S, et al. (1992) Paternal chloroplast DNA inheritance in Pinus consora and Pinus banksiana: independence of parenetal species or cross direction. Journal of Heredity 83: 419-422.
88. Ohba K, Iwakawa M, Okada Y, Murai M, (1971) Paternal transmission of a plastid anomaly in some reciprocal crosses of Sugi, Cryptomeria japonica D. Don. Silvae Genet 20: 101-107.
89. Szmidt AE, Aldén T, Hällgren JE, (1987) Paternal inheritance of chloroplast DNA in Larix. Plant Mol Biol 9: 59-64.
90. Sutton BCS, Flanagan DJ, Gawley JR, Newton CH, Lester DT, et al. (1991) Inheritance of chloroplast and mitochondrial DNA in Picea and composition of hybrids from introgression zones. Theoret Appl Genetics 82. doi:10.1007/BF00226220.
91. Lee RW, Jones RF, (1973) Induction of Mendelian and non-Mendelian streptomycin resistant mutants during the synchronous cell cycle of Chlamydomonas reinhardtii. Molecular and General Genetics 121: 99-108.
92. Suda S, Watanabe MM, Inouye I, (2004) Electron microscopy of sexual reproduction in Nephroselmis olivacea (Prasinophyceae, Chlorophyta). Phycological Res 52: 273-283 doi:10.1111/j.1440-183.2004.00346.x.
93. Miyamura S, (2010) Cytoplasmic inheritance in green algae: patterns, mechanisms and relation to sex type. J Plant Res 123: 171-184 doi:10.1007/s10265-010-0309-6.