The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation

American Journal of Botany

Volumn 99, Issue 9, 2012, Pages 1513-1523

  Barrett, Craig F ^a,b   Davis, Jerrold I ^a  

^a Department of Obstetrics Gynecology   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Corallorhiza striata; Deletion; Evolution; Molecular; Negative; Next generation sequencing; Orchidaceae; Pseudogene; Purifying; Selection

Indexed keywords

AUTOTROPHY; DEGRADATION; GENOME; HETEROTROPHY; MOLECULAR ANALYSIS; MONOCOTYLEDON; MUTATION; PHOTOSYNTHESIS; PLASTID; SELECTION; TAXONOMY;

AMINO ACID SUBSTITUTION; ARTICLE; GENE DELETION; GENETICS; HETEROTROPHY; ORCHIDACEAE; PLANT GENE; PLASTID GENOME; PSEUDOGENE;

AMINO ACID SUBSTITUTION; GENE DELETION; GENES, PLANT; GENOME, PLASTID; HETEROTROPHIC PROCESSES; ORCHIDACEAE; PSEUDOGENES;

CORALLORHIZA; CORALLORRHIZA STRIATA; MAGNOLIOPHYTA; ONCIDIUM; ORCHIDACEAE;

EID: 84866127282     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1200256     Document Type: Article

References (82)

1. ALLEN, J. F., W. B. M. DE PAULA, S. PUTHIYAVEETIL, and J. NIELD. 2011. A structural phylogenetic map for chloroplast photosynthesis. Trends in Plant Science 16: 645-655.
2. BARBROOK, A. C., C. J. HOWE, and S. PURTON. 2006. Why are plastid genomes retained in non-photosynthetic organisms? Trends in Plant Science 11: 101-108.
3. BARRETT, C. F., J. I. DAVIS, J. Leebens-Mack, J. G. CONRAN, and D. W. STEVENSON. In press. Plastid genomes and deep support among the commelinid monocot angiosperms. Cladistics.
4. BARRETT, C. F., and J. V. FREUDENSTEIN. 2008. Molecular evolution of rbcL in the mycoheterotrophic coralroot orchids (Corallorhiza Gagnebin, Orchidaceae). Molecular Phylogenetics and Evolution 47: 665-679.
5. BARRETT, C. F., and J. V. FREUDENSTEIN. 2009. Patterns of morphological and plastid DNA variation in the Corallorhiza striata species complex (Orchidaceae). Systematic Botany 34: 496-504.
6. BARRETT, C. F., and J. V. FREUDENSTEIN. 2011. An integrative approach to delimiting species in a rare but widespread mycoheterotrophic orchid. Molecular Ecology 20: 2771-2786.
7. BARRETT, C. F., J. V. FREUDENSTEIN, D. L. TAYLOR, and U. KÕLJALG. 2010. Rangewide analysis of fungal associations in the fully mycoheterotrophic Corallorhiza striata complex (Orchidaceae) reveals extreme specificity on ectomycorrhizal Tomentella (Thelephoraceae) across North America. American Journal of Botany 97: 628-643.
8. BIDARTONDO, M. I. 2005. The evolutionary ecology of myco-heterotrophy. New Phytologist 167: 335-352.
9. BLAZIER, J. C., M. M. GUISINGER, and R. K. JANSEN. 2011. Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae). Plant Molecular Biology 76: 263-272.
10. BRAUKMANN, T. W. A., M. KUZMINA, and S. STEFANOVIĆ. 2009. Loss of all plastid ndh genes in Gnetales and conifers: Extent and evolutionary significance for the seed plant phylogeny. Current Genetics 55: 323-337.
11. BRAUKMANN, T. W. A., and S. STEFANOVIĆ. 2012. Plastid genome evolution in mycoheterotrophic Ericaceae. Plant Molecular Biology 79: 5-20.
12. BUNGARD, R. A. 2004. Photosynthetic evolution in parasitic plants: Insight from the chloroplast genome. BioEssays 26: 235-247.
13. CAMERON, D. D., K. PREISS, G. GEBAUER, and D. J. READ. 2009. The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytologist 183: 358-364.
14. CAMERON, K. M., M. W. CHASE, and P. J. RUDALL. 2003. Recircumscription of the monocotyledonous family Petrosaviaceae to include Japonolirion. Brittonia 55: 214-225.
15. CHANG, C. C., H. C. LIN, I. P. LIN, T. Y. CHOW, H. H. CHEN, W. H. CHEN, C. H. CHENG, ET AL. 2006. The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): Comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Molecular Biology and Evolution 23: 279-291.
16. CLARKE, A. K., T. M. MACDONALD, and L. L. E. SJÖGREN. 2005. The ATPdependent Clp protease in chloroplasts of higher plants. Physiologia Plantarum 123: 406-412.
17. COLWELL, A. E. 1994. Genome evolution in a non-photosynthetic plant, Conopholis americana. Ph.D. dissertation, Washington University, St. Louis, Missouri, USA.
18. CONANT, G. C., and K. H. WOLFE. 2008. GenomeVx: Simple web-based creation of editable circular chromosome maps. Bioinformatics 24: 861-862.
19. CONRAN, J. G., J. M. BANNISTER, and D. E. LEE. 2009. Earliest orchid macrofossils: Early Miocene Dendrobium and Earina (Orchidaceae: Epidendroideae) from New Zealand. American Journal of Botany 96: 466-474.
20. DELANNOY, E., S. FUJII, C. COLAS DES Francs-Small, M. BRUNDRETT, and I. SMALL. 2011. Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Molecular Biology and Evolution 28: 2077-2086.
21. DELAVAULT, P. M., N. M. RUSSO, N. A. LUSSON, and P. A. THATOUARN. 1996. Organization of the reduced plastid genome of Lathraea clandestina, an achlorophyllous parasitic plant. Physiologia Plantarum 96: 674-682.
22. DEPAMPHILIS, C. W., and J. D. PALMER. 1990. Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348: 337-339.
23. DOWNIE, S. R., D. S. Katz-Downie, K. H. W OLFE, P. J. CALIE, and J. D. PALMER. 1994. Structure and evolution of the largest chloroplast gene (ORF2280): Internal plasticity and multiple gene loss during angiosperm evolution. Current Genetics 25: 367-378.
24. DRESCHER, A., S. RUF, T. CALSA, H. CARRER, and R. BOCK. 2000. The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant Journal 22: 97-104.
25. EDGAR, R. C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797.
26. FREUDENSTEIN, J. V., and C. F. BARRETT. 2010. Mycoheterotrophy and diversity in Orchidaceae. In Diversity, phylogeny and evolution in the monocotyledons, the proceedings of the Fourth International Conference on Monocot Systematics, 25-37. Aarhus University Press, Copenhagen, Denmark.
27. FREUDENSTEIN, J. V., and J. J. DOYLE. 1994. Character transformation and relationships in Corallorhiza (Orchidaceae, Epidendroideae). 1. Plastid DNA. American Journal of Botany 81: 1449-1457.
28. FREUDENSTEIN, J. V., and D. M. S ENYO. 2008. Relationships and evolution of matK in a group of leafless orchids (Corallorhiza and Corallorhizinae; Orchidaceae: Epidendroideae). American Journal of Botany 95: 498-505.
29. FUNK, H. T., S. BERG, K. KRUPINSKA, U. G. MAIER, and K. KRAUSE. 2007. Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biology 7: 45.
30. Gandolfo, M. A., K. C. NIXON, and W. L. CREPET. 2002. Triuridaceae fossil flowers from the Upper Cretaceous of New Jersey. American Journal of Botany 89: 1940-1957.
31. GIVNISH, T. J., M. A MES, J. R. M CNEAL, M. R. M CKAIN, P. R. STEELE, C. W. DEPAMPHILIS, S. W. GRAHAM, ET AL. 2010. Assembling the tree of the monocotyledons: Plastome sequence phylogeny and evolution of poales. Annals of the Missouri Botanical Garden 97: 584-616.
32. GOLDMAN, D. H., J. V. FREUDENSTEIN, P. J. KORES, M. MOLVRAY, D. C. JARRELL, W. M. WHITTEN, K. M. CAMERON, and M. W. CHASE. 2001. Phylogenetics of Arethuseae (Orchidaceae) based on plastid matK and rbcL sequences. Systematic Botany 26: 670-695.
33. HAJDUKIEWICZ, P. T. J., L. A. ALLISON, and P. MALIGA. 1997. The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. European Molecular Biology Organization Journal 16: 4041-4048.
34. ILES, W. J. D., S. Y. SMITH, and S. W. GRAHAM. In press. A well-supported phylogenetic framework for the monocot order Alismatales reveals multiple losses of the plastid NADH dehydrogenase complex and a strong long-branch effect. In P. Wilkin and S. J. Mayo [eds.], Early events in monocot evolution, Systematics Association special volume. Cambridge University Press, Cambridge, UK.
35. KORES, P. J., P. WESTON, M. MOLVRAY, and M. W. CHASE. 2000. Phylogenetic relationships within Diurideae: Inferences from plastid matK DNA sequences. In K. L. Wilson and D. A. Morrison [eds.], Monocots: Systematics and evolution, 449-456. CSIRO Publishing, Collingwood, Victoria, Australia.
36. KRAUSE, K. 2008. From chloroplasts to "cryptic" plastids: Evolution of plastid genomes in parasitic plants. Current Genetics 54: 111-121.
37. KURODA, H., and P. MALIGA. 2003. The plastid clpP1 protease gene is essential for plant development. Nature 425: 86-89.
38. LEAKE, J. R. 1994. The biology of myco-heterotrophic (saprophytic) plants. New Phytologist 127: 171-216.
39. LEMAIRE, B., S. HUYSMANS, E. SMETS, and V. MERCKX. 2011. Rate accelerations in nuclear 18S rDNA of mycoheterotrophic and parasitic angiosperms. Journal of Plant Research 124: 561-576.
40. LIERE, K., and G. LINK. 1995. RNA binding activity of the matK protein encoded by the chloroplast trnK intron from mustard (Sinapis alba). Nucleic Acids Research 23: 917-921.
41. LOGACHEVA, M. D., M. I. SCHELKUNOV, and A. A. PENIN. 2011. Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biology and Evolution 3: 1296-1303.
42. LÖYTYNOJA, A., and N. G OLDMAN. 2010. webPRANK: A phylogenyaware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics 11: 579.
43. MACHADO, M. A., and K. ZETSCHE. 1990. A structural, functional and molecular analysis of plastids of the holoparasites Cuscuta reflexa and Cuscuta europaea. Planta 181: 91-96.
44. MADDISON, W. P., and D. R. MADDISON. 2007. Mesquite: A modular system for evolutionary analysis, version 2.0. Website http://mesquiteproject.org.
45. MARTIN, M., and B. SABATER. 2010. Plastid ndh genes in plant evolution. Plant Physiology and Biochemistry 48: 636-645.
46. MCNEAL, J. R., K. ARUMUGUNATHAN, J. V. KUEHL, J. L. BOORE, and C. W. DEPAMPHILIS. 2007. Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae). BMC Biology 5: 55.
47. MERCKX, V., M. I. BIDARTONDO, and N. A. HYNSON. 2009. Mycoheterotrophy: When fungi host plants. Annals of Botany 104: 1255-1261.
48. MERCKX, V., and J. V. FREUDENSTEIN. 2010. Evolution of mycoheterotrophy in plants: A phylogenetic perspective. New Phytologist 185: 605-609.
49. MEYERS, S. C., A. LISTON, and R. MEINKE. 2012. An evaluation of putative sympatric speciation within Limnanthes (Limnanthaceae). PLoS ONE 7: e36480.
50. MILNE, I., M. BAYER, L. CARDLE, P. SHAW, G. STEPHEN, F. WRIGHT, and D. MARSHALL. 2010. Tablet-next generation sequence assembly visualization. Bioinformatics 26: 401-402.
51. MOHR, G., P. S. PERLMAN, and A. M. LAMBOWITZ. 1993. Evolutionary relationships among group-II intron-encoded proteins and identification of a conserved domain that may be related to maturase function. Nucleic Acids Research 21: 4991-4997.
52. MONTFORT, C., and E. KÜSTERS. 1940. Saprophytismus und photosythese. I. Biochemische physiologische studien an humus-orchideen. Botanisces Archiv 40: 571-633.
53. NEI, M., and T. GOJOBORI. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Molecular Biology and Evolution 3: 418-426.
54. NEI, M., and S. KUMAR. 2000. Molecular evolution and phylogenetics. Oxford University Press, New York, New York, USA.
55. NEUHAUS, H. E., and M. J. EMES. 2000. Nonphotosynthetic metabolism in plastids. Annual Review of Plant Physiology and Plant Molecular Biology 51: 111-140.
56. NICKRENT, D. L., O. Y. YAN, R. J. DUFF, and C. W. DEPAMPHILIS. 1997. Do nonasterid holoparasitic flowering plants have plastid genomes? Plant Molecular Biology 34: 717-729.
57. OVCHARENKO, I., G. G. LOOTS, B. M. GIARDINE, M. M. HOU, J. MA, R. C. HARDISON, L. STUBBS, ET AL. 2005. Mulan: Multiple-sequence local alignment and visualization for studying function and evolution. Genome Research 15: 184-194.
58. PARKS, M., R. CRONN, and A. LISTON. 2009. Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes. BMC Biology 7: doi:10.1186/1741-7007-7-84
59. RAMÍREZ, S. R., B. GRAVENDEEL, R. B. SINGER, C. R. MARSHALL, and N. E. PIERCE. 2007. Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448: 1042-1045.
60. RASMUSSEN, H. N. 1995. Terrestrial orchids: From seed to mycotrophic plant. Cambridge University Press, Cambridge, UK.
61. RATAN, A. 2009. Assembly algorithms for next-generation sequence data. Ph.D. dissertation, Pennsylvania State University, University Park, Pennsylvania, USA.
62. STEELE, P. R., and J. C. PIRES. 2011. Biodiversity assessment: State-of-the-art techniques in phylogenomics and species identification. American Journal of Botany 98: 415-425.
63. STEELE, P. R., K. L. HERTWECK, D. MAYFIELD, M. R. MCKAIN, J. LEEBENSMACK, and J. C. PIRES. 2012. Quality and quantity of data recovered from massively parallel sequencing: Examples in Asparagales and Poaceae. American Journal of Botany 99: 330-348.
64. STRAUB, S. C. K., M. FISHBEIN, T. LIVSHULTZ, Z. FOSTER, M. PARKS, K. WEITEMIER, R. C. CRONN, ET AL. 2011. Building a model: Developing genomic resources for common milkweed (Asclepias syriaca) with low coverage genome sequencing. BMC Genomics 12: 211.
65. STRAUB, S. C. K., M. P ARKS, K. W EITEMIER, M. F ISHBEIN, R. C. CRONN, and A. LISTON. 2012. Navigating the tip of the genomic iceberg: Next-generation sequencing for plant systematics. American Journal of Botany 99: 349-364.
66. TAJIMA, F. 1993. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135: 599-607.
67. TAMURA, K., D. PETERSON, N. PETERSON, G. STECHER, M. NEI, and S. KUMAR. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
68. TAYLOR, D. L. 1997. The evolution of mycoheterotrophy and specificity in some North American orchids. Ph.D. dissertation, University of California-Berkeley, Berkeley, California, USA.
69. TAYLOR, D. L., and T. D. BRUNS. 1997. Independent, specialized invasions of ectomycorrhizal mutualism by two nonphotosynthetic orchids. Proceedings of the National Academy of Sciences, USA 94: 4510-4515.
70. TAYLOR, D. L., T. D. BRUNS, and S. A. HODGES. 2004. Evidence for mycorrhizal races in a cheating orchid. Proceedings of Royal Society, B, Biological Sciences 271: 35-43.
71. TAYLOR, D. L., T. D. BRUNS, J. R. LEAKE, and D. J. READ. 2002. Mycorrhizal specificity and function in myco-heterotrophic plants. In M. van der Heijden and I. Sanders [eds.], The ecology of mycorrhizas, vol. 157, 375-414. Springer, Berlin, Germany.
72. VAIDYA, G., D. J. LOHMAN, and R. MEIER. 2011. SequenceMatrix: Concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27: 171-180.
73. WHITTEN, W. M., N. H. WILLIAMS, and M. W. CHASE. 2000. Subtribal and generic relationship of Maxillarieae (Orchidaceae) with emphasis on Stanhopeinae: Combined molecular evidence. American Journal of Botany 87: 1842-1856.
74. WICKE, S., G. M. S CHNEEWEISS, C. W. D EPAMPHILIS, K. F. MULLER, and D. Quandt. 2011. The evolution of the plastid chromosome in land plants: Gene content, gene order, gene function. Plant Molecular Biology 76: 273-297.
75. WICKETT, N. J., Y. ZHANG, S. K. HANSEN, J. M. ROPER, J. V. KUEHL, S. A. PLOCK, P. G. WOLF, ET AL. 2008. Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Molecular Biology and Evolution 25: 393-401.
76. WIMPEE, C. F., R. L. WROBEL, and D. K. GARVIN. 1991. A divergent plastid genome in Conopholis americana, an achlorophyllous parasitic plant. Plant Molecular Biology 17: 161-166.
77. WOLFE, K. H., C. W. MORDEN, and J. D. PALMER. 1992. Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proceedings of the National Academy of Sciences, USA 89: 10648-10652.
78. WU, F. H., M. T. CHAN, D. C. LIAO, C. T. HSU, Y. W. LEE, H. DANIELL, M. R. DUVALL, ET AL. 2010. Complete chloroplast genome of Oncidium Gower Ramsey and evaluation of molecular markers for identification and breeding in Oncidiinae. BMC Plant Biology 10: 68.
79. WYMAN, S. K., R. K. JANSEN, and J. L. BOORE. 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252-3255.
80. ZERBINO, D. R., and E. BIRNEY. 2008. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Research 18: 821-829.
81. ZIMMER, K., C. MEYER, and G. GEBAUER. 2008. The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytologist 178: 395-400.
82. ZOSCHKE, R., M. NAKAMURA, K. LIERE, M. SUGIURA, T. BÖRNER, and C. Schmitz-Linneweber. 2010. An organellar maturase associates with multiple group II introns. Proceedings of the National Academy of Sciences, USA 107: 3245-3250.