Investigating the path of plastid genome degradation in an early-transitional clade of heterotrophic orchids, and implications for heterotrophic angiosperms

Molecular Biology and Evolution

Volumn 31, Issue 12, 2014, Pages 3095-3112

  Barrett, Craig F ^a   Freudenstein, John V ^b   Li, Jeff ^a   Mayfield Jones, Dustin R ^c   Perez, Leticia ^a   Pires, J Chris ^c   Santos, Cristian ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

chlorophyll; chloroplast; Orchidaceae; parasite; photosynthesis; pseudogene

Indexed keywords

CHLOROPHYLL; GENOMIC DNA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); RIBOSOME DNA;

ANGIOSPERM; ARTICLE; CHLOROPHYLL CONTENT; CISTRON; CLADISTICS; GENE DELETION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; ORCHIDACEAE; PHOTOSYNTHESIS; PLASTID GENOME; PSEUDOGENE; QUANTITATIVE ANALYSIS; SEQUENCE ALIGNMENT; SPECIES; TAXONOMY; TREE; DNA SEQUENCE; GENETICS; HETEROTROPHY; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLANT GENE;

CORALLORHIZA; MAGNOLIOPHYTA; ORCHIDACEAE;

CHLOROPHYLL; EVOLUTION, MOLECULAR; GENES, PLANT; GENOME, PLASTID; HETEROTROPHIC PROCESSES; MOLECULAR SEQUENCE DATA; ORCHIDACEAE; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 84908182778     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu252     Document Type: Article

References (98)

1. Allen JF, de Paula WBM, Puthiyaveetil S, Nield J. 2011. A structural phylogenetic map for chloroplast photosynthesis. Trends Plant Sci. 16:645-655.
2. Barbrook AC, Howe CJ, Purton S. 2006. Why are plastid genomes retained in non-photosynthetic organisms? Trends Plant Sci. 11: 101-108.
3. Barrett CF, Davis JI. 2012. The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation. Am J Bot. 99:1513-1523.
4. Barrett CF, Davis JI, Leebens-Mack J, Conran JG, Stevenson DW. 2013. Plastid genomes and deep relationships among the commelinid monocot angiosperms. Cladistics 29:65-87.
5. Barrett CF, Freudenstein JV. 2008. Molecular evolution of rbcL in the mycoheterotrophic coralroot orchids (Corallorhiza Gagnebin, Orchidaceae). Mol Phylogenet Evol. 47:665-679.
6. Bellino A, Alfani A, Selosse M-A, Guerrieri R, Borghetti M, Baldantoni D. 2014. Nutritional regulation in mixotrophic plants: new insights from Limodorum abortivum. Oecologia 175:875-885.
7. Bernardi G. 1989. The isochore organization of the human genome. Annu Rev Genet. 23:637-661.
8. Bidartondo MI. 2005. The evolutionary ecology of myco-heterotrophy. New Phytol. 167:335-352.
9. Blazier J, Guisinger MM, Jansen RK. 2011. Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae). PlantMol Biol. 76:263-272.
10. Braukmann T, Kuzmina M, Stefanovic S. 2013. Plastid genome evolution across the genus Cuscuta (Convolvulaceae): two clades within subgenus Grammica exhibit extensive gene loss. J Exp Bot. 64:977-989.
11. Braukmann T, Stefanovic S. 2012. Plastid genome evolution in mycoheterotrophic Ericaceae. Plant Mol Biol. 79:5-20.
12. Braukmann TWA, Kuzmina M, Stefanovic 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.
13. Burnham KP, Anderson DR. 2002. Avoiding pitfalls when using information-theoretic methods. J Wildl Manage. 66:912-918.
14. Cameron DD, Preiss K, Gebauer G, Read DJ. 2009. The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytol. 183:358-364.
15. Chang CC, Lin HC, Lin IP, Chow TY, Chen HH, Chen WH, Cheng CH, Lin CY, Liu SM, Chang CC, et al. 2006. The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mol Biol Evol. 23:279-291.
16. Conant GC, Wolfe KH. 2008. GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics 24:861-862.
17. Cummings MP, Welschmeyer NA. 1998. Pigment composition of putatively achlorophyllous angiosperms. Plant Syst Evol. 210: 105-111.
18. Delannoy E, Fujii S, Colas des Francs-Small C, Brundrett M, Small I. 2011. Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol Biol Evol. 28:2077-2086.
19. Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 19:11-15.
20. Dunn OJ. 1959. Confidence intervals for the means of dependent, normally distributed variables. J Am Stat Assoc. 54:613-621.
21. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
22. Evron Y, Johnson EA, McCarty RE. 2000. Regulation of proton flow and ATP synthesis in chloroplasts. J Bioenerg Biomembr. 32:501-506.
23. Fang YJ,Wu H, Zhang TW, YangM, Yin YX, Pan LL, Yu XG, Zhang XW, Hu SNA, Al-Mssallem IS, et al. 2012. A complete sequence and transcriptomic analyses of date palm (Phoenix dactylifera L.) mitochondrial genome. PLoS One 7:e37164.
24. Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat. 125:1-15.
25. Freudenstein JV. 1992. Systematics of Corallorhiza and the Corallorhizinae (Orchidaceae) [Ph.D. dissertation]. [Ithaca (NY)]: Cornell University.
26. Freudenstein JV. 1997. A monograph of Corallorhiza (Orchidaceae). Harv Pap Bot. 10:5-51.
27. Freudenstein JV, Barrett CF. 2010. Mycoheterotrophy and diversity in Orchidaceae. In: Seberg O, Petersen G, Barfod A, Davis JI, editors. Diversity, phylogeny and evolution in the monocotyledons. The Proceedings of the Fourth International Conference on Monocot Systematics. Aarhus (Denmark): Aarhus University Press. p. 25-37.
28. Freudenstein JV, Doyle JJ. 1994a. Character transformation and relationships in Corallorhiza (Orchidaceae, Epidendroideae). 1. Plastid DNA. Am J Bot. 81:1449-1457.
29. Freudenstein JV, Doyle JJ. 1994b. Plastid DNA, morphological variation, and the phylogenetic species concept-the Corallorhiza maculata (Orchidaceae) complex. Syst Bot. 19:273-290.
30. Freudenstein JV, Senyo DM. 2008. Relationships and evolution of matK in a group of leafless orchids (Corallorhiza and Corallorhizinae; Orchidaceae : Epidendroideae). Am J Bot. 95:498-505.
31. Funk HT, Berg S, Krupinska K,Maier UG, Krause K. 2007. Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol. 7:45.
32. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, et al. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868.
33. Garland T, Dickerman AW, Janis CM, Jones JA. 1993. Phylogenetic analysis of covariance by computer simulation. Syst Biol. 42:265-292.
34. Glemin S, Clement Y, David J, Ressayre A. 2014. GC content evolution in coding regions of angiosperm genomes: a unifying hypothesis. Trends Genet. 30:263-270.
35. Goloboff PA, Farris JS, Kallersjo M, Oxelman B, Ramirez MJ, Szumik CA. 2003. Improvements to resampling measures of group support. Cladistics 19:324-332.
36. Goloboff PA, Farris JS, Nixon KC. 2008. TNT, a free program for phylogenetic analysis. Cladistics 24:774-786.
37. Hajdukiewicz PTJ, Allison LA, Maliga P. 1997. The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16:4041-4048.
38. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W. 2008. GEIGER: investigating evolutionary radiations. Bioinformatics 24:129-131.
39. Iles WJD, Smith SY, Graham SW. 2013. 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: Wilkin P, Mayo S, editors. Early events in monocot evolution. Cambridge: Cambridge University Press. p. 1-28.
40. Iorizzo M, Grzebelus D, Senalik D, Szklarczyk M, Spooner D, Simon P. 2012. Against the traffic: the first evidence for mitochondrial DNA transfer into the plastid genome. Mob Genet Elements. 2:261.
41. Jensen PE, Bassi R, Boekema EJ, Dekker JP, Jansson S, Leister D, Robinson C, Scheller HV. 2007. Structure, function and regulation of plant photosystem I. Biochim Biophys Acta. 1767:335-352.
42. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, et al. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450-453.
43. Katoh K, Misawa K, Kuma Ki, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059-3066.
44. Kawakami K, Umena Y, Iwai M, Kawabata Y, Ikeuchi M, Kamiya N, Shen J-R. 2011. Roles of PsbI and PsbM in photosystem II dimer formation and stability studied by deletion mutagenesis and X-ray crystallography. Biochim Biophys Acta. 1807:319-325.
45. Knaus BJ. 2010. Short read toolbox. Available from: http://brianknaus.com.
46. Krause K. 2008. From chloroplasts to "cryptic" plastids: evolution of plastid genomes in parasitic plants. Curr Genet. 54:111-121.
47. Krause K. 2012. Plastid genomes of parasitic plants: a trail of reductions and losses. In: Bullerwell C, editor. Organelle genetics. Berlin (Germany): Springer. p. 79-103.
48. Kuijt J. 1969. The biology of flowering parasitic plants. Berkeley (CA): University of California Press.
49. Lawrence JG. 2005. Common themes in the genome strategies of pathogens. Curr Opin Genet Dev. 15:584-588.
50. Leake JR. 1994. The biology of myco-heterotrophic (Saprophytic) plants. New Phytol. 127:171-216.
51. Leake JR, Cameron DD. 2010. Physiological ecology of mycoheterotrophy. New Phytol. 185:601-605.
52. Liere K,Weihe A, Borner T. 2011. The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol. 168:1345-1360.
53. Logacheva MD, Schelkunov MI, Nuraliev MS, Samigullin TH, Penin AA. 2014. The plastid genome of mycoheterotrophic monocot Petrosavia stellaris exhibits both gene losses and multiple rearrangements. Genome Biol Evol. 6:238-246.
54. LogachevaMD, Schelkunov MI, Penin AA. 2011. Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biol Evol. 3:1296-1303.
55. Maddison WP, Maddison DR. 2011. Mesquite: a modular system for evolutionary analysis. version 2.75. Available from: http://mesquiteproject.org.
56. Martin M, Funk HT, Serrot PH, Poltnigg P, Sabater B. 2009. Functional characterization of the thylakoid ndh complex phosphorylation by site-directed mutations in the ndhF gene. Biochim Biophys Acta. 1787:920-928.
57. Martýn M, Sabater B. 2010. Plastid ndh genes in plant evolution. Plant Physiol Biochem. 48:636-645.
58. McCarty RE, Evron Y, Johnson EA. 2000. The chloroplast ATP synthase: a rotary enzyme? Annu Rev Plant Physiol Plant Mol Biol. 51:83-109.
59. McNeal JR, Arumugunathan K, Kuehl JV, Boore JL, Depamphilis CW. 2007. Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae). BMC Biol. 5:55.
60. McNeal JR, Bennett JR, Wolfe AD, Mathews S. 2013. Phylogeny and origins of holoparasitism in Orobanchaceae. Am J Bot. 100: 971-983.
61. Merckx V, Freudenstein JV. 2010. Evolution of mycoheterotrophy in plants: a phylogenetic perspective. New Phytol. 185:605-609.
62. Midford PE, Garland T Jr, Maddison WP. 2005. PDAP package of Mesquite. version 1.07. Available from: http://mesquiteproject.org/.
63. Molina J, Hazzouri KM, Nickrent D, Geisler M, Meyer RS, Pentony MM, Flowers JM, Pelser P, Barcelona J, Inovejas SA, et al. 2014. Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae). Mol Biol Evol. 31:793-803.
64. Montfort C, Kusters E. 1940. Saprophytismus und photosythese. I. Biochemische physiologische studien an humus-orchideen. Botanisces Archiv 40:571-633.
65. Moran NA. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583-586.
66. Morrison HG,McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, et al. 2007. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317:1921-1926.
67. Nickrent DL, Yan OY, Duff RJ, dePamphilis CW. 1997. Do nonasterid holoparasitic flowering plants have plastid genomes? Plant Mol Biol. 34:717-729.
68. Patel RK, Jain M. 2012. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619.
69. Peredo EL, King UM, Les DH. 2013. The plastid genome of Najas flexilis: adaptation to submersed environments is accompanied by the complete loss of the NDH complex in an aquatic angiosperm. PLoS One 8:e68591.
70. Porra RJ. 2002. The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosyn Res. 73:149-156.
71. ProtasioAV, Tsai IJ, Babbage A, Nichol S, Hunt M, Aslett MA,De Silva N, Velarde GS, Anderson TJC, Clark RC, et al. 2012. A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLoS Negl Trop Dis. 6: e1455.
72. Randle CP, Wolfe AD. 2005. The evolution and expression of rbcL in holoparasitic sister-genera Harveya and Hyobanche (Orobanchaceae). Am J Bot. 92:1575-1585.
73. Ranwez V, Harispe S, Delsuc F, Douzery EJP. 2011. MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS One 6:e22594.
74. Sanderson MJ. 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol. 14: 1218-1231.
75. Smith DR, Lee RW. 2014. A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol. 164: 1812-1819.
76. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
77. Straub SCK, Cronn RC, Edwards C, Fishbein M, Liston A. 2013. Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (Apocynaceae). Genome Biol Evol. 5:1872-1885.
78. Straub SCK, Fishbein M, Livshultz T, Foster Z, Parks M, Weitemier K, Cronn RC, Liston A. 2011. Building a model: developing genomic resources for common milkweed (Asclepias syriaca) with low coverage genome sequencing. BMC Genomics 12:211.
79. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 30:2725-2729.
80. Tsai IJ, Zarowiecki M, Holroyd N, Garciarrubio A, Sanchez-Flores A, Brooks KL, Tracey A, Bobes RJ, Fragoso G, Sciutto E, et al. 2013. The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496:57-63.
81. Umate P, Schwenkert S, Karbat I, Dal Bosco C, Mlcochova L, Volz S, Zer H, Herrmann RG, Ohad I, Meurer J. 2007. Deletion of psbM in tobacco alters the Q(B) site properties and the electron flow within photosystem II. J Biol Chem. 282:9758-9767.
82. Vaidya G, Lohman DJ, Meier R. 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27:171-180.
83. Westwood JH, Yoder JI, Timko MP, dePamphilis CW. 2010. The evolution of parasitism in plants. Trends Plant Sci. 15:227-235.
84. Wicke S, Muller KF, de Pamphilis CW, Quandt D, Wickett NJ, Zhang Y, Renner SS, Schneeweiss GM. 2013. Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family. Plant Cell 25: 3711-3725.
85. Wicke S, Schaferhoff B, dePamphilis CW, Muller KF. 2014. Disproportional plastome-wide increase of substitution rates and relaxed purifying selection in genes of carnivorous Lentibulariaceae. Mol Biol Evol. 31:529-545.
86. Wicke S, Schneeweiss GM, dePamphilis CW, Muller KF, Quandt D. 2011. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol. 76: 273-297.
87. Wickett NJ, Honaas LA,Wafula EK, DasM, Huang K, Wu BA, Landherr L, TimkoMP, Yoder J,Westwood JH, et al. 2011. Transcriptomes of the parasitic plant family Orobanchaceae reveal surprising conservation of chlorophyll synthesis. Curr Biol. 21:2098-2104.
88. Wimpee CF,Wrobel RL, Garvin DK. 1991. A divergent plastid genome in Conopholis americana, an achlorophyllous parasitic plant. Plant Mol Biol. 17:161-166.
89. Wolfe AD, dePamphilis CW. 1998. The effect of relaxed functional constraints on the photosynthetic gene rbcL in photosynthetic and nonphotosynthetic parasitic plants. Mol Biol Evol. 15:1243-1258.
90. Wolfe KH, Morden CW, Palmer JD. 1992. Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci U S A. 89:10648-10652.
91. Wu FH, Chan MT, Liao DC, Hsu CT, Lee YW, Daniell H, Duvall MR, Lin CS. 2010. Complete chloroplast genome of Oncidium Gower Ramsey and evaluation of molecular markers for identification and breeding in Oncidiinae. BMC Plant Biol. 10:68.
92. Wyman SK, Jansen RK, Boore JL. 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252-3255.
93. Yang JB, Tang M, Li HT, Zhang ZR, Li DZ. 2013. Complete chloroplast genome of the genus Cymbidium: lights into the species identification, phylogenetic implications and population genetic analyses. BMC Evol Biol. 13:84.
94. Yang ZH. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
95. Yang ZH. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
96. Yoder OC, Turgeon BG. 2001. Fungal genomics and pathogenicity. Curr Opin Plant Biol. 4:315-321.
97. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18:821-829.
98. Zimmer K, Meyer C, Gebauer G. 2008. The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytol. 178:395-400.