Genome analysis of Elysia chlorotica egg DNA provides no evidence for horizontal gene transfer into the germ line of this kleptoplastic mollusc

Molecular Biology and Evolution

Volumn 30, Issue 8, 2013, Pages 1843-1852

  Bhattacharya, Debashish ^a   Pelletreau, Karen N ^b,c   Price, Dana C ^a   Sarver, Kara E ^b   Rumpho, Mary E ^b,c  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF MAINE   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Elysia chlorotica; Genomics; Horizontal gene transfer; Kleptoplasty; Symbiosis; Vaucheria litorea

Indexed keywords

COMPLEMENTARY DNA; EXTRACHROMOSOMAL DNA; GENOMIC DNA; NUCLEIC ACID; DNA;

ALGA; ARTICLE; CONTROLLED STUDY; DNA DETERMINATION; ELYSIA CHLOROTICA; GENE EXPRESSION; GENOME ANALYSIS; GERM LINE; HORIZONTAL GENE TRANSFER; MOLECULAR EVOLUTION; MOLLUSC; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PLASTID; POLYMERASE CHAIN REACTION; VAUCHERIA LITOREA; ANIMAL; BIOLOGY; GASTROPOD; GENETIC TRANSCRIPTION; GENETICS; GENOMICS; GERM CELL; KLEPTOPLASTY; METABOLISM; METHODOLOGY; NUCLEIC ACID DATABASE; SYMBIOSIS; PROCEDURES;

ELYSIA CHLOROTICA; GENOMICS; HORIZONTAL GENE TRANSFER; KLEPTOPLASTY; SYMBIOSIS; VAUCHERIA LITOREA;

ANIMALS; COMPUTATIONAL BIOLOGY; DATABASES, NUCLEIC ACID; DNA; GASTROPODA; GENE TRANSFER, HORIZONTAL; GENOMICS; GERM CELLS; TRANSCRIPTION, GENETIC;

EID: 84886648134     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mst084     Document Type: Article

References (40)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215: 403-410.
2. Boschetti C, Carr A, Crisp A, Eyres I, Wang-Koh Y, Lubzens E, Barraclough TG, Micklem G, Tunnacliffe A 2012. Biochemical diversification through foreign gene expression in bdelloid rotifers. PloS Genet 8:e1003035.
3. Chan CX, Yang EC, Banerjee T, Yoon HS, Martone PT, Estevez JM, Bhattacharya D. 2011. Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr Biol. 21:328-333.
4. Cohen S, Houben A, Segal D. 2007. Extrachromosomal circular DNA derived from tandemly repeated genomic sequences in plants. PlantJ. 53:1027-1034
5. Cohen S, Segal D 2009. Extrachromosomal circular DNA in eukaryotes: possible involvement in the plasticity of tandem repeats. Cytogenet Genome Res. 124:327-338.
6. Evertsen J, Burghardt I, Johnsen G, Wägele H. 2007. Retention of functional chloroplasts in some sacoglossans from the Indo-Pacific and Mediterranean. Mar Biol. 151:2159-2166.
7. Evertsen J, Johnsen G. 2009. In vivo and in vitro differences in chloroplast functionality in the two north Atlantic sacoglossans (Gastropoda, Opisthobranchia) Placida dendritica and Elysia viridis. Mar Biol. 156:847-859
8. Frøkjær-Jensen C, Wayne Davis M, Hopkins CE, Newman BJ, Thummel JM, Olesen S-P, Grunnet M, Jorgensen EM. 2008. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40: 1375-1383
9. Green BJ, Li WY, Manhart JR Fox TC, Summer EJ, Kennedy RA, Pierce SK, Rumpho ME 2000. Mollusc-algal chloroplast endosymbiosis: photosynthesis, thylakoid protein maintenance, and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Phys. 124:331-342
10. Händeler K, Grzymbowski Y, Krug PJ, Wägele H. 2009. Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life. Front Zool. 6:28.
11. Jensen K 1997. Evolution of the Sacoglossa (Mollusca, Opisthobranchia) and the ecological association with their food plants. Evol Ecol. 11: 301-335.
12. Maeda T, Hirose E, Chikaraishi Y, et al. (13 co-authors). 2012. Algivore or phototroph? Plakobranchus ocellatus (Gastropoda) continuously acquires kleptoplasts and nutrition from multiple algal species in nature. PLoS One 7:e42024.
13. Melters DP, Paliulis LV, Korf IF, Chan SWL. 2012. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res. 20:579-593.
14. Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D. 2009. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724-1726.
15. Müjer CV, Andrews DL, Manhart JR, Pierce SK, Rumpho ME. 1996. Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proc Natl Acad Sci U S A. 93: 12333-12338.
16. Noto T, Yazaki K, Endoh H. 2003. Developmentally regulated extrachromosomal circular DNA formation in the mesozoan Dicyema japonicum. Chromosoma 111:359-368.
17. Pelletreau KN, Bhattacharya D, Price DC, Worful JM, Moustafa A, Rumpho ME. 2011. Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Phys. 155:1561-1565.
18. Pelletreau KN, Worful J, Sarver KE, Rumpho ME. 2012. Laboratory culturing of Elysia chlorotica reveals a shift from transient to permanent kleptoplasty. Symbiosis 58:221-232.
19. Pierce SK, Biron R, Rumpho ME. 1996. Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol. 199:2323-2330.
20. Pierce SK, Curtis NE. 2012. Cell biology of the chloroplast symbiosis in sacoglossan sea slugs. In: Jeon WK, editor. International review of cell and molecular biology, Vol. 293. Burlington (VT): Academic Press. p. 123-149.
21. Pierce SK, Curtis NE, Hanten JJ, Boerner SL, Schwartz JA. 2007. Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis 43:57-64.
22. Pierce SK, Curtis NE, Schwartz JA. 2009. Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49: 121-131.
23. Pierce SK, Fang X, Schwartz JA, Jiang X, Zhao W, Curtis NE, Kocot KM, Yang B, Wang J. 2012. Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Mol Biol Evol. 29:1545-1556.
24. Pillet L, Pawlowski J. 2013. Transcriptome analysis of foraminiferan Elphidium margaritaceum questions the role of gene transfer in kleptoplasty. Mol Biol Evol. 30:66-69.
25. Price DC, Chan CX, Yoon HS, et al. (27 co-authors). 2012. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335:843-847.
26. Puthiyaveetil S, Ibrahim IM, Jelicic B, Tomasic A, Fulgosi H, Allen JF. 2010. Transcriptional control of photosynthesis genes: the evolutionarily conserved regulatory mechanism in plastid genome function. Genome Biol Evol. 2:888-896.
27. Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D. 2011. The making of a photosynthetic animal. J Exp Biol. 214:303-311.
28. Rumpho ME, Pochareddy S, Worful JM, Summer EJ, Bhattacharya D, Pelletreau KN, Tyler MS, Lee J, Manhart JR, Soule KM. 2009. Molecular characterization of the Calvin cycle enzyme phosphoribulokinase in the stramenopile alga Vaucheria litorea and the plastid hosting mollusc Elysia chlorotica. Mol Plant 2: 1384-1396.
29. Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc Natl Acad Sci U S A. 105:17867-17871.
30. Schwartz JA, Curtis NE, Pierce SK. 2010. Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evol Biol. 37:29-37.
31. Shibata Y, Kumar P, Layer R, Willcox S, Gagan JR, Griffith JD, Dutta A. 2012. Extrachromosomal microDNAs and chromosomal microdeletions in normal tissues. Science 336:82-86.
32. Soule K. 2009. Light regulated photosynthetic gene expression and enzyme activity in the heterokont alga Vaucheria litorea and its symbiotic partner the sacoglossan mollusc Elysia chlorotica. [master's thesis]. [Orono (ME)]: University of Maine.
33. Soule KM, Rumpho ME. 2012. Light-regulated photosynthetic gene expression and phosphoribulokinase enzyme activity in the heterokont alga Vaucheria litorea (Xanthophyceae) and its symbiotic molluscan partner Elysia chlorotica. J Phycol. 48:373-383.
34. Stinchcomb DT, Mello C, Hirsh D. 1985. Caenorhabditis elegans DNA that directs segregation in yeast cells. Proc Natl Acad Sci U S A. 82:4167-4171.
35. Trench RK. 1975. Of "leaves that crawl": functional chloroplasts in animal cells. Symp Soc Exp Biol. 29:229-265.
36. Wägele H, Deusch O, Händeler K, et al. (11 co-authors). 2011. Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Mol Biol Evol. 28:699-706.
37. West HH. 1979. Chloroplast symbiosis and development of the ascoglossan opisthobranch Elysia chlorotica [dissertation]. [Boston (MA)]: Northeastern University. p. 1-176.
38. Wisecaver JH, Hackett JD. 2010. Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata. BMC Genomics 11:366.
39. Woodson JD, Chory J. 2008. Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet. 9:383-395.
40. Yamamoto YY, Yusa Y, Yamamoto S, Hirano Y, Hirano Y, Motomura T, Tanemura T, Obokata J. 2009. Identification of photosynthetic sacoglossans from Japan. Encocytobiosis Cell Res. 19:112-119.