Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica

Molecular Biology and Evolution

Volumn 29, Issue 6, 2012, Pages 1545-1556

  Pierce, Sidney K ^a,b   Fang, Xiaodong ^c   Schwartz, Julie A ^a   Jiang, Xuanting ^c   Zhao, Wei ^c   Curtis, Nicholas E ^a   Kocot, Kevin M ^d   Yang, Bicheng ^c   Wang, Jian ^c,d  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c BGI SHENZHEN   (China)

^d AUBURN UNIVERSITY   (United States)

Author keywords

Chloroplast symbiosis; Elysia chlorotica; HGT; Horizontal gene transfer; Kleptoplasty; Transcriptome; Vaucheria litorea

Indexed keywords

COMPLEMENTARY DNA; TRANSCRIPTOME;

ALGA; ARTICLE; CELL ORGANELLE; CHLOROPLAST; GENE SEQUENCE; GENOME; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; MOLLUSC; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; POLYMERASE CHAIN REACTION; SEA SLUG; SYMBIOSIS; TRANSCRIPTOMICS; UNINDEXED SEQUENCE;

ANIMALS; BASE SEQUENCE; CHLOROPHYTA; GASTROPODA; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE TRANSFER, HORIZONTAL; GENES, CHLOROPLAST; GENOME; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PHOTOSYNTHESIS; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA;

ALGAE; ELYSIA CHLOROTICA; OPISTHOBRANCHIA; VAUCHERIA LITOREA;

EID: 84855855908     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr316     Document Type: Article

References (28)

1. Al-Samarrai TH, Schmid J. 2000. A simple method for extraction of fungal genomic DNA. Lett Appl Microbiol. 30:53-56. (Pubitemid 30128904)
2. Altschul SF, Gish W, Miller W, Myer EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
3. Birney E, Clamp M, Durbin R. 2004. GeneWise and Genomewise. Genome Res. 14:988-995. (Pubitemid 38660520)
4. Casalduero FG, Muniain C. 2008. The role of kleptoplasts in the survival rates of Elysia timida (Risso, 1818) (Sacoglossa: opisthobranchia) during periods of food shortage. J Mar Biol Ecol. 357:181-187.
5. Darling A, Carey L, Feng W. 2003. The design, implementation, and evaluation of mpiBLAST. In: Proceedings of the ClusterWorld Conference Expo and the 4th International Conference on Linux Cluster: The HPC Revolution; June 2003; San Jose, CA.
6. Green BJ, Li W-Y, Manhart JW, 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 Physiol. 124:331-342.
7. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Res. 12:656-664.
8. Li R, Fan W, Tian G, et al. (116 co-authors). 2010. The sequence and de novo assembly of the giant Panda genome. Nature 463(7279):311-317.
9. Li R, Zhu H, Ruan J, et al. (14 co-authors). 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20:265-272.
10. Lin H, Ma X, Chandramohan P, Geist A, Samatova N. 2005. Efficient data access for parallel BLAST. In: Proceedings of 19th IEEE International Parallel and Distributed Processing Symposium; 2005 Apr 3-8; Denver, CO.
11. Los Alamitos (CA): IEEE Computer Society Conference Publishing Services. Marín A, Ros J. 1989. The chloroplast-animal association of four Iberian Sacoglossan opisthobranchs: elysia timida, Elysia translucens, Thuridilla hopei and Bosellia mimetica. In: Ros J, editor. Topics in marine biology. Proceedings of the 22nd European Marine Biology Symposium. Sci Mar. 53:429-440.
12. Marín A, Ros J. 1992. Dynamics of a peculiar plant-herbivore relationship: the photosynthetic ascoglossan Elysia timida and the chlorophycean Acetabularia acetabulum. Mar Biol. 112: 677-682. (Pubitemid 23398403)
13. Mujer 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 Nat Acad Sci. 93:12333-12338. (Pubitemid 26367143)
14. Pelletreau KN, Bharracharya D, Price DC, Worful JM, Moustafa A, Rumpho ME. 2011. Update on sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiol. 155:1561-1565.
15. Pierce SK, Biron RW, Rumpho ME. 1996. Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol. 199:2323-2330. (Pubitemid 27004880)
16. Pierce SK, Curtis NE. 2012. The cell biology of the chloroplast symbiosis in sacoglossan sea slugs. Int Rev Cell Mol Biol. 293: 123-148.
17. 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. (Pubitemid 350104468)
18. Pierce SK, Curtis NE, Schwartz JA. 2009. Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49: 121-131.
19. Rahat M. 1976. Direct development and symbiotic chloroplasts in Elysia timida (Mollusca: Opisthobranchia). Israel J Zool. 25: 186-193.
20. Rahat M, Monselise EBI. 1979. Photobiology of the chloroplasthosting mollusc, Elysia timida (Opisthobranchia). J Exp Biol. 79: 225-233.
21. Rumpho ME, Pochareddy S, Worful JM, Summer EJ, Bhattacharya D, Pelletreau KN, Tyler MS, Lee J, Marhart 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.
22. 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 USA. 105:17867-17871.
23. Schmitt V, Wägele H. 2011. Behavioral adaptations in relation to longterm retention of endosymbiotic chloroplasts in the sea slug Elysia timida (Opisthobranchia, Sacoglossa). Thalassas 27:225-238.
24. 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.
25. Soule KM. 2009. Light-regulated photosynthetic gene expression and enzyme activity in the heterokont alga Vaucheria litorea and its symbiotic partner the sacoglossan mollusc, Elysia chlorotica [MS thesis]. [Orono (ME)]: University of Maine. p. 120.
26. Stanke M, Waack S. 2003. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19(Suppl 2): ii215-ii225. (Pubitemid 41296659)
27. 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.
28. Wägele H, Johnsen G. 2001. Observations on the histology and photosynthetic performance of "solar-powered" opisthobranchs (Mollusca, Gastropoda, Opishobranchia) containing symbiotic chloroplasts or zooxanthellae. Org Divers Evol. 1:193-210. (Pubitemid 33706586)