Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae

Journal of Experimental Biology

Volumn 214, Issue 1, 2011, Pages 59-68

  Boschetti, Chiara ^a   Pouchkina Stantcheva, Natalia ^a,b   Hoffmann, Pia ^a   Tunnacliffe, Alan ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

Anhydrobiosis; Bdelloid rotifer; Desiccation tolerance; Desiccome; Horizontal gene transfer; Hydrophilin; Lateral gene transfer; LEA protein

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOLOGY; CLUSTER ANALYSIS; DEHYDRATION; DNA SEQUENCE; EXPRESSED SEQUENCE TAG; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; HORIZONTAL GENE TRANSFER; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; ROTIFERA; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DEHYDRATION; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION REGULATION; GENE LIBRARY; GENE TRANSFER, HORIZONTAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; ROTIFERA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

ADINETA; ADINETA RICCIAE; BDELLOIDA; FUNGI; INVERTEBRATA; ROTIFERA;

EID: 78651315449     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.050328     Document Type: Article

References (56)

1. Adhikari, B. N., Wall, D. H. and Adams, B. J. (2009). Desiccation survival in an Antarctic nematode: molecular analysis using expressed sequenced tags. BMC Genomics 10, 69.
2. Alpert, P. (2006). Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J. Exp. Biol. 209, 1575-1584.
3. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
4. Bartels, D. (2005). Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr. Comp. Biol. 45, 696-701.
5. Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F. and Covarrubias, A. A. (2008). The enigmatic LEA proteins and other hydrophilins. Plant Physiol. 148, 6-24.
6. Browne, J., Tunnacliffe, A. and Burnell, A. (2002). Anhydrobiosis-plant desiccation gene found in a nematode. Nature 416, 38-38.
7. Browne, J. A., Dolan, K. M., Tyson, T., Goyal, K., Tunnacliffe, A. and Burnell, A. M. (2004). Dehydration-specific induction of hydrophilic protein genes in the anhydrobiotic nematode Aphelenchus avenae. Eukaryotic Cell 3, 966-975.
8. Burnell, A. M. and Tunnacliffe, A. (2011). Gene induction and desiccation stress in nematodes. In Molecular and Physiological Basis of Nematode Survival (ed. R. N. Perry and D. Wharton). Wallingford, UK: CABI Publishing.
9. Caprioli, M., Krabbe Katholm, A., Melone, G., Ramløv, H., Ricci, C. and Santo, N. (2004). Trehalose in desiccated rotifers: a comparison between a bdelloid and a monogonont species. Comp. Biochem. Physiol. 139 A, 527-532.
10. Chakrabortee, S., Meersman, F., Kaminski Schierle, G. S., Bertoncini, C. W., McGee, B., Kaminski, C. F. and Tunnacliffe, A. (2010). Catalytic and chaperonelike functions in an intrinsically disordered protein associated with desiccation tolerance. Proc. Natl. Acad. Sci. USA 107, 16084-16089.
11. Clegg, J. S. (2001). Cryptobiosis-a peculiar state of biological organization. Comp. Biochem. Physiol. 128 B, 613-624.
12. Colaco, C., Sen, S., Thangavelu, M., Pinder, S. and Roser, B. (1992). Extraordinary stability of enzymes dried in trehalose: simplified molecular biology. Biotechnology 10, 1007-1011.
13. Crowe, J. H., Hoekstra, F. A. and Crowe, L. M. (1992). Anhydrobiosis. Annu. Rev. Physiol. 54, 579-599.
14. Crowe, J. H., Carpenter, J. F. and Crowe, L. M. (1998). The role of vitrification in anhydrobiosis. Annu. Rev. Physiol. 60, 73-103.
15. Denekamp, N. Y., Reinhardt, R., Kube, M. and Lubzens, E. (2010). Late embryogenesis abundant (LEA) proteins in nondesiccated, encysted, and diapausing embryos of rotifers. Biol. Reprod. 82, 714-724.
16. Dunker, A. K., Obradovic, Z., Romero, P., Garner, E. C. and Brown, C. J. (2000). Intrinsic protein disorder in complete genomes. Genome Inform. Ser. Workshop Genome Inform. 11, 161-171.
17. Gal, T. Z., Glazer, I. and Koltai, H. (2003). Differential gene expression during desiccation stress in the insect-killing nematode Steinernema feltiae IS-6. J. Parasitol. 89, 761-766.
18. Garay-Arroyo, A., Colmenero-Flores, J. M., Garciarrubio, A. and Covarrubias, A. A. (2000). Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J. Biol. Chem. 275, 5668-5674.
19. Gladyshev, E. A., Meselson, M. and Arkhipova, I. R. (2008). Massive horizontal gene transfer in bdelloid rotifers. Science 320, 1210-1213.
20. Goyal, K., Tisi, L., Basran, A., Browne, J., Burnell, A., Zurdo, J. and Tunnacliffe, A. (2003). Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J. Biol. Chem. 278, 12977-12984.
21. Hengherr, S., Brummer, F. and Schill, R. O. (2008). Anhydrobiosis in tardigrades and its effects on longevity traits. J. Zool. 275, 216-220.
22. Hoekstra, F. A., Golovina, E. A. and Buitink, J. (2001). Mechanisms of plant desiccation tolerance. Trends Plant Sci. 6, 431-438.
23. Illing, N., Denby, K. J., Collett, H., Shen, A. and Farrant, J. M. (2005). The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integr. Comp. Biol. 45, 771-787.
24. Ingram, J. and Bartels, D. (1996). The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 377-403.
25. Keeling, P. J. and Palmer, J. D. (2008). Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605-618.
26. Kranner, I. and Birtic, S. (2005). A modulating role for antioxidants in desiccation tolerance. Integr. Comp. Biol. 45, 734-740.
27. Lapinski, J. and Tunnacliffe, A. (2003). Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett. 553, 387-390.
28. Li, X., Romero, P., Rani, M., Dunker, A. K. and Obradovic, Z. (1999). Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform. 10, 30-40.
29. Mali, B., Grohme, M. A., Forster, F., Dandekar, T., Schnolzer, M., Reuter, D., Welnicz, W., Schill, R. O. and Frohme, M. (2010). Transcriptome survey of the anhydrobiotic tardigrade Milnesium tardigradum in comparison with Hypsibius dujardini and Richtersius coronifer. BMC Genomics 11, 168.
30. Mark Welch, D. and Meselson, M. (2000). Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288, 1211-1215.
31. Mattimore, V. and Battista, J. R. (1996). Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J. Bacteriol. 178, 633-637.
32. Potts, M. (1994). Desiccation tolerance of prokaryotes. Microbiol. Rev. 58, 755-805.
33. Potts, M. (2004). The desiccome: humble beginnings. Integr. Comp. Biol. 44, 624-624.
34. Pouchkina-Stantcheva, N. N. and Tunnacliffe, A. (2005). Spliced leader RNA-mediated trans-splicing in phylum Rotifera. Mol. Biol. Evol. 22, 1482-1489.
35. Pouchkina-Stantcheva, N. N., McGee, B. M., Boschetti, C., Tolleter, D., Chakrabortee, S., Popova, A. V., Meersman, F., Macherel, D., Hincha, D. K. and Tunnacliffe, A. (2007). Functional divergence of former alleles in an ancient asexual invertebrate. Science 318, 268-271.
36. Prilusky, J., Felder, C. E., Zeev-Ben-Mordehai, T., Rydberg, E. H., Man, O., Beckmann, J. S., Silman, I. and Sussman, J. L. (2005). FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21, 3435-3438.
37. Radivojac, P., Obradovic, Z., Brown, C. J. and Dunker, A. K. (2003). Prediction of boundaries between intrinsically ordered and disordered protein regions. Pac. Symp. Biocomput. 8, 216-227.
38. Ratnakumar, S. and Tunnacliffe, A. (2006). Intracellular trehalose is neither necessary nor sufficient for desiccation tolerance in yeast. Fems Yeast Res. 6, 902-913.
39. Reardon, W., Chakrabortee, S., Pereira, T. C., Tyson, T., Banton, M. C., Dolan, K. M., Culleton, B. A., Wise, M. J., Burnell, A. M. and Tunnacliffe, A. (2010). Expression profiling and cross-species RNA interference (RNAi) of desiccationinduced transcripts in the anhydrobiotic nematode Aphelenchus avenae. BMC Mol. Biol. 11, 6.
40. Ricci, C. and Covino, C. (2005). Anhydrobiosis of Adineta ricciae: costs and benefits. Hydrobiologia 546, 307-314.
41. Ricci, C., Melone, G., Santo, N. and Caprioli, M. (2003). Morphological response of a bdelloid rotifer to desiccation. J. Morphol. 257, 246-253.
42. Ricci, C., Caprioli, M. and Santo, N. (2004). Feeding and anhydrobiosis in bdelloid rotifers: a preparatory study for an experiment aboard the International Space Station. Invertebr. Biol. 123, 283-288.
43. Rice, W. R. and Friberg, U. (2007). Genomic clues to an ancient asexual scandal. Genome Biol. 8, 232.
44. Rizzo, A. M., Negroni, M., Altiero, T., Montorfano, G., Corsetto, P., Berselli, P., Berra, B., Guidetti, R. and Rebecchi, L. (2010). Antioxidant defences in hydrated and desiccated states of the tardigrade Paramacrobiotus richtersi. Comp. Biochem. Physiol. 156 B, 115-121.
45. Schill, R. O., Steinbruck, G. H. and Kohler, H. R. (2004). Stress gene (hsp70) sequences and quantitative expression in Milnesium tardigradum (Tardigrada) during active and cryptobiotic stages. J. Exp. Biol. 207, 1607-1613.
46. Segers, H. and Shiel, R. J. (2005). Tale of a sleeping beauty: a new and easily cultured model organism for experimental studies on bdelloid rotifers. Hydrobiologia 546, 141-145.
47. Shannon, A. J., Browne, J. A., Boyd, J., Fitzpatrick, D. A. and Burnell, A. M. (2005). The anhydrobiotic potential and molecular phylogenetics of species and strains of Panagrolaimus (Nematoda, Panagrolaimidae). J. Exp. Biol. 208, 2433-2445.
48. Sharon, M. A., Kozarova, A., Clegg, J. S., Vacratsis, P. O. and Warner, A. H. (2009). Characterization of a group 1 late embryogenesis abundant protein in encysted embryos of the brine shrimp Artemia franciscana. Biochem. Cell Biol. 87, 415-430.
49. Shih, M., Hoekstra, F. and Hsing, Y. (2008). Late embryogenesis abundant proteins. Adv. Bot. Res. 48, 211-255.
50. Tompa, P. (2009). Structure and Function of Intrinsically Disordered Proteins. Boca Raton, FL: Taylor and Francis.
51. Tompa, P., Szasz, C. and Buday, L. (2005). Structural disorder throws new light on moonlighting. Trends Biochem. Sci. 30, 484-489.
52. Tunnacliffe, A. and Lapinski, J. (2003). Resurrecting Van Leeuwenhoek's rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 1755-1771.
53. Tunnacliffe, A. and Wise, M. J. (2007). The continuing conundrum of the LEA proteins. Naturwissenschaften 94, 791-812.
54. Tunnacliffe, A., Hincha, D. K., Leprince, O. and Macherel, D. (2010). LEA proteins: versatility of form and function. In Dormancy and Resistance in Harsh Environments (ed. E. Lubzens, J. Cerda and M. S. Clark), pp. 91-108. Berlin: Springer.
55. Tyson, T., Reardon, W., Browne, J. A. and Burnell, A. M. (2007). Gene induction by desiccation stress in the entomopathogenic nematode Steinernema carpocapsae reveals parallels with drought tolerance mechanisms in plants. Int. J. Parasitol. 37, 763-776.
56. Watanabe, M., Kikawada, T., Minagawa, N., Yukuhiro, F. and Okuda, T. (2002). Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J. Exp. Biol. 205, 2799-2802.