Life without water: expression of plant LEA genes by an anhydrobiotic arthropod
Abstract
Anhydrobiotic animals protect cellular architecture and metabolic machinery in the dry state, yet the molecular repertoire supporting this profound dehydration tolerance is not fully understood. For the desiccation‐tolerant crustacean, Artemia franciscana, we report differential expression of two distinct mRNAs encoding for proteins that share sequence similarities and structural features with late‐embryogenesis abundant (LEA) proteins originally discovered in plants. Bioinformatic analyses support assignment of the LEA proteins from A. franciscana to group 3. This eucoelomate species is the most highly evolved animal for which LEA gene expression has been reported. It is becoming clear that an ensemble of micromolecules and macromolecules is important for establishing the physical conditions required for cellular stabilization during drying in nature. J. Exp. Zool. 305A:62–66, 2006. © 2006 Wiley‐Liss, Inc.
Number of times cited: 43
- Nishit Pathak and Shinya Ikeno, In vivo expression of a short peptide designed from late embryogenesis abundant protein for enhancing abiotic stress tolerance in Escherichia coli, Biochemical and Biophysical Research Communications, 10.1016/j.bbrc.2017.08.091, 492, 3, (386-390), (2017).
- Alejandra A. Covarrubias, Cesar L. Cuevas-Velazquez, Paulette S. Romero-Pérez, David F. Rendón-Luna and Caspar C. C. Chater, Structural disorder in plant proteins: where plasticity meets sessility, Cellular and Molecular Life Sciences, 10.1007/s00018-017-2557-2, 74, 17, (3119-3147), (2017).
- T. Amuge, D. K. Berger, M. S. Katari, A. A. Myburg, S. L. Goldman and M. E. Ferguson, A time series transcriptome analysis of cassava (Manihot esculenta Crantz) varieties challenged with Ugandan cassava brown streak virus, Scientific Reports, 7, 1, (2017).
- Brett Janis, Vladimir N. Uversky and Michael A. Menze, Potential functions of LEA proteins from the brine shrimp Artemia franciscana – anhydrobiosis meets bioinformatics, Journal of Biomolecular Structure and Dynamics, (1), (2017).
- Steven C. Hand, David L. Denlinger, Jason E. Podrabsky and Richard Roy, Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish, American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 310, 11, (R1193), (2016).
- Daniel S. Moore and Steven C. Hand, Cryopreservation of lipid bilayers by LEA proteins from Artemia franciscana and trehalose, Cryobiology, 73, 2, (240), (2016).
- Takao Furuki, Takahiro Watanabe, Tadaomi Furuta, Kiyoshi Takano, Ryo Shirakashi and Minoru Sakurai, The Dry Preservation of Giant Vesicles Using a Group 3 LEA Protein Model Peptide and Its Molecular Mechanism, Bulletin of the Chemical Society of Japan, 89, 12, (1493), (2016).
- Daniel S. Moore, Richard Hansen and Steven C. Hand, Liposomes with diverse compositions are protected during desiccation by LEA proteins from Artemia franciscana and trehalose, Biochimica et Biophysica Acta (BBA) - Biomembranes, 1858, 1, (104), (2016).
- Takao Furuki and Minoru Sakurai, Group 3 LEA protein model peptides protect enzymes against desiccation stress, Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1864, 9, (1237), (2016).
- Thomas H. MacRae, Stress tolerance during diapause and quiescence of the brine shrimp, Artemia, Cell Stress and Chaperones, 10.1007/s12192-015-0635-7, 21, 1, (9-18), (2015).
- Scott R. Strachan, Edwin T. Chester and Belinda J. Robson, Freshwater Invertebrate Life History Strategies for Surviving Desiccation, Springer Science Reviews, 3, 1, (57), (2015).
- Steven C. Hand and Michael A. Menze, Molecular approaches for improving desiccation tolerance: insights from the brine shrimp Artemia franciscana, Planta, 242, 2, (379), (2015).
- Leaf C. Boswell, Michael A. Menze and Steven C. Hand, Group 3 Late Embryogenesis Abundant Proteins from Embryos ofArtemia franciscana: Structural Properties and Protective Abilities during Desiccation, Physiological and Biochemical Zoology, 87, 5, (640), (2014).
- Takao Furuki and Minoru Sakurai, Group 3 LEA protein model peptides protect liposomes during desiccation, Biochimica et Biophysica Acta (BBA) - Biomembranes, 10.1016/j.bbamem.2014.07.009, 1838, 11, (2757-2766), (2014).
- Jantina Toxopeus, Alden H. Warner and Thomas H. MacRae, Group 1 LEA proteins contribute to the desiccation and freeze tolerance of Artemia franciscana embryos during diapause, Cell Stress and Chaperones, 19, 6, (939), (2014).
- Leaf C. Boswell, Daniel S. Moore and Steven C. Hand, Quantification of cellular protein expression and molecular features of group 3 LEA proteins from embryos of Artemia franciscana, Cell Stress and Chaperones, 10.1007/s12192-013-0458-3, 19, 3, (329-341), (2013).
- Imen Amara, Ikram Zaidi, Khaled Masmoudi, M. Dolors Ludevid, Montserrat Pagès, Adela Goday and Faiçal Brini, Insights into Late Embryogenesis Abundant (LEA) Proteins in Plants: From Structure to the Functions, American Journal of Plant Sciences, 10.4236/ajps.2014.522360, 05, 22, (3440-3455), (2014).
- Leaf C. Boswell and Steven C. Hand, Intracellular localization of group 3 LEA proteins in embryos of Artemia franciscana, Tissue and Cell, 10.1016/j.tice.2014.09.004, 46, 6, (514-519), (2014).
- Shinya Ikeno, Tetsuya Haruyama and Anna Mitraki, Boost Protein Expression through Co-Expression of LEA-Like Peptide in Escherichia coli, PLoS ONE, 8, 12, (e82824), (2013).
- F. Campos, C. Cuevas-Velazquez, M. A. Fares, J. L. Reyes and A. A. Covarrubias, Group 1 LEA proteins, an ancestral plant protein group, are also present in other eukaryotes, and in the archeae and bacteria domains, Molecular Genetics and Genomics, 288, 10, (503), (2013).
- Matthew R. Marunde, Dilini A. Samarajeewa, John Anderson, Shumin Li, Steven C. Hand and Michael A. Menze, Improved tolerance to salt and water stress in Drosophila melanogaster cells conferred by late embryogenesis abundant protein, Journal of Insect Physiology, 59, 4, (377), (2013).
- Rie Hatanaka, Yuka Hagiwara-Komoda, Takao Furuki, Yasushi Kanamori, Mika Fujita, Richard Cornette, Minoru Sakurai, Takashi Okuda and Takahiro Kikawada, An abundant LEA protein in the anhydrobiotic midge, PvLEA4, acts as a molecular shield by limiting growth of aggregating protein particles, Insect Biochemistry and Molecular Biology, 43, 11, (1055), (2013).
- Takao Furuki, Tempei Shimizu, Sohini Chakrabortee, Kentarou Yamakawa, Rie Hatanaka, Tsuyoshi Takahashi, Takahiro Kikawada, Takashi Okuda, Hisakazu Mihara, Alan Tunnacliffe and Minoru Sakurai, Effects of Group 3 LEA protein model peptides on desiccation-induced protein aggregation, Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1824, 7, (891), (2012).
- Alden H. Warner, Sohini Chakrabortee, Alan Tunnacliffe and James S. Clegg, Complexity of the heat-soluble LEA proteome in Artemia species, Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 10.1016/j.cbd.2012.04.002, 7, 3, (260-267), (2012).
- Brande L. Jones, Dana M. Schneider and Terry W. Snell, Thermostable proteins in the diapausing eggs of Brachionus manjavacas (Rotifera), Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 162, 3, (193), (2012).
- Steven C. Hand, Michael A. Menze, Mehmet Toner, Leaf Boswell and Daniel Moore, LEA Proteins During Water Stress: Not Just for Plants Anymore, Annual Review of Physiology, 73, 1, (115), (2011).
- Brandon M. Hall, Kjerstin M. Owens and Keshav K. Singh, Distinct Functions of Evolutionary Conserved MSF1 and Late Embryogenesis Abundant (LEA)-like Domains in Mitochondria, Journal of Biological Chemistry, 286, 45, (39141), (2011).
- Takao Furuki, Tempei Shimizu, Takahiro Kikawada, Takashi Okuda and Minoru Sakurai, Salt Effects on the Structural and Thermodynamic Properties of a Group 3 LEA Protein Model Peptide, Biochemistry, 50, 33, (7093), (2011).
- Steffen Hengherr and Ralph O. Schill, Dormant stages in freshwater bryozoans—An adaptation to transcend environmental constraints, Journal of Insect Physiology, 57, 5, (595), (2011).
- Steffen Hengherr, Ralph O. Schill and James S. Clegg, Mechanisms Associated with Cellular Desiccation Tolerance in the Animal Extremophile Artemia , Physiological and Biochemical Zoology, 10.1086/659314, 84, 3, (249-257), (2011).
- Gang Wu, Hangxiao Zhang, Jing Sun, Fei Liu, Xiaomeng Ge, Wei-Hua Chen, Jun Yu and Weiwei Wang, Diverse LEA (late embryogenesis abundant) and LEA-like genes and their responses to hypersaline stress in post-diapause embryonic development of Artemia franciscana, Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 160, 1, (32), (2011).
- Yuichi Nakahara, Shigeo Imanishi, Kanako Mitsumasu, Yasushi Kanamori, Ken-ichi Iwata, Masahiko Watanabe, Takahiro Kikawada and Takashi Okuda, Cells from an anhydrobiotic chironomid survive almost complete desiccation, Cryobiology, 60, 2, (138), (2010).
- Alden H. Warner, Olga Miroshnychenko, Anna Kozarova, Panayiotis O. Vacratsis, Thomas H. MacRae, Jinnie Kim and James S. Clegg, Evidence for multiple group 1 late embryogenesis abundant proteins in encysted embryos of Artemia and their organelles, The Journal of Biochemistry, 10.1093/jb/mvq091, 148, 5, (581-592), (2010).
- Thomas H. MacRae, Gene expression, metabolic regulation and stress tolerance during diapause, Cellular and Molecular Life Sciences, 10.1007/s00018-010-0311-0, 67, 14, (2405-2424), (2010).
- Richard Cornette, Yasushi Kanamori, Masahiko Watanabe, Yuichi Nakahara, Oleg Gusev, Kanako Mitsumasu, Keiko Kadono-Okuda, Michihiko Shimomura, Kazuei Mita, Takahiro Kikawada and Takashi Okuda, Identification of Anhydrobiosis-related Genes from an Expressed Sequence Tag Database in the Cryptobiotic MidgePolypedilum vanderplanki(Diptera; Chironomidae), Journal of Biological Chemistry, 285, 46, (35889), (2010).
- Nadav Y. Denekamp, Richard Reinhardt, Michael Kube and Esther Lubzens, Late Embryogenesis Abundant (LEA) Proteins in Nondesiccated, Encysted, and Diapausing Embryos of Rotifers1, Biology of Reproduction, 82, 4, (714), (2010).
- Michael A. Menze, Leaf Boswell, Mehmet Toner and Steven C. Hand, Occurrence of Mitochondria-targeted Late Embryogenesis Abundant (LEA) Gene in Animals Increases Organelle Resistance to Water Stress, Journal of Biological Chemistry, 284, 16, (10714), (2009).
- Ralph O. Schill, Brahim Mali, Thomas Dandekar, Martina Schnölzer, Dirk Reuter and Marcus Frohme, Molecular mechanisms of tolerance in tardigrades: New perspectives for preservation and stabilization of biological material, Biotechnology Advances, 27, 4, (348), (2009).
- Michelle A. Sharon, Anna Kozarova, James S. Clegg, Panayiotis O. Vacratsis and Alden H. Warner, Characterization of a group 1 late embryogenesis abundant protein in encysted embryos of the brine shrimp Artemia franciscana, Biochemistry and Cell Biology, 87, 2, (415), (2009).
- Michael A. Menze and Steven C. Hand, How do animal mitochondria tolerate water stress?, Communicative & Integrative Biology, 2, 5, (428), (2009).
- Xiaoming He, Alex Fowler, Michael Menze, Steve Hand and Mehmet Toner, Desiccation Kinetics and Biothermodynamics of Glass Forming Trehalose Solutions in Thin Films, Annals of Biomedical Engineering, 36, 8, (1428), (2008).
- Weiwei Wang, Bo Meng, Weihua Chen, Xiaomeng Ge, Siqi Liu and Jun Yu, A proteomic study on postdiapaused embryonic development of brine shrimp (Artemia franciscana), PROTEOMICS, 7, 19, (3580), (2007).
- Brett Janis, Clinton Belott and Michael A. Menze, Role of Intrinsic Disorder in Animal Desiccation Tolerance, PROTEOMICS, 1800067, (2018).




