Abstract
The universal stress proteins (USPs) comprise a large family of proteins that has been found and characterized in a variety of organisms including plants. Intrinsic domains of these proteins are considered as one of the most ancient domains in all life forms. The first member of the USP family was isolated and extensively characterized in bacteria during the 1990s, demonstrating that the USP-containing proteins are phosphoproteins responsive to a variety of abiotic stress stimuli. Since then, many other members of the family have been characterized. Here, we present the isolation and characterization of two USP genes from Gossypium hirsutum, the most widely cultivated cotton species that has a serious impact in world’s economy. The two cotton USP genes, each in the form of two alleles, possess the same structural organization with their Arabidopsis homologues, possessing one intron sequence separating the coding sequence into two unequal parts, a large 5′-end part and a small 3′-end tail. In silico amino acid sequence analysis and three-dimensional modeling show the high levels of conservation in the USP domain, an indication that the cotton GhUSPs may function in a variety of developmental and stress-induced pathways. Moreover, expression analysis showed that while both are expressed in stems and meristems, although at different levels, only one of them is expressed in flowers. Upon salt treatment, both GhUSPs are transcriptionally activated, with the GhUSP1 reaching a peak within 30 min after the application of the stress stimuli, whereas activation of the GhUSP2 lasts longer.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aravind L, Anantharaman V, Koonin EV (2002) Monophyly of class I aminoacyl tRNA synthetase, USPA, ETFP, Photolyase, and PP-ATPase nucleotide-binding domains: implications for protein evolution in the RNA world. Proteins 48:1–14. doi:10.1002/prot.10064
Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201. doi:10.1093/bioinformatics/bti770
Becker JD, Moreira LM, Kapp D, Frosch SC, Pühler A, Perlick AM (2001) The nodulin VfENOD18 is an ATP-binding protein in infected cells of Vicia faba L. nodules. Plant Mol Biol 47:749–759. doi:10.1023/A:1013664311052
Chou MX, Wei XY, Chen DS, Zhou JC (2007) A novel nodule-enhanced gene encoding a putative universal stress protein from Astragalus sinicus. J Plant Physiol 164:764–772. doi:10.1016/j.jplph.2006.05.009
Foret S, Seneca F, de Jong D, Bieller A, Hemmrich G, Augustin R, Hayward DC, Ball EE, Bosch TCG, Agata K, Hassel M, Miller DJ (2011) Phylogenomics reveals an anomalous distribution of USP genes in metazoans. Mol Biol Evol 28:153–161. doi:10.1093/molbev/msq183
Freestone P, Trinei M, Clarke SC, Nystrom T, Norris V (1998) Tyrosine phosphorylation in Escherichia coli. J Mol Biol 279:1045–1051. doi:10.1006/jmbi.1998.1836
Hohnjec N, Kuster H, Albus U, Frosch SC, Becker JD, Puhler A, Perlick AM, Fruhling M (2000) The broad bean nodulin VfENOD18 is a member of the novel family of plant proteins with homologies to the bacterial MJ0577 superfamily. MGG 264:241–250. doi:10.1007/s004380000292
Jones PG, Cashel M, Glaser G, Neidhardt FC (1992) Function of a relaxed-like state following temperature downshifts in Escherichia coli. J Bacteriol 174:3903–3914
Kerk D, Bulgrien J, Smith DW, Gribskov M (2003) Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria. Plant Physiol 131:1209–1219. doi:10.1104/pp. 102.016006
Kvint K, Nachin L, Diez A, Nystrom T (2003) The bacterial universal stress protein: function and regulation. Curr Opin Microbiol 6:140–145. doi:10.1016/S1369-5274(03)00025-0
Lee JJ, Woodward AW, Chen ZJ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot 100:1391–1401. doi:10.1093/aob/mcm232
Li H, Luo J, Hemphill JK, Wang J, Gould J (2001) A rapid and high yielding DNA miniprep for cotton (Gossypium spp.). Plant Mol Biol Rep 19:183a–183e, http://link.springer.com/content/pdf/10.1007%2FBF02772162.pdf
Li W-T, Wei Y-M, Wang J-R, Liu C-J, Lan X-J, Jiang Q-T, Pu Z-E, Zheng Y-L (2010) Identification, localization and characterization of putative USP genes in barley. TAG 121:907–917. doi:10.1007/s00122-010-1359-9
Maqbool A, Zahur M, Husnain T, Riazuddin S (2009) GUSP1 and GUSP2, two drought-responsive genes in Gossypium arboreum have homology to universal stress proteins. Plant Mol Biol Rep 27:107–114. doi:10.1007/s11105-008-0049-0
Merkouropoulos G, Andreasson E, Hess D, Boller T, Peck SC (2008) An Arabidopsis protein phosphorylated in response to microbial elicitation, AtPHOS32, is a substrate of MAP kinases 3 and 6. J Biol Chem 283:10493–10499. doi:10.1074/jbc.M800735200
Nachin L, Nannmark U, Nystrom T (2005) Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J Bacteriol 187:6265–6272. doi:10.1128/JB.187.18.6265-6272.2005
O’Toole R, Williams HD (2003) Universal stress proteins and Mycobacterium tuberculosis. Res Microbiol 154:387–392. doi:10.1016/S0923-2508(03)00081-0
Rodriguez-Uribea L, Higbiea SM, Stewartb J-MD, Wilkinsc T, Lindemanna W, Sengupta-Gopalana C, Zhang J (2011) Identification of salt responsive genes using comparative microarray analysis in upland cotton (Gossypium hirsutum L.). Plant Sci 180:461–469. doi:10.1016/j.plantsci.2010.10.009
Sasaki T, Matsumoto T, Yamamoto K et al (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316. doi:10.1038/nature01184
Sauter M, Rzewuski G, Marwedel T, Lorbiecke R (2002) The novel ethylene-regulated gene OsUsp1 from rice encodes a member of a plant protein family related to prokaryotic universal stress proteins. J Exp Bot 53:2325–2331. doi:10.1093/jxb/erf096
Sousa MC, McKay DB (2001) Structure of the universal stress protein of Haemophilus influenzae. Structure 9:1135–1141. doi:10.1016/S0969-2126(01)00680-3
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092
van Bogelen RA, Hutton ME, Neidhardt FC (1990) Gene-protein database of Escherichia coli K-12: edition 3. Electrophoresis 11:1131–1166. doi:10.1002/elps.1150111205
Zarembinski TI, Hung LW, Muller-Dieckman HJ, Kim KK, Yokota H, Kim R, Kim SH (1998) Structure-based assignment of the biochemical function of a hypothetical protein: a test case of structural genomics. Proc Nat Acad Sci USA 95:15189–15193. doi:10.1073/pnas.95.26.15189
Zegzouti H, Jones B, Frasse P, Marty C, Maitre B, Latche A, Pech JC, Bouzayen M (1999) Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening related genes isolated by differential display. Plant J 18:589–600. doi:10.1046/j.1365-313x.1999.00483.x
Acknowledgments
This work was supported by grants awarded to Athanasios S. Tsaftaris.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Merkouropoulos, G., Tsaftaris, A.S. Differential Expression of Gossypium hirsutum USP-Related Genes, GhUSP1 and GhUSP2, During Development and upon Salt Stress. Plant Mol Biol Rep 31, 1539–1547 (2013). https://doi.org/10.1007/s11105-013-0630-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-013-0630-z