Phylogenetic and Evolutionary Analysis of the Late Embryogenesis Abundant (LEA) Gene Product in Poaceae

Document Type : Research Article

Authors

1 Department of Plant Breeding and Biotechnology, College of Agriculture, University of Zabol, Zabol, Iran

2 Institute of Biotechnology, College of Agriculture, Shiraz University, Shiraz, Iran

10.22080/jgr.2021.20336.1229

Abstract

The late Embryogenesis Abundant (LEA) protein family obtains a group of stress-induced hyper-hydrophilic proteins that accumulate in response to cellular dehydration. They are generally unstructured polypeptides without a well-defined three-dimensional structure and have been identified in a wide range of organisms from bacteria to higher plants. Herein, we made a phylogenetic and evolutionary analysis for LEA proteins in Poaceae. The full-length LEA protein sequences were acquired by performing the sequence search of sequenced hva1 against Poaceae species in the non-redundant protein database by a BlastX search tool. The sequences were aligned with the Clustal Omega tool. The MEME suite searched for conserved blocks among each LEA protein sequence. Also, the evolutionary relationship among the LEA protein sequences evaluates using the MEGA tool. The results display close sequence similarity not only into the species but also between species. The results demonstrated that LEA proteins cluster into two large subgroups. The overall average evolutionary difference in LEA protein sequence pairs estimated as 0.4022 amino acid substitutions per site from averaging over all sequence pairs. The LEA protein sequences contain a significant percentage of glycine residues but lack cysteine and tryptophan residues. The results indicate the occurrence of homologs in the subgroup before the divergence of the species. However, the expansion of the gene number in the Poaceae was approved by the duplication events in the preexisting genes rather than by the appearance of the altered LEA gene. Our data will provide novel insights for further studies of the Late Embryogenesis Abundant protein family in Poaceae.

Keywords


Abba S, Ghignone S, Bonfante P. 2006. A dehydration inducible gene in the truffle Tuber borchii identifies a novel group of dehydrins. BMC Genom 7: 1-15.
Kader AA, Almeslemani M, Baghdady A, Alzubi H, Alasaad N, Basha NA, Hassan F. 2012. Isolation, characterization of the hva1 gene from Syrian barely varieties and cloning into binary plasmid vector. Int J Botany 8(3): 117-126.
Alpert P, Oliver MJ. 2002. Drying without dying. Desiccation and survival in plants. Wallingford: CABI Publishing, 3-43.
Alpert P. 2005. The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45: 685-695.
Altunoglu YC, Baloglu MC, Baloglu P, Yer EN, Kara S. 2017. Genome-wide identification and comparative expression analysis of LEA genes in watermelon and melon genomes. Physiol Mol Biol Plants 23: 5-21. 
Altunoglu YC, Baloglu PC, Nurten E et al. 2016. Identification and expression analysis of LEA gene family members in cucumber genome. Plant Growth Regul 80:225.
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-8.
Bray EA. 1997. Plant responses to water deficit. Trend Plant Sci 2: 48-54.
Browne JA, Dolan KM, Tyson T, Goyal K, Tunnacliffe A, Burnell AM. 2004. Dehydration-specific induction of hydrophilic protein genes in the anhydrobiotic nematode Aphelenchus avenae. Eukaryot Cell 3: 966-975.
Campos F, Cuevas-Velazquez C, Fares MA, Reyes JL, Covarrubias AA. 2013. Group 1 LEA proteins, an ancestral plant protein group, are also present in other eukaryotes, and in the archeae and bacteria domains. Mol Genet Genomics 288(10): 503-517.
Cao J, Li X. 2015. Identification and phylogenetic analysis of late embryogenesis abundant proteins family in tomato (Solanum lycopersicum). Planta 241: 757-772.
Cuming AC. 1999. LEA proteins. In R Casey, PR Shewry, eds, Seed Proteins. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 753-780.
Dellaporta SL, Wood J, Hicks JB. 1983. A plant DNA minipreparation: version II. Plant Mol Biol Rep 1: 19-21.
Dure L, Chilan CA. 1981. Development biochemistry of cottonseed embryogenesis and germination. XII. Purification and properties of principle storage proteins. Plant Physiol 68: 180-186.
Dure L, Crouch M, Harada J, Ho TH, Mundy J, Quatrano R, Thomas T, Sung ZR. 1989. Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12:475-486.
Dure L, Greenway, SC, Galau GA. 1981. Developmental biochemistry of cottonseed embryogenesis and germination, changing messenger ribonucleic acid populations as shown by in vitro protein synthesis. Biochemistry 20: 4162-4168.
Dure L. 1993. A repeating 11-mer amino acid motif and plant desiccation. Plant J 3: 363-369.
Felsenstein J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783-791.
Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Eddy SR. 2015. HMMER web server: 2015 update. Nucleic Acids Res 43: W30-W38.
Gao J, Lan T. 2016. Functional characterization of the late embryogenesis abundant (LEA) protein gene family from Pinus tabuliformis (Pinaceae) in Escherichia coli. Sci Rep 19467.
Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA. 2000. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J Biol Chem 275: 5668-5674.
Hand SC, Menze MA, Toner M, Boswell L, Moore D. 2011. LEA proteins during water stress: not just for plants anymore. Annu Rev Physiol 73, 115-134.
He JX, Fu JR. 1996. The research progresses in LEA proteins of seeds. Plant Physiol Commun 32(4): 241-246.
Hincha DK, Thalhammer A. 2012. LEA proteins: IDPs with versatile functions in cellular dehydration tolerance. Biochem Soc T 40:1000-1003
Hong-Bo S, Zong-Suo L, Ming-An S. 2005. LEA proteins in higher plants: Structure, function, gene expression, and regulation. Colloids Surf B Biointerfaces 45:131-135.
Hunault G, Jaspard E. 2010. LEAPdb: a database for the late embryogenesis abundant proteins. BMC Genomics 11: 1-9.
Hundertmark M, Hincha DK. 2008. LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9: 1-22.
Ibrahime M, Kibar U, Kazan K, Özmen CY, Mutaf F, Asci SD, Ergül A. 2019. Genome-wide identification of the LEA protein gene family in grapevine (Vitis vinifera L.). Tree Genet Genomes 15: 1-4.
Ingram J, Bartels D. 1996. The molecular basis of dehydration tolerance in plants. Annu Rev Plant Biol 47: 377-403.
Iturriaga G, Cushman MAF, Cushman JC. 2006. An EST catalog from the resurrection plant Selaginella lepidophylla reveals abiotic stress-adaptive genes. Plant Sci 170: 1173-1184.
Jaspard E, Macherel D, Hunault G. 2012. Computational and statistical analyses of amino acid usage and physicochemical properties of the twelve-late embryogenesis abundant protein classes. Plos One 16; 7(5): e36968.
Jin X, Cao D, Wang Z, Ma L, Tian K, Liu Y, Gong Z, Zhu X, Jiang C, Li Y. 2019. Genome-wide identification and expression analyses of the LEA protein gene family in tea plant reveal their involvement in seed development and abiotic stress responses. Sci Rep 9: 1-5.
Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275-282.
Kong H, Landherr LL, Frohlich MW, Leebens‐Mack J, Ma H, DePamphilis CW. 2007.  The pattern of gene duplication in the plant SKP1gene family in angiosperms: evidence for multi mechanisms of rapid gene birth. Plant J 50:873-885. 
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 3:1870-1874.
Liang Y, Xiong Z, Zheng J, Xu D, Zhu Z, Xiang J, Li M. 2016. Genome-wide identification, structural analysis and new insights into late embryogenesis abundant (LEA) gene family formation pattern in Brassica napus. Sci Rep 2:4265.
Liu H, Xing M, Yang W, Mu X, Wang X, Lu F, Zhang L. 2019. Genome-wide identification of and functional insights into the late embryogenesis abundant (LEA) gene family in bread wheat (Triticum aestivum). Sci Rep 9: 1-11.
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Lopez R. 2019. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47(W1): 636-641.
Magwanga RO, Lu P, Kirungu JN, Lu H, Wang X, Cai X, Liu F. 2018. Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton. BMC Genetics 19: 1-31.
Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York.
Oliver MJ, Dowd SE, Zaragoza J, Mauget SA, Payton PR. 2004. The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5: 89-107.
Oliver MJ, Tuba Z, Mishler BD. 2000. The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151: 85-100.
Proctor MC, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD. 2007. Desiccation-tolerance in bryophytes: a review. Bryologist 110: 595-621.
Reynolds TL, Bewley JD. 1993. Characterization of protein synthetic changes in a desiccation-tolerant fern, Polypodium virginianum: comparison of the effects of drying, rehydration, and abscisic acid. J Exp Bot 44: 921-928.
Rorat T. 2006. Plant dehydrins--tissue location, structure, and function. Cell Mol Biol Lett 11(4): 536-556.
Saavedra L, Svensson J, Carballo V, Izmendi D, Welin B, Vidal S. 2006. A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant J 45: 237-249.
Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
Sasaki K, Christov NK, Tsuda S, Imai R. 2014. Identification of a novel LEA protein involved in freezing tolerance in wheat. Plant Cell Physiol 55:139-147.
Singh TR, Bansal A. 2019. Gene duplication and speciation. Encycl Bioinf Comput Biol 3: 965-974.
Solomon A, Salomon R, Paperna I, Glazer I. 2000. Desiccation stress of entomopathogenic nematodes induces the accumulation of a novel heat-stable protein. Parasitology 121: 409-416.
Stacy RAP, Aalen RB. 1998. Identification of Sequence Homology Between the Internal Hydrophilic Repeated Motifs in Group 1 Late-Embryogenesis-Abundant Proteins in Plants and Hydrophilic Repeats of the General Stress Protein GsiB of Bacillus subtilis. Planta 206: 476-478.
Tamura K, Battistuzzi FU, Billing-Ross P, Murillo O, Filipski A, Kumar S. 2012. Estimating divergence times in large molecular phylogenies. Proc Natl Acad Sci 109:19333-19338.
Tanaka S, Ikeda K, Miyasaka H. 2004. Isolation of a new member of group 3 late embryogenesis abundant protein gene from a halotolerant green alga by a functional expression screening with cyanobacterial cells. FEMS Microbiol Lett 236: 41-45.
Thomashow MF. 1998. Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118: 1-7.
Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 2009. Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinf 25(9): 1189-91.
Wise MJ. 2003. LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinf 4: 1-19.
Zeng X, Ling H, Yang J, Li Y, Guo S. 2018. LEA proteins from Gastrodia elata enhance tolerance to low-temperature stress in Escherichia coli. Gene 646:136-142.