Tree Genetics & Genomes

, 11:126 | Cite as

The complete peach dehydrin family: characterization of three recently recognized genes

  • Carole Leavel BassettEmail author
  • Kirsten M. Fisher
  • Robert E. FarrellJr.
Original Article
Part of the following topical collections:
  1. Genome Biology


Three genes encoding dehydrins have been previously described from peach. In the course of searching the peach genome, three additional members of this stress-associated family were recognized, PpDhn4-6. PpDhn1 and 6 have no introns, whereas the remaining four genes have a single intron located near the 3′ end of the serine (S) tract. PpDHN2 was the only dehydrin with a predicted basic pI; pI predictions for the other dehydrins ranged from about 5.3 to about 6.3. None of the peach dehydrins have tryptophan residues, but, in contrast to most dehydrins, three (PpDHN1, 3, and 4) have one or more cysteine residues. Phylogenetic analysis indicated a close relationship between PpDhn1 and 6 and PpDhn3 and 4. Expression analysis under low temperature and dehydration confirmed that PpDhn2 is the major responder to drought, while both PpDhn1 and 6 respond exclusively to cold. Comparison of the first 500 base pairs upstream of the translation start site revealed the presence of cis-elements associated with low temperature and drought/osmotic/salt and hormone response regulation.


Abiotic stress Gene expression Promoter comparison Woody plants 



We appreciate the expert technical assistance of Ms. Jing Ma in the expression studies. This work was supported in its entirety by the USDA, the Agricultural Research Service, CRIS project 8080-21000-022-00D.

Data archiving statement

The genes described herein can be found at the National Center for Biotechnology Information or the Genome Database for Rosaceae as follows: PpDhn 4: GenBank Accession No. XM_007200796, GDR Locus No. ppa026861m; PpDhn5: GenBank Accession No. XM_007201751, GDR Locus No. ppa010975m; and PpDhn6: GenBank Accession No. XM_007202386, GDR Locus No. ppa009997m. Promoter regions can be found under GenBank Accession numbers as follows: PpDhn1: AY819770, PpDhn2: AY819770, PpDhn3: EU286278; use 500 bases upstream of GDR scaffold_8:16894027…16894705 (− strand) for PpDhn4; scaffold_8:11638043…11641172 (− strand) for PpDhn5; and scaffold_7:17137970…17139156 (+ strand) for PpDhn6.

GenBank accession numbers for the grape dehydrin sequences are as follows: XM03631828 (VvDHN1a), XM022285883 (VvDHN2), CAN73166 (VvDHN3), and XM002285369 (VvDHN4). Arabidopsis dehydrin GenBank gene ID numbers for the polypeptides identified by gene name are as follows: At3g50980 (Xero1), At3g50970 (Xero2), At5g66400 (Rab18), At1g20450 (ERD10), At1g76180 (ERD14), and At1g20440 (COR47).

Supplementary material

11295_2015_923_MOESM1_ESM.docx (15 kb)
Fig. S1 The alignment was conducted using the T-Coffee program (Notredame et al. 2000; Di Tommaso et al. 2011). Additional alignment was done by hand to maximize matches to relevant sequence features, such as the Y domain, the S tract and the last K motif. Dashes indicate regions lacking in sequence matches; the K motif is underlined and the Y domain is highlighted in gray. Degenerate K motifs are indicated by a dotted underline. (DOCX 15 kb)
11295_2015_923_MOESM2_ESM.pdf (23 kb)
Fig. S2 Phylogenetic tree resulting from the maximum likelihood analysis of six peach dehydrins (−lnL 3669.353). Bootstrap support values > 50 % (100 replicates) are indicated above branches. (PDF 23 kb)
11295_2015_923_Fig9_ESM.jpg (1.2 mb)
Fig. S3

Intrinsic disorder profiles for PPDHN1 and 2. Amino acid sequences for the two predicted proteins were submitted to the DISOPRED server at PSIPRED (Ward et al. 2004). The graphic shows the DISOPRED3 disorder confidence levels relative to the amino acid positions as solid blue lines; solid orange lines represent confidence predictions on residuess involved in protein-protein interaction. The dashed line represents the threshold above which amino acids are regarded as disordered. (JPEG 1263 kb)

11295_2015_923_Fig10_ESM.jpg (1.3 mb)
Fig. S4

Intrinsic disorder profiles for PPDHN3 and 4. The legend is the same as that for Figure S3. (JPEG 1311 kb)

11295_2015_923_Fig11_ESM.jpg (1.2 mb)
Fig. S5

Intrinsic disorder profiles for PPDHN5. Two polypeptides are predicted beginning at different translation start sites. PPDHN5 begins at MAQIRDEYGN.... whereas PPDHN5B begins 22 residues 5' of the predicted PPDHN5 start site (MGLPFLISYFDRGLALFVKNTQ-MAQIRDEYGN...). (JPEG 1227 kb)

11295_2015_923_Fig12_ESM.jpg (886 kb)
Fig. S6

Intrinsic disorder profile for PPDHN6. The legend is the same as that for Figure S3. (JPEG 886 kb)

11295_2015_923_MOESM3_ESM.docx (15 kb)
Supplemental Table S1 (DOCX 14 kb)


  1. Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889CrossRefPubMedGoogle Scholar
  2. Alsheikh MK, Svensson JT, Randall SK (2005) Phosphorylation regulated ion-binding is a property shared by the acidic subclass dehydrins. Plant Cell Environ 28:1114–1122CrossRefGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  4. Artlip TS, Callahan AM, Bassett CL, Wisniewski ME (1997) Seasonal expression of a dehydrin gene in sibling deciduous and evergreen genotypes of peach (Prunus persica [L.] Batsch). Plant Mol Biol 33:61–70CrossRefPubMedGoogle Scholar
  5. Asghar R, Fenton RD, DeMason DA, Close TJ (1994) Nuclear and cytoplasmic localization of maize embryo and aleurone dehydrin. Protoplasma 177:87–94CrossRefGoogle Scholar
  6. Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought-, and ABA-regulated gene expression. Plant Mol Biol 24:701–713CrossRefPubMedGoogle Scholar
  7. Bassett CL, Wisniewski ME, Artlip TS, Norelli JL, Renaut J, Farrell RE Jr (2006) Global analysis of genes regulated by low temperature and photoperiod in peach bark. J Am Soc Hortic Sci 131:551–563Google Scholar
  8. Bassett CL, Wisniewski ME, Artlip TS, Richart G, Norelli JL, Farrell RE Jr (2009) Comparative expression and transcript initiation of three peach dehydrin genes. Planta 230:107–118CrossRefPubMedGoogle Scholar
  9. Block WB, Dangl JL, Hahlbrock K, Schulze LP (1990) Functional borders, genetic fine structure, and distance requirements of cis elements mediating light responsiveness of the parsley chalcone synthase promoter. Proc Natl Acad Sci U S A 87:5387–5391PubMedCentralCrossRefPubMedGoogle Scholar
  10. Blum T, Briesemeister S, Kohlbacher O (2009) MultiLoc2: integrating phylogeny and gene ontology terms improves subcellular localization prediction. BMC Bioinforma 10:274. doi: 10.1186/1471-2105-10-274 CrossRefGoogle Scholar
  11. Brameier M, Krings A, MacCallum RM (2007) NucPred—Predicting nuclear localization of proteins. Bioinformatics 23:1159–1160Google Scholar
  12. Briesemeister S, Blum T, Brady S, Lam Y, Kohlbacher O, Shatkay H (2009) SherLoc2: a high-accuracy hybrid method for predicting subcellular localization of proteins. J Proteome Res 8:5363–5366CrossRefPubMedGoogle Scholar
  13. Busk PK, Jensen AB, Pagès M (1997) Regulatory elements in vivo in the promoter of the abscisic acid responsive gene rab17 from maize. Plant J 11:1285–129CrossRefPubMedGoogle Scholar
  14. Casadio R, Martelli PL, Pierleoni A (2008) The prediction of protein subcellular localization from sequence: a shortcut to functional genome annotation. Brief Funct Genom Proteomics 7:63. doi: 10.1093/bfgp/eln003 CrossRefGoogle Scholar
  15. Ceroni A, Passerini A, Vullo A, Frasconi P (2006) DISULFIND: a disulfide bonding state and cysteine connectivity prediction server. Nucleic Acids Res 34:W177–W181PubMedCentralCrossRefPubMedGoogle Scholar
  16. Chang WC, Lee TY, Huang HD, Huand HY, Pan RL (2008) PlantPAN: plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene group. BMC Genomics 9:561PubMedCentralCrossRefPubMedGoogle Scholar
  17. Claeys M, Storms V, Sun H, Michoel T, Marchal K (2012) MotifSuite: workflow for probabilistic motif detections and assessment. Bioinformatics 28:193101932CrossRefGoogle Scholar
  18. Close TJ (1997) Dehydrins: a commonalty in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296CrossRefGoogle Scholar
  19. Close TJ, Fenton RD, Moonan F (1993) A view of plant dehydrins using antibodies specific to the carboxy terminal peptide. Plant Mol Biol 23:279–286CrossRefPubMedGoogle Scholar
  20. Close TJ, Kortt AA, Chandler PM (1989) A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13:95–108CrossRefPubMedGoogle Scholar
  21. Cooper SJ, Trinklein ND, Anton ED, Nguyen L, Myers RM (2006) Comprehensive analysis of transcriptional promoter structure and function in 1 % of the human genome. Genome Res 16:1–10PubMedCentralCrossRefPubMedGoogle Scholar
  22. Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C (2011) T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. doi: 10.1093/nar/gkr245 PubMedCentralPubMedGoogle Scholar
  23. Donald RGK, Cashmore AR (1990) Mutation of either G box or I box sequences profoundly affects expression from the Arabidopsis rbcS-1A promoter. EMBO J 9:1717–1726PubMedCentralPubMedGoogle Scholar
  24. Dure L III, Crouch M, Harada J, Ho T-HD, Mundy J, Quatrano R, Thomas T, Sund ZR (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12:475–486CrossRefPubMedGoogle Scholar
  25. Ezcurra I, Ellerström M, Wycliffe P, Stålberg K, Rask L (1999) Interaction between composite elements in the napA promoter: both the B-box ABA-responsive complex and the RY/G complex are necessary for seed-specific expression. Plant Mol Biol 40:699–709CrossRefPubMedGoogle Scholar
  26. Fisher KM (2008) Bayesian reconstruction of ancestral expression of the LEA gene families reveals propagule-derived desiccation tolerance in resurrection plants. Am J Bot 95:506–515CrossRefPubMedGoogle Scholar
  27. Galau GA, Hughes DW, Dure L III (1986) Abscisic acid induction of cloned cotton late embryogenesis-abundant (LEA) mRNAs. Plant Mol Biol 7:155–170CrossRefPubMedGoogle Scholar
  28. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Springer Science + Business Media, New York, pp 571–607CrossRefGoogle Scholar
  29. Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13–21CrossRefPubMedGoogle Scholar
  30. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442CrossRefPubMedGoogle Scholar
  31. Graff L, Obrdlik P, Yuan L, Loqué D, Frommer WB, von Wirén N (2011) N-terminal cysteines affect oligomer stability of the allosterically regulated ammonium transporter LeAMT1;1. J Exp Bot 62:1361–1373CrossRefPubMedGoogle Scholar
  32. Guruprasad K, Reddy BVB, Pandit MW (1990) Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Eng Des Sel 4:155–161CrossRefGoogle Scholar
  33. Hara M (2010) The multifunctionality of dehydrins: an overview. Plant Signal Behav 5:503–508CrossRefPubMedGoogle Scholar
  34. Hara M, Shinoda Y, Tanaka Y, Kuboi T (2009) DNA binding of citrus dehydrin promoter by zinc ion. Plant Cell Environ 32:532–541CrossRefPubMedGoogle Scholar
  35. Heyen BJ, Alsheikh MK, Smith EA, Torvik CF, Seals DF, Randall SK (2002) The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation. Plant Physiol 130:675–687PubMedCentralCrossRefPubMedGoogle Scholar
  36. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300PubMedCentralCrossRefPubMedGoogle Scholar
  37. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106CrossRefPubMedGoogle Scholar
  38. Jones DT, Taylor WR, Thorton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282PubMedGoogle Scholar
  39. Kosugi S, Hasebe M, Tomita M, Yanagawa H (2009) Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Nat Acad Sci USA 106:10171–10176Google Scholar
  40. Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147:381–390PubMedCentralCrossRefPubMedGoogle Scholar
  41. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132Google Scholar
  42. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van De Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327PubMedCentralCrossRefPubMedGoogle Scholar
  43. Lin K, Simossis VA, Taylor WR, Heringa J (2005) A simple and fast secondary structure prediction algorithm using hidden neural networks. Bioinformatics 21:152–159CrossRefPubMedGoogle Scholar
  44. Lisse T, Bartels D, Kalbitzer HR, Jaenicke R (1996) The recombinant dehydrin-like desiccation stress protein from the resurrection plant Craterostigma plantagineum displays no defined three-dimensional structure in its native state. Biol Chem 377:555–561PubMedGoogle Scholar
  45. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406PubMedCentralCrossRefPubMedGoogle Scholar
  46. Loake GJ, Faktor O, Lamb CJ, Dixon RA (1992) Combination of H-box (CCTACCN7CT) and G-box (CACGTG) cis-elements is necessary for feed-forward stimulation of a chalcone synthase promoter by the phenylpropanoid-pathway intermediate ρ-coumaric acid. Proc Natl Acad Sci U S A 89:9230–9234PubMedCentralCrossRefPubMedGoogle Scholar
  47. McGuffin LJ, Bryson K, Jones DT (2000) The PSIPRED protein structure prediction server. Bioinformatics 16:404–405CrossRefPubMedGoogle Scholar
  48. Mikkelsen MD, Thomashow MF (2009) A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. Plant J 60:328–339CrossRefPubMedGoogle Scholar
  49. Molina C, Grotewold E (2005) Genome wide analysis of Arabidopsis core promoters. BMC Genomics 6:25. doi: 10.1186/1471-2164-6-25 PubMedCentralCrossRefPubMedGoogle Scholar
  50. Mouillon J-M, Gustafsson P, Harryson P (2006) Structural investigation of disordered stress proteins. Comparison of full-length dehydrins with isolated peptides of their conserved segments. Plant Physiol 141:638–650PubMedCentralCrossRefPubMedGoogle Scholar
  51. Nakai K, Horton P (1999) PSORT: a program for detecting the sorting signals of proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–35CrossRefPubMedGoogle Scholar
  52. Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148CrossRefPubMedGoogle Scholar
  53. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217CrossRefPubMedGoogle Scholar
  54. Rinne PLH, Kaikuranta PLM, van der Plas LHW, van der Schoot C (1999) Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209:377–388CrossRefPubMedGoogle Scholar
  55. Rombauts S, Déhais P, Van Montagu M, Rouzé P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27:295–296PubMedCentralCrossRefPubMedGoogle Scholar
  56. Rost B (1999) Twilight zone of protein sequence alignments. Protein Eng 12:85–94CrossRefPubMedGoogle Scholar
  57. Shen Q, Ho T-HD (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-Box and a novel cis-acting element. Plant Cell 7:395–307CrossRefGoogle Scholar
  58. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417CrossRefPubMedGoogle Scholar
  59. Soulages JL, Kangmin K, Arrese EL, Walters C, Cushman JC (2003) Conformation of a group 2 late embryogenesis abundant protein from soybean. Evidence of poly (L-proline)-type II structure. Plant Physiol 131:963–975PubMedCentralCrossRefPubMedGoogle Scholar
  60. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci U S A 94:1035–1040PubMedCentralCrossRefPubMedGoogle Scholar
  61. Svensson J, Palva ET, Welin B (2000) Purification of recombinant Arabidopsis dehydrins by metal ion affinity chromatography. Protein Expr Purif 20:169–178CrossRefPubMedGoogle Scholar
  62. Thijs H, Molenberghs G, Michiels B, Verbeke G, Curran D (2002) Strategies to fit pattern-mixture models. Biostatistics 3:245CrossRefPubMedGoogle Scholar
  63. Tompa P, Bánki P, Bokor M, Kamasa P, Kovács D, Lasanda G, Tompa K (2006) Protein-water and protein-buffer interactions in the aqueous solution of an intrinsically unstructured plant dehydrin: NMR intensity and DSC aspects. Biophys J 91:2243–2249PubMedCentralCrossRefPubMedGoogle Scholar
  64. Verde I, Abbott AG, Scalabrin S et al (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494. doi: 10.1038/ng.2586 CrossRefPubMedGoogle Scholar
  65. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337:635–645CrossRefPubMedGoogle Scholar
  66. Welin BV, Olson A, Palva ET (1995) Structure and organization of two closely related low-temperature-induced dhn/lea/rab-like genes in Arabidopsis thaliana L. Heynh. Plant Mol Biol 29:391–395CrossRefPubMedGoogle Scholar
  67. Wisniewski ME, Bassett CL, Arora R (2004) Distribution and partial characterization of seasonally expressed proteins in different aged shoots and roots of ‘Loring’ peach (Prunus persica). Tree Physiol 24:339–345CrossRefPubMedGoogle Scholar
  68. Wisniewski ME, Bassett CL, Renaut J, Farrell RE Jr, Tworkoski T, Artlip TS (2006) Differential regulation of two dehydrin genes from peach (Prunus persica) by photoperiod, low temperature and water deficit. Tree Physiol 26:575–584CrossRefPubMedGoogle Scholar
  69. Wisniewski M, Webb R, Balsamo R, Close TJ, Yu X-M, Griffith M (1999) Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol Plant 105:600–608CrossRefGoogle Scholar
  70. Xiao H, Nassuth A (2006) Stress- and development-induced expression of spliced and unspliced transcripts from two highly similar dehydrin 1 genes in V. riparia and V. vinifera. Plant Cell Rep 25:968–977CrossRefPubMedGoogle Scholar
  71. Xu J, Zhang YX, Wei W, Han L, Guan ZQ, Wang Z, Chai TY (2008) BjDHNs confer heavy-metal tolerance in plants. Mol Biotechnol 38:91–98CrossRefPubMedGoogle Scholar
  72. Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264PubMedCentralCrossRefPubMedGoogle Scholar
  73. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94CrossRefPubMedGoogle Scholar
  74. Yang Y, He M, Zhu Z, Li S, Xu Y, Zhang C, Singer SD, Wang Y (2012) Identification of the dehydrin gene family from grapevine species and analysis of their responsiveness to various forms of abiotic and biotic stress. BMC Plant Biol 12:140PubMedCentralCrossRefPubMedGoogle Scholar
  75. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological datasets under the maximum likelihood criterion. Dissertation, University of TexasGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2015

Authors and Affiliations

  • Carole Leavel Bassett
    • 1
    Email author
  • Kirsten M. Fisher
    • 2
  • Robert E. FarrellJr.
    • 3
  1. 1.USDA, ARS, Appalachian Fruit Research Station (formerly)KeedysvilleUSA
  2. 2.Department of Biological SciencesCalifornia State University, Los AngelesLos AngelesUSA
  3. 3.Department of BiologyPennsylvania State University, YorkYorkUSA

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