CoChat
Sign Up
Cited by 59

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Molecular Characterization Revealed the Role of Thaumatin-Like Proteins of Bread Wheat in Stress Response

Sharma, Alok, Sharma, Himanshu, Rajput, Ruchika, Pandey, Ashutosh, Upadhyay, Santosh Kumar·2022·Frontiers in Plant Science
DOI 10.3389/fpls.2021.807448PMC PMC8786798

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Thaumatin-like proteins (TLPs) are related to pathogenesis-related-5 (PR-5) family and involved in stress response. Herein, a total of 93 TLP genes were identified in the genome of Triticum aestivum. Further, we identified 26, 27, 39, and 37 TLP genes in the Brachypodium distachyon , Oryza sativa , Sorghum bicolor , and Zea mays genomes for comparative characterization, respectively. They could be grouped into small and long TLPs with conserved thaumatin signature motif. Tightly clustered genes exhibited conserved gene and protein structure. The physicochemical analyses suggested significant differences between small and long TLPs. Evolutionary analyses suggested the role of duplication events and purifying selection in the expansion of the TLP gene family. Expression analyses revealed the possible roles of TLPs in plant development and abiotic and fungal stress response. Recombinant expression of TaTLP2-B in Saccharomyces cerevisiae provided significant tolerance against cold, heat, osmotic, and salt stresses. The results depicted the importance of TLPs in cereal crops that would be highly useful in future crop improvement programs.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fpls.2021.807448

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Figures

FIGURE 1 Chromosomal distribution and paralogous gene analysis of Thaumatin-like proteins (TLPs) in five cereal crops. Image depicts the scattered localization of TLP genes of (A) B. distachyon, (B) O. sativa, (C) S. bicolor, (D) T. aestivum, and (E) Z. mays at their respective chromosomes. Red lines and blue lines denote the tandem and segmental duplication events, respectively.
FIGURE 1 Chromosomal distribution and paralogous gene analysis of Thaumatin-like proteins (TLPs) in five cereal crops. Image depicts the scattered localization of TLP genes of (A) B. distachyon, (B) O. sativa, (C) S. bicolor, (D) T. aestivum, and (E) Z. mays at their respective chromosomes. Red lines and blue lines denote the tandem and segmental duplication events, respectively.CC BY · PubMed Central
FIGURE 2 Multiple sequence alignment of selected long and small TLPs of B. distachyon, O. sativa, S. bicolor, T. aestivum, and Z. mays with a known thaumatin protein sequence. Figure shows the alignment of long (OsTLP5, SbTLP2, BdTLP13, ZmTLP13, and TaTLP1-A) and small (BdTLP10, OsTLP25, ZmTLP6, SbTLP29, and TaTLP6-B) TLPs with a known thaumatin (P02883.2| THM1_THADA) protein sequence. The characteristic thaumatin signature motif is shown in the sky blue box. All the conserved cysteine residues were marked with an asterisk. The REDDD motif was marked with a red circle. The FF hydrophobic motif and bottom of acidic cleft forming regions are marked with a green triangle and brown box, respectively. The conserved regions of the thaumatin domain are marked with a black line.
FIGURE 2 Multiple sequence alignment of selected long and small TLPs of B. distachyon, O. sativa, S. bicolor, T. aestivum, and Z. mays with a known thaumatin protein sequence. Figure shows the alignment of long (OsTLP5, SbTLP2, BdTLP13, ZmTLP13, and TaTLP1-A) and small (BdTLP10, OsTLP25, ZmTLP6, SbTLP29, and TaTLP6-B) TLPs with a known thaumatin (P02883.2| THM1_THADA) protein sequence. The characteristic thaumatin signature motif is shown in the sky blue box. All the conserved cysteine residues were marked with an asterisk. The REDDD motif was marked with a red circle. The FF hydrophobic motif and bottom of acidic cleft forming regions are marked with a green triangle and brown box, respectively. The conserved regions of the thaumatin domain are marked with a black line.CC BY · PubMed Central
FIGURE 3 Phylogenetic tree analysis of A. thaliana, B. distachyon, O. sativa. S, bicolor, T. aestivum, and Z. mays using full-length peptide of TLPs. The figure shows the phylogenetic tree of TLPs, built by the maximum likelihood approach with 1000 bootstrap values using MEGA X software. The phylogenetic tree displays the clustering of TLPs of six plant species in I-XI different groups, each group is colored differently. The TLPs from each plant are marked with a different color.
FIGURE 3 Phylogenetic tree analysis of A. thaliana, B. distachyon, O. sativa. S, bicolor, T. aestivum, and Z. mays using full-length peptide of TLPs. The figure shows the phylogenetic tree of TLPs, built by the maximum likelihood approach with 1000 bootstrap values using MEGA X software. The phylogenetic tree displays the clustering of TLPs of six plant species in I-XI different groups, each group is colored differently. The TLPs from each plant are marked with a different color.CC BY · PubMed Central
FIGURE 4 Subcellular localization analysis of TaTLP2-B by YFP fusion. The YFP fluorescence depicts the localization of TaTLP2-B protein majorly in the extracellular region.
FIGURE 4 Subcellular localization analysis of TaTLP2-B by YFP fusion. The YFP fluorescence depicts the localization of TaTLP2-B protein majorly in the extracellular region.CC BY · PubMed Central
FIGURE 5 Expression analysis of TLP genes of B. distachyon (BdTLP), O. sativa (OsTLP). S. bicolor (SbTLP), T. aestivum (TaTLP), and Z. mays (ZmTLP) under various tissue and developmental stages. Heat maps (A–E) show the clustering and expression profiling of TLP genes in (A) B. distachyon, (B) O. sativa, (C) S. bicolor, (D) T. aestivum, and (E) Z. mays. The different clusters are formed based on expression values of TLP genes in the respective crop, which are represented with different colors. The color bar depicts the upregulated and downregulated expression with red and green colors, respectively.
FIGURE 5 Expression analysis of TLP genes of B. distachyon (BdTLP), O. sativa (OsTLP). S. bicolor (SbTLP), T. aestivum (TaTLP), and Z. mays (ZmTLP) under various tissue and developmental stages. Heat maps (A–E) show the clustering and expression profiling of TLP genes in (A) B. distachyon, (B) O. sativa, (C) S. bicolor, (D) T. aestivum, and (E) Z. mays. The different clusters are formed based on expression values of TLP genes in the respective crop, which are represented with different colors. The color bar depicts the upregulated and downregulated expression with red and green colors, respectively.CC BY · PubMed Central
FIGURE 6 Expression profiling of TLP genes of T. aestivum under biotic and abiotic stress conditions. Heat maps (A–C) show the clustering and expression profiling of TaTLP genes under (A) Blumeria graminis (Bgt) and Puccinia striiformis (Pst), (B) heat (HS), osmotic (OS), and combined heat and osmotic (HO), and (C) salt stress conditions. The clustering of TaTLP genes in each heat map is based on their expression pattern in respective stress conditions. The color bar shows high and low expressions with red and green colors, respectively.
FIGURE 6 Expression profiling of TLP genes of T. aestivum under biotic and abiotic stress conditions. Heat maps (A–C) show the clustering and expression profiling of TaTLP genes under (A) Blumeria graminis (Bgt) and Puccinia striiformis (Pst), (B) heat (HS), osmotic (OS), and combined heat and osmotic (HO), and (C) salt stress conditions. The clustering of TaTLP genes in each heat map is based on their expression pattern in respective stress conditions. The color bar shows high and low expressions with red and green colors, respectively.CC BY · PubMed Central
FIGURE 7 qRT-PCR analysis of eight TaTLP genes. Expression patterns in the form of fold changes have been shown in the bar graphs. (A,C,E,G,I,K,M,O) Show expression of TaTLP2-B, TaTLP5-D, TaTLP7-D, TaTLP9-D, TaTLP10-D, TaTLP14-B1, TaTLP25-B, and TaTLP29-A genes, under HS, OS, and HO stress conditions, while (B,D,F,H,J,L,N,P) shows the expression pattern of these genes under salt stress, respectively. Significance between the control and treated conditions is carried using a two-tailed student’s t-test. The ns, *, **, and *** markings represent the significance at p-value > 0.05, ≤0.05, ≤0.01, ≤0.001, respectively.
FIGURE 7 qRT-PCR analysis of eight TaTLP genes. Expression patterns in the form of fold changes have been shown in the bar graphs. (A,C,E,G,I,K,M,O) Show expression of TaTLP2-B, TaTLP5-D, TaTLP7-D, TaTLP9-D, TaTLP10-D, TaTLP14-B1, TaTLP25-B, and TaTLP29-A genes, under HS, OS, and HO stress conditions, while (B,D,F,H,J,L,N,P) shows the expression pattern of these genes under salt stress, respectively. Significance between the control and treated conditions is carried using a two-tailed student’s t-test. The ns, *, **, and *** markings represent the significance at p-value > 0.05, ≤0.05, ≤0.01, ≤0.001, respectively.CC BY · PubMed Central
FIGURE 8 Comparative expression analysis of duplicated gene pairs in T. aestivum. (A–E) Represent the comparative expression pattern of paralogous TaTLPs under various tissue and developmental stages. Based on their expression trend, TaTLPs are categorized into the retention of function (A–C) and pseudo functionalization types (D,E).
FIGURE 8 Comparative expression analysis of duplicated gene pairs in T. aestivum. (A–E) Represent the comparative expression pattern of paralogous TaTLPs under various tissue and developmental stages. Based on their expression trend, TaTLPs are categorized into the retention of function (A–C) and pseudo functionalization types (D,E).CC BY · PubMed Central
FIGURE 9 Spot assay of recombinant Saccharomyces cerevisiae (yeast) cells under various stress conditions. (A) Shows similar growth of both TaTLP2-B (pYES2.1-TaTLP2-B) and control vector (pYES2.1/V5-His/lacZ) containing yeast cells under control conditions. (B–F) Shows the spot assay analysis of TaTLP2-B and control vector containing yeast cells in (B) cold (4°C), (C) osmotic (30% PEG), (D) heat (37°C), (E) combined heat and osmotic (37°C and 30% PEG), and (F) salt (1M NaCl) stress conditions, respectively.
FIGURE 9 Spot assay of recombinant Saccharomyces cerevisiae (yeast) cells under various stress conditions. (A) Shows similar growth of both TaTLP2-B (pYES2.1-TaTLP2-B) and control vector (pYES2.1/V5-His/lacZ) containing yeast cells under control conditions. (B–F) Shows the spot assay analysis of TaTLP2-B and control vector containing yeast cells in (B) cold (4°C), (C) osmotic (30% PEG), (D) heat (37°C), (E) combined heat and osmotic (37°C and 30% PEG), and (F) salt (1M NaCl) stress conditions, respectively.CC BY · PubMed Central

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 1 references

Research works printed but not linked: 84

  1. Abad, 1996, Antifungal activity of tobacco osmotin has specificity and involves plasma membrane permeabilization., Plant Sci., 118, 11, 10.1016/0168-9452(96)04420-2 · DOI
  2. Ahmed, 2013, Molecular characterization of thaumatin family genes related to stresses in Brassica rapa., Sci. Hortic., 152, 26, 10.1016/j.scienta.2013.01.007 · DOI
  3. Appels, 2018, Shifting the limits in wheat research and breeding using a fully annotated reference genome., Science, 361, 10.1126/science.aar7191 · DOI
  4. Bailey, 2009, MEME SUITE: tools for motif discovery and searching., Nucleic Acids Res., 37, W202, 10.1093/nar/gkp335 · DOI · Paper page
  5. Cao, 2016, Expansion and evolution of thaumatin-like protein (TLP) gene family in six plants., Plant Growth Regul., 79, 299, 10.1007/s10725-015-0134-y · DOI
  6. Choulet, 2014, Structural and functional partitioning of bread wheat chromosome 3B., Science, 345, 10.1126/science.1249721 · DOI
  7. Christensen, 2002, The molecular characterization of two barley proteins establishes the novel PR-17 family of pathogenesis-related proteins., Mol. Plant Pathol., 3, 135, 10.1046/j.1364-3703.2002.00105.x · DOI
  8. Corpet, 1988, Multiple sequence alignment with hierarchical clustering., Nucleic Acids Res., 16, 10881, 10.1093/nar/16.22.10881 · DOI
  9. Cserzo, 2004, TM or not TM: transmembrane protein prediction with low false positive rate using DAS-TMfilter., Bioinformatics, 20, 136, 10.1093/bioinformatics/btg394 · DOI
  10. Cui, 2021, Transgenic expression of TaTLP1, a thaumatin-like protein gene, reduces susceptibility to common root rot and leaf rust in wheat., Crop J., 9, 1214, 10.1016/J.CJ.2021.03.021 · DOI
  11. Datta, 1999, Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease., Theor. Appl. Genet., 98, 1138, 10.1007/s001220051178 · DOI
  12. Edgar, 2004, MUSCLE: multiple sequence alignment with high accuracy and high throughput., Nucleic Acids Res., 32, 1792, 10.1093/nar/gkh340 · DOI · Paper page
  13. Ellegren, 2008, Comparative genomics and the study of evolution by natural selection., Mol. Ecol., 17, 4586, 10.1111/j.1365-294X.2008.03954.x · DOI
  14. Emanuelsson, 2000, Predicting subcellular localization of proteins based on their N-terminal amino acid sequence., J. Mol. Biol., 300, 1005, 10.1006/jmbi.2000.3903 · DOI
  15. Fierens, 2009, Biochemical and structural characterization of TLXI, the Triticum aestivum L. thaumatin-like xylanase inhibitor., J. Enzyme Inhib. Med. Chem., 24, 646, 10.1080/14756360802321831 · DOI
  16. Fils-Lycaon, 1996, A cherry protein and its gene, abundantly expressed in ripening fruit, have been identified as thaumatin-like., Plant Physiol., 111, 269, 10.1104/pp.111.1.269 · DOI
  17. Gasteiger, 2005, Protein identification and analysis tools on the ExPASy Server, The Proteomics Protocols Handbook, 10.1385/1-59259-890-0:571 · DOI
  18. Gaut, 2002, Evolutionary dynamics of grass genomes., New Phytol., 154, 15, 10.1046/j.1469-8137.2002.00352.x · DOI
  19. Gaut, 1996, Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL., Proc. Natl. Acad. Sci. U.S.A., 93, 10.1073/PNAS.93.19.10274 · DOI
  20. Gou, 2007, Gene expression and metabolite profiles of cotton fiber during cell elongation and secondary cell wall synthesis., Cell Res., 17, 422, 10.1038/sj.cr.7310150 · DOI
  21. Grenier, 1999, Some thaumatin-like proteins hydrolyse polymeric β-1,3-glucans., Plant J., 19, 473, 10.1046/J.1365-313X.1999.00551.X · DOI
  22. Haas, 2013, De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis., Nat. Protoc., 8, 1494, 10.1038/nprot.2013.084 · DOI · Paper page
  23. He, 2021, Boltlp1, a thaumatin-like protein gene, confers tolerance to salt and drought stresses in broccoli (Brassica oleracea l. var. italica)., Int. J. Mol. Sci., 22, 10.3390/IJMS222011132/S1 · DOI
  24. He, 2017, Overexpression of a thaumatin-like protein gene from Vitis amurensis improves downy mildew resistance in Vitis vinifera grapevine., Protoplasma, 254, 1579, 10.1007/s00709-016-1047-y · DOI
  25. Higo, 1998, PLACE: a database of plant cis -acting regulatory DNA elements., Nucleic Acids Res., 26, 358, 10.1093/nar/26.1.358 · DOI
  26. Hiroyuki, 2008, Regulation of expression of rice thaumatin-like protein: inducibility by elicitor requires promoter W-box elements., Plant Cell Rep., 27, 1521, 10.1007/s00299-008-0536-7 · DOI
  27. Horton, 2007, WoLF PSORT: protein localization predictor., Nucleic Acids Res., 35, W585, 10.1093/nar/gkm259 · DOI
  28. Hu, 2015, GSDS 2.0: an upgraded gene feature visualization server., Bioinformatics, 31, 1296, 10.1093/bioinformatics/btu817 · DOI
  29. Huang, 2002, Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat., Proc. Natl. Acad. Sci. U.S.A., 99, 8133, 10.1073/pnas.072223799 · DOI
  30. Käll, 2004, A combined transmembrane topology and signal peptide prediction method., J. Mol. Biol., 338, 1027, 10.1016/j.jmb.2004.03.016 · DOI
  31. King, 2007, ngLOC: an n-gram-based Bayesian method for estimating the subcellular proteomes of eukaryotes., Genome Biol., 8, 10.1186/gb-2007-8-5-r68 · DOI
  32. Kombrink, 1997, Pathogenesis-related proteins and plant defense, Plant Relationships, 107, 10.1007/978-3-662-10370-8_7 · DOI
  33. Kumar, 2018, MEGA X: molecular evolutionary genetics analysis across computing platforms., Mol. Biol. Evol., 35, 1547, 10.1093/molbev/msy096 · DOI
  34. Kuwabara, 2002, Abscisic acid- and cold-induced thaumatin-like protein in winter wheat has an antifungal activity against snow mould, Microdochium nivale., Physiol. Plant., 115, 101, 10.1034/j.1399-3054.2002.1150112.x · DOI
  35. Lei, 2021, Genome-wide identification of PYL gene family in wheat: evolution, expression and 3D structure analysis., Genomics, 113, 854, 10.1016/j.ygeno.2020.12.017 · DOI
  36. Letunic, 2015, SMART: recent updates, new developments and status in 2015., Nucleic Acids Res., 43, D257, 10.1093/nar/gku949 · DOI
  37. Li, 2020, Thaumatin-like protein genes of Panax notoginseng confers resistance to Alternaria panax., Physiol. Mol. Plant Pathol., 112, 10.1016/J.PMPP.2020.101537 · DOI
  38. Li, 2020, Comprehensive genome-wide analysis of thaumatin-like gene family in four cotton species and functional identification of GhTLP19 involved in regulating tolerance to Verticillium dahlia and drought., Front. Plant Sci., 11, 10.3389/fpls.2020.575015 · DOI
  39. Liu, The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function., Plant Cell Rep., 29, 419, 10.1007/s00299-010-0826-8 · DOI
  40. Liu, Expression profiling of a complex thaumatin-like protein family in western white pine., Planta, 231, 637, 10.1007/s00425-009-1068-2 · DOI
  41. Liu, 2020, Genome-wide identification, characterization and expression analysis of the TLP gene family in melon (Cucumis melo L.)., Genomics, 112, 2499, 10.1016/j.ygeno.2020.02.001 · DOI
  42. Liu, 2015, Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.)., BMC Plant Biol., 15, 10.1186/s12870-015-0511-8 · DOI
  43. Livak, 2001, Analysis of relative gene expression data using Real-Time quantitative PCR and the 2-ΔΔCT method., Methods, 25, 402, 10.1006/meth.2001.1262 · DOI · Paper page
  44. Mackintosh, 2007, Overexpression of defense response genes in transgenic wheat enhances resistance to Fusarium head blight., Plant Cell Rep., 26, 479, 10.1007/s00299-006-0265-8 · DOI
  45. Marcussen, 2014, Ancient hybridizations among the ancestral genomes of bread wheat., Science, 345, 10.1126/science.1250092 · DOI
  46. Misra, 2016, A thaumatin-like protein of Ocimum basilicum confers tolerance to fungal pathogen and abiotic stress in transgenic Arabidopsis., Sci. Rep., 6, 10.1038/srep25340 · DOI
  47. Munis, 2010, A thaumatin-like protein gene involved in cotton fiber secondary cell wall development enhances resistance against Verticillium dahliae and other stresses in transgenic tobacco., Biochem. Biophys. Res. Commun., 393, 38, 10.1016/j.bbrc.2010.01.069 · DOI
  48. Nagaraju, 2020, Genome-wide identification and transcriptional profiling of small heat shock protein gene family under diverse abiotic stress conditions in Sorghum bicolor (L.)., Int. J. Biol. Macromol., 142, 822, 10.1016/j.ijbiomac.2019.10.023 · DOI
  49. Naseri, 2012, In planta transformation of rice (Oryza sativa) using thaumatin-like protein gene for enhancing resistance to sheath blight., Afr. J. Biotechnol., 11, 7885, 10.5897/AJB11.3331 · DOI
  50. Neale, 1990, Chitinase, [beta]-1,3-glucanase, osmotin, and extensin Are expressed in tobacco explants during flower formation., Plant cell online, 2, 673, 10.1105/tpc.2.7.673 · DOI
  51. Nussbaumer, 2013, MIPS PlantsDB: a database framework for comparative plant genome research., Nucleic Acids Res., 41, D1144, 10.1093/nar/gks1153 · DOI
  52. Papatheodorou, 2018, Expression Atlas: gene and protein expression across multiple studies and organisms., Nucleic Acids Res., 46, D246, 10.1093/nar/gkx1158 · DOI
  53. Park, 2021, Thaumatin-like genes function in the control of both biotic stress signaling and ABA signaling pathways., Biochem. Biophys. Res. Commun., 567, 17, 10.1016/J.BBRC.2021.06.012 · DOI
  54. Paterson, 2004, Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics., Proc. Natl. Acad. Sci. U.S.A., 101, 9903, 10.1073/pnas.0307901101 · DOI
  55. Petre, 2011, Genome-wide analysis of eukaryote thaumatin-like proteins (TLPs) with an emphasis on poplar., BMC Plant Biol., 11, 10.1186/1471-2229-11-33 · DOI
  56. Pingault, 2015, Deep transcriptome sequencing provides new insights into the structural and functional organization of the wheat genome., Genome Biol., 16, 10.1186/s13059-015-0601-9 · DOI
  57. Rajam, 2007, Thaumatin gene confers resistance to fungal pathogens as well as tolerance to abiotic stresses in transgenic tobacco plants., Biol. Plant., 51, 135, 10.1007/s10535-007-0026-8 · DOI
  58. Rushton, 2010, WRKY transcription factors., Trends Plant Sci., 15, 247, 10.1016/j.tplants.2010.02.006 · DOI
  59. Sakamoto, 2006, Lentinula edodes tlg1 encodes a thaumatin-like protein that is involved in lentinan degradation and fruiting body senescence., Plant Physiol., 141, 793, 10.1104/pp.106.076679 · DOI
  60. Salzman, 1998, Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape., Plant Physiol., 117, 465, 10.1104/pp.117.2.465 · DOI
  61. Seo, 2006, An interactive power analysis tool for microarray hypothesis testing and generation., Bioinformatics, 22, 808, 10.1093/bioinformatics/btk052 · DOI
  62. Seo, 2008, Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination., Plant Cell Physiol., 49, 334, 10.1093/pcp/pcn011 · DOI
  63. Sharma, 2020, Thaumatin-like protein kinases: molecular characterization and transcriptional profiling in five cereal crops., Plant Sci., 290, 10.1016/j.plantsci.2019.110317 · DOI
  64. Sharma, 2020, Identification, characterization and expression profiling of cation-proton antiporter superfamily in Triticum aestivum L. and functional analysis of TaNHX4-B., Genomics, 112, 356, 10.1016/j.ygeno.2019.02.015 · DOI
  65. Sharma, 2014, Comprehensive expression analysis of rice armadillo gene family during abiotic stress and development., DNA Res., 21, 267, 10.1093/dnares/dst056 · DOI
  66. Shatters, 2006, Phylogenetic and structural relationships of the PR5 gene family reveal an ancient multigene family conserved in plants and select animal taxa., J. Mol. Evol., 63, 12, 10.1007/s00239-005-0053-z · DOI
  67. Shumayla, 2019, Genomic dissection and transcriptional profiling of cysteine-rich receptor-like kinases in five cereals and functional characterization of TaCRK68-A., Int. J. Biol. Macromol., 134, 316, 10.1016/j.ijbiomac.2019.05.016 · DOI
  68. Stothard, 2000, The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences., Biotechniques, 28, 10.2144/00286ir01 · DOI
  69. Suyama, 2006, PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments., Nucleic Acids Res., 34, W609, 10.1093/nar/gkl315 · DOI
  70. Tajima, 1993, Simple methods for testing the molecular evolutionary clock hypothesis., Genetics, 135, 599, 10.1093/genetics/135.2.599 · DOI
  71. Tyagi, 2021, Molecular characterization revealed the role of catalases under abiotic and arsenic stress in bread wheat (Triticum aestivum L.)., J. Hazardous Mater., 403, 10.1016/j.jhazmat.2020.123585 · DOI
  72. van der Wel, 1972, Isolation and characterization of thaumatin I and II, the sweet-tasting proteins from Thaumatococcus daniellii Benth., Eur. J. Biochem., 31, 221, 10.1111/j.1432-1033.1972.tb02522.x · DOI
  73. van Loon, 2006, Significance of inducible defense-related proteins in infected plants., Annu. Rev. Phytopathol., 44, 135, 10.1146/annurev.phyto.44.070505.143425 · DOI
  74. Velazhahan, 1999, The PR-5 family: thaumatin-like proteins, Pathogenesis-Related Proteins in Plants, 107
  75. Wang, 2020, TaTLP1 interacts with TaPR1 to contribute to wheat defense responses to leaf rust fungus., PLoS Genet., 16, 10.1371/journal.pgen.1008713 · DOI
  76. Wang, 2010, Characterization of a pathogenesis-related thaumatin-like protein gene TaPR5 from wheat induced by stripe rust fungus., Physiol. Plant., 139, 27, 10.1111/j.1399-3054.2009.01338.x · DOI
  77. Yan, 2017, Analysis of the grape (Vitis vinifera L.) thaumatin-like protein (TLP) gene family and demonstration that TLP29 contributes to disease resistance., Sci. Rep., 7, 10.1038/s41598-017-04105-w · DOI
  78. Yang, 1999, Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages., J. Mol. Evol., 48, 597, 10.1007/PL00006502 · DOI
  79. Yu, 2006, Prediction of protein subcellular localization., Proteins Struct. Funct. Bioinform., 64, 643, 10.1002/prot.21018 · DOI
  80. Zhang, 2014, Large-scale transcriptome comparison reveals distinct gene activations in wheat responding to stripe rust and powdery mildew., BMC Genomics, 15, 10.1186/1471-2164-15-898 · DOI
  81. Zhang, 2018, Functional analysis of a pathogenesis-related thaumatin-like protein gene TaLr35PR5 from wheat induced by leaf rust fungus., BMC Plant Biol., 18, 10.1186/s12870-018-1297-2 · DOI
  82. Zhang, 2005, A putative nucleoporin 96 is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1, constitutive 1., Plant Cell, 17, 1306, 10.1105/tpc.104.029926 · DOI
  83. Zhang, 2016, Expression partitioning of homeologs and tandem duplications contribute to salt tolerance in wheat (Triticum aestivum L.)., Sci. Rep., 6, 10.1038/srep21476 · DOI
  84. Zhang, 2007, Isolation of an osmotin-like protein gene from strawberry and analysis of the response of this gene to abiotic stresses., J. Plant Physiol., 164, 68, 10.1016/j.jplph.2006.02.002 · DOI

Cited by

Sorted by citations

See all 59

Metadata

Authors
Sharma, A., Sharma, H., Rajput, R., Pandey, A., & Upadhyay, S. K.
Venue
Frontiers in Plant Science
Publisher
Frontiers Media SA
Published
2022-01-11
Volume
12
ISSN
1664-462X
DOI
10.3389/fpls.2021.807448
PMC
PMC8786798
Cited by
59
References
1
Licence
creativecommons.org/licenses/by/4.0/ (vor)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Molecular Characterization Revealed the Role of Thaumatin-Like Proteins of Bread Wheat in Stress Response. https://app.cochat.ai/papers/10.3389/fpls.2021.807448
The paper
Sharma, A., Sharma, H., Rajput, R., Pandey, A., & Upadhyay, S. K. (2022). Molecular Characterization Revealed the Role of Thaumatin-Like Proteins of Bread Wheat in Stress Response. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2021.807448