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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

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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.

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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

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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 ›

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