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Genome-wide analysis of the Thaumatin-like gene family in Qingke (Hordeum vulgare L. var. nudum) uncovers candidates involved in plant defense against biotic and abiotic stresses

Wang, Le, Xu, Zepeng, Yin, Wei, Xu, Kai, Wang, Shuai, Shang, Qianhan, Sa, Wei, Liang, Jian, Wang, Li·2022·Frontiers in Plant Science
DOI 10.3389/fpls.2022.912296PMC PMC9428612
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Abstract

Thaumatin-like proteins (TLPs) participate in the defense responses of plants as well as their growth and development processes, including seed germination. Yet the functioning of TLP family genes, in addition to key details of their encoded protein products, has not been thoroughly investigated for Qingke ( Hordeum vulgare L. var. nudum ). Here, a total of 36 TLP genes were identified in the genome of Qingke via HMM profiling. Of them, 25 TLPs contained a signal peptide at the N-terminus, with most proteins predicted to localize in the cytoplasm or outer membrane. Sequence alignment and motif analysis revealed that the five REDDD residues required for β-1,3-glucanase activity were conserved in 21 of the 36 Qingke TLPs. Phylogenetically, the TLPs in plants are clustered in 10 major groups. Our analysis of gene structure did not detect an intron in 15 Qingke TLPs whereas the other 21 did contain 1–7 introns. A diverse set of cis -acting motifs were found in the promoters of the 36 TLPs , including elements related to light, hormone, and stress responses, growth and development, circadian control, and binding sites of transcription factors, thus suggesting a multifaceted role of TLPs in Qingke. Expression analyses revealed the potential involvement of TLPs in plant defense against biotic and abiotic stresses. Taken together, the findings of this study deepen our understanding of the TLP family genes in Qingke, a staple food item in Tibet, which could strengthen future investigations of protein function in barley and its improved genetic engineering.

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FIGURE 1 Phylogenetic relationships of TLPs from Qingke, Hordeum vulgare, Cucumis melo, Oryza sativa, Brachypodium distachyon, and Arabidopsis thaliana. The phylogeny was constructed by MEGA 11, using the maximum likelihood (ML) method with 1000 bootstrap replicates. The inferred phylogeny was visualized in the Evolview online server. TLPs were classified into 10 groups, these indicated by different background colors.
FIGURE 1 Phylogenetic relationships of TLPs from Qingke, Hordeum vulgare, Cucumis melo, Oryza sativa, Brachypodium distachyon, and Arabidopsis thaliana. The phylogeny was constructed by MEGA 11, using the maximum likelihood (ML) method with 1000 bootstrap replicates. The inferred phylogeny was visualized in the Evolview online server. TLPs were classified into 10 groups, these indicated by different background colors.CC BY · PubMed Central
FIGURE 2 Conserved motifs identified in the Qingke TLP proteins. (A) Distribution of conserved motifs. (B) Sequence logo of motifs identified. The height of a symbol reflects the relative frequency of the amino acid at that position.
FIGURE 2 Conserved motifs identified in the Qingke TLP proteins. (A) Distribution of conserved motifs. (B) Sequence logo of motifs identified. The height of a symbol reflects the relative frequency of the amino acid at that position.CC BY · PubMed Central
FIGURE 3 Exon–intron structure of the Qingke TLP genes. Yellow boxes and black lines respectively indicate the exons and introns. The numbers (0, 1, and 2) indicate phases of introns.
FIGURE 3 Exon–intron structure of the Qingke TLP genes. Yellow boxes and black lines respectively indicate the exons and introns. The numbers (0, 1, and 2) indicate phases of introns.CC BY · PubMed Central
FIGURE 4 The electrostatic surface and the 3D structure of three Qingke TLPs. (A–C) The electrostatic surface of HOVUSG6558000, HOVUSG5063500 and HOVUSG5062800, respectively. Surfaces where the electrostatic potential is positive are colored blue, while those negatively charged are colored red. The arrows point to the acidic clefts formed by five conserved residues (REDDD). (D–F) The 3D structure of HOVUSG6558000, HOVUSG5063500 and HOVUSG5062800, with residues of the REDDD motif (red circles) and the bottom of acidic cleft forming regions (yellow circles) shown.
FIGURE 4 The electrostatic surface and the 3D structure of three Qingke TLPs. (A–C) The electrostatic surface of HOVUSG6558000, HOVUSG5063500 and HOVUSG5062800, respectively. Surfaces where the electrostatic potential is positive are colored blue, while those negatively charged are colored red. The arrows point to the acidic clefts formed by five conserved residues (REDDD). (D–F) The 3D structure of HOVUSG6558000, HOVUSG5063500 and HOVUSG5062800, with residues of the REDDD motif (red circles) and the bottom of acidic cleft forming regions (yellow circles) shown.CC BY · PubMed Central
FIGURE 5 Distribution of cis-elements in the promoters of Qingke TLP genes. Black lines indicate the promoters. Cis-elements differing in function are color-coded accordingly.
FIGURE 5 Distribution of cis-elements in the promoters of Qingke TLP genes. Black lines indicate the promoters. Cis-elements differing in function are color-coded accordingly.CC BY · PubMed Central
FIGURE 6 Expression of Qingke TLP genes in response to powdery mildew infection. Their expression levels at 0, 6, 36, 72, and 168 h post-inoculation (hpi) (A) in the powdery mildew-resistant cultivar Gannongda7 (G7) and (B) the powdery mildew-sensitive cultivar Zangqing13 (Z13). The RNA-seq data was downloaded from SRA database, and aligned to the Qingke genome to calculate the expression levels of TLP genes. Bars are colored according to the log2 (TPM + 1) values.
FIGURE 6 Expression of Qingke TLP genes in response to powdery mildew infection. Their expression levels at 0, 6, 36, 72, and 168 h post-inoculation (hpi) (A) in the powdery mildew-resistant cultivar Gannongda7 (G7) and (B) the powdery mildew-sensitive cultivar Zangqing13 (Z13). The RNA-seq data was downloaded from SRA database, and aligned to the Qingke genome to calculate the expression levels of TLP genes. Bars are colored according to the log2 (TPM + 1) values.CC BY · PubMed Central
FIGURE 7 Expression of Qingke TLP genes in response to drought and cold stresses. (A) Expression of Qingke TLP genes in drought-tolerant cultivar Z772 and drought-sensitive cultivar Z013 at 0, 1, and 5 h post-stress treatment. (B) Expression of Qingke TLP genes in the cold-tolerant cultivar Tibet148 subjected to 20/15°C (day/night), 3/1°C (day/night), –2°C (for 4 h) and –8°C (for 18 h) stress treatments. The RNA-seq data was downloaded from SRA database, and aligned to the Qingke genome to calculate the expression levels of TLP genes. Bars are colored according to the log2 (TPM + 1) values.
FIGURE 7 Expression of Qingke TLP genes in response to drought and cold stresses. (A) Expression of Qingke TLP genes in drought-tolerant cultivar Z772 and drought-sensitive cultivar Z013 at 0, 1, and 5 h post-stress treatment. (B) Expression of Qingke TLP genes in the cold-tolerant cultivar Tibet148 subjected to 20/15°C (day/night), 3/1°C (day/night), –2°C (for 4 h) and –8°C (for 18 h) stress treatments. The RNA-seq data was downloaded from SRA database, and aligned to the Qingke genome to calculate the expression levels of TLP genes. Bars are colored according to the log2 (TPM + 1) values.CC BY · PubMed Central
FIGURE 8 Relative expression levels of TLP genes responding to sodium salicylate (SA) and methyl jasmonate (MeJA) treatments. (A) Expression patterns of HOVUSG6558000, HOVUSG3036300, HOVUSG0170200, HOVUSG3065300 and HOVUSG5063600 in response to the SA treatment. (B) Expression patterns of HOVUSG6558000, HOVUSG3036300, HOVUSG0170200, HOVUSG3065300 and HOVUSG5063600 in response to the MeJA treatment. The expression level of the untreated control (0 h) was used to calculate the relative expression levels at different time-points after imposing the hormone treatments. Bars are the mean ± SD of expression levels obtained from three independent biological replicates.
FIGURE 8 Relative expression levels of TLP genes responding to sodium salicylate (SA) and methyl jasmonate (MeJA) treatments. (A) Expression patterns of HOVUSG6558000, HOVUSG3036300, HOVUSG0170200, HOVUSG3065300 and HOVUSG5063600 in response to the SA treatment. (B) Expression patterns of HOVUSG6558000, HOVUSG3036300, HOVUSG0170200, HOVUSG3065300 and HOVUSG5063600 in response to the MeJA treatment. The expression level of the untreated control (0 h) was used to calculate the relative expression levels at different time-points after imposing the hormone treatments. Bars are the mean ± SD of expression levels obtained from three independent biological replicates.CC BY · PubMed Central
FIGURE 9 Proposed working model for TLP-mediated plant defense response in Qingke. Blue arrows indicate the promotion of gene transcription, while the red arrow indicates its negative regulation.
FIGURE 9 Proposed working model for TLP-mediated plant defense response in Qingke. Blue arrows indicate the promotion of gene transcription, while the red arrow indicates its negative regulation.CC BY · PubMed Central

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Sorted by citations

Metadata

Authors
Wang, L., Xu, Z., Yin, W., Xu, K., Wang, S., Shang, Q., Sa, W., Liang, J., & Wang, L.
Venue
Frontiers in Plant Science
Publisher
Frontiers Media SA
Published
2022-08-17
Volume
13
ISSN
1664-462X
DOI
10.3389/fpls.2022.912296
PMC
PMC9428612
Cited by
26
References
0
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
Natural Science Foundation of Qinghai

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