Third-Generation Sequencing Reveals LncRNA-Regulated HSP Genes in the Populus x canadensis Moench Heat Stress Response
Long non-coding RNAs (lncRNAs) regulate plant responses to abiotic stresses. However, the short reads produced by second-generation sequencing technology make it difficult to accurately explore full-length transcripts, limiting the study of lncRNAs. In this study, we used third-generation long-read...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2020-05-01
|
| Series: | Frontiers in Genetics |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fgene.2020.00249/full |
| _version_ | 1818329194472407040 |
|---|---|
| author | Jiahong Xu Jiahong Xu Jiahong Xu Meng Fang Meng Fang Meng Fang Zhihao Li Zhihao Li Zhihao Li Maoning Zhang Maoning Zhang Maoning Zhang Xiaoyu Liu Xiaoyu Liu Xiaoyu Liu Yuanyuan Peng Yuanyuan Peng Yuanyuan Peng Yinglang Wan Jinhui Chen Jinhui Chen Jinhui Chen |
| author_facet | Jiahong Xu Jiahong Xu Jiahong Xu Meng Fang Meng Fang Meng Fang Zhihao Li Zhihao Li Zhihao Li Maoning Zhang Maoning Zhang Maoning Zhang Xiaoyu Liu Xiaoyu Liu Xiaoyu Liu Yuanyuan Peng Yuanyuan Peng Yuanyuan Peng Yinglang Wan Jinhui Chen Jinhui Chen Jinhui Chen |
| author_sort | Jiahong Xu |
| collection | DOAJ |
| description | Long non-coding RNAs (lncRNAs) regulate plant responses to abiotic stresses. However, the short reads produced by second-generation sequencing technology make it difficult to accurately explore full-length transcripts, limiting the study of lncRNAs. In this study, we used third-generation long-read sequencing technology with the PacBio Sequel and Illumina platform to explore the role of lncRNAs in the heat stress response of Populus x canadensis Moench trees. We using 382,034,416 short reads to correct 4,297,179 long reads by resulted in 66,657 full-length transcripts, representing 33,840 genes. Then, 753 putative lncRNAs were identified, including 658 sense lncRNAs (87.38%), 41 long intervening/intergenic non-coding RNAs (lincRNAs) (5.44%), 12 antisense lncRNAs (1.59%), and 42 sense intronic lncRNAs (5.58%). Using the criteria | log2FC| ≥ 1 and q-value < 0.05, 3,493 genes and 78 lncRNAs were differentially expressed under the heat treatment. Furthermore, 923 genes were detected as targets of 43 differently expressed lncRNAs by cis regulation. Functional annotation demonstrated that these target genes were related to unfolded protein binding, response to stress, protein folding, and response to stimulus. Lastly, we identified a lncRNA–gene interaction network consisting of four lncRNAs and six genes [Heat Shock Protein 82 (HSP82), HSP83, Disease Resistance Protein 27 (DRL27), DnaJ family protein (DNJH), and two other predicted protein-coding genes], which showed that lncRNAs could regulate HSP family genes in response to heat stress in Populus. Therefore, our third-generation sequencing has improved the description of the P. canadensis transcriptome. The potential lncRNAs and HSP family genes identified here present a genetic resource to improve our understanding of the heat-adaptation mechanisms of trees. |
| first_indexed | 2024-12-13T12:44:11Z |
| format | Article |
| id | doaj.art-8cdf9af7b8eb45ac9ba4f378cd89aa8a |
| institution | Directory Open Access Journal |
| issn | 1664-8021 |
| language | English |
| last_indexed | 2024-12-13T12:44:11Z |
| publishDate | 2020-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Genetics |
| spelling | doaj.art-8cdf9af7b8eb45ac9ba4f378cd89aa8a2022-12-21T23:45:32ZengFrontiers Media S.A.Frontiers in Genetics1664-80212020-05-011110.3389/fgene.2020.00249516366Third-Generation Sequencing Reveals LncRNA-Regulated HSP Genes in the Populus x canadensis Moench Heat Stress ResponseJiahong Xu0Jiahong Xu1Jiahong Xu2Meng Fang3Meng Fang4Meng Fang5Zhihao Li6Zhihao Li7Zhihao Li8Maoning Zhang9Maoning Zhang10Maoning Zhang11Xiaoyu Liu12Xiaoyu Liu13Xiaoyu Liu14Yuanyuan Peng15Yuanyuan Peng16Yuanyuan Peng17Yinglang Wan18Jinhui Chen19Jinhui Chen20Jinhui Chen21Key Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education/Engineering Research Center of Rare and Precious Tree Species in Hainan Province, College of Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Biology of Tropical Ornamental Plant Germplasm, College of Forestry, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, ChinaKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education/Engineering Research Center of Rare and Precious Tree Species in Hainan Province, College of Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Biology of Tropical Ornamental Plant Germplasm, College of Forestry, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaSchool of Life Sciences, Lanzhou University, Lanzhou, ChinaKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education/Engineering Research Center of Rare and Precious Tree Species in Hainan Province, College of Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Biology of Tropical Ornamental Plant Germplasm, College of Forestry, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, ChinaKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education/Engineering Research Center of Rare and Precious Tree Species in Hainan Province, College of Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Biology of Tropical Ornamental Plant Germplasm, College of Forestry, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, ChinaKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education/Engineering Research Center of Rare and Precious Tree Species in Hainan Province, College of Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Biology of Tropical Ornamental Plant Germplasm, College of Forestry, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, ChinaKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education/Engineering Research Center of Rare and Precious Tree Species in Hainan Province, College of Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Biology of Tropical Ornamental Plant Germplasm, College of Forestry, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, ChinaKey Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, Ministry of Education/Engineering Research Center of Rare and Precious Tree Species in Hainan Province, College of Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Biology of Tropical Ornamental Plant Germplasm, College of Forestry, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, ChinaLong non-coding RNAs (lncRNAs) regulate plant responses to abiotic stresses. However, the short reads produced by second-generation sequencing technology make it difficult to accurately explore full-length transcripts, limiting the study of lncRNAs. In this study, we used third-generation long-read sequencing technology with the PacBio Sequel and Illumina platform to explore the role of lncRNAs in the heat stress response of Populus x canadensis Moench trees. We using 382,034,416 short reads to correct 4,297,179 long reads by resulted in 66,657 full-length transcripts, representing 33,840 genes. Then, 753 putative lncRNAs were identified, including 658 sense lncRNAs (87.38%), 41 long intervening/intergenic non-coding RNAs (lincRNAs) (5.44%), 12 antisense lncRNAs (1.59%), and 42 sense intronic lncRNAs (5.58%). Using the criteria | log2FC| ≥ 1 and q-value < 0.05, 3,493 genes and 78 lncRNAs were differentially expressed under the heat treatment. Furthermore, 923 genes were detected as targets of 43 differently expressed lncRNAs by cis regulation. Functional annotation demonstrated that these target genes were related to unfolded protein binding, response to stress, protein folding, and response to stimulus. Lastly, we identified a lncRNA–gene interaction network consisting of four lncRNAs and six genes [Heat Shock Protein 82 (HSP82), HSP83, Disease Resistance Protein 27 (DRL27), DnaJ family protein (DNJH), and two other predicted protein-coding genes], which showed that lncRNAs could regulate HSP family genes in response to heat stress in Populus. Therefore, our third-generation sequencing has improved the description of the P. canadensis transcriptome. The potential lncRNAs and HSP family genes identified here present a genetic resource to improve our understanding of the heat-adaptation mechanisms of trees.https://www.frontiersin.org/article/10.3389/fgene.2020.00249/fullPopulus x canadensis Moenchthird-generation sequencingheat stresslncRNAsheat shock protein |
| spellingShingle | Jiahong Xu Jiahong Xu Jiahong Xu Meng Fang Meng Fang Meng Fang Zhihao Li Zhihao Li Zhihao Li Maoning Zhang Maoning Zhang Maoning Zhang Xiaoyu Liu Xiaoyu Liu Xiaoyu Liu Yuanyuan Peng Yuanyuan Peng Yuanyuan Peng Yinglang Wan Jinhui Chen Jinhui Chen Jinhui Chen Third-Generation Sequencing Reveals LncRNA-Regulated HSP Genes in the Populus x canadensis Moench Heat Stress Response Frontiers in Genetics Populus x canadensis Moench third-generation sequencing heat stress lncRNAs heat shock protein |
| title | Third-Generation Sequencing Reveals LncRNA-Regulated HSP Genes in the Populus x canadensis Moench Heat Stress Response |
| title_full | Third-Generation Sequencing Reveals LncRNA-Regulated HSP Genes in the Populus x canadensis Moench Heat Stress Response |
| title_fullStr | Third-Generation Sequencing Reveals LncRNA-Regulated HSP Genes in the Populus x canadensis Moench Heat Stress Response |
| title_full_unstemmed | Third-Generation Sequencing Reveals LncRNA-Regulated HSP Genes in the Populus x canadensis Moench Heat Stress Response |
| title_short | Third-Generation Sequencing Reveals LncRNA-Regulated HSP Genes in the Populus x canadensis Moench Heat Stress Response |
| title_sort | third generation sequencing reveals lncrna regulated hsp genes in the populus x canadensis moench heat stress response |
| topic | Populus x canadensis Moench third-generation sequencing heat stress lncRNAs heat shock protein |
| url | https://www.frontiersin.org/article/10.3389/fgene.2020.00249/full |
| work_keys_str_mv | AT jiahongxu thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT jiahongxu thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT jiahongxu thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT mengfang thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT mengfang thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT mengfang thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT zhihaoli thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT zhihaoli thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT zhihaoli thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT maoningzhang thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT maoningzhang thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT maoningzhang thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT xiaoyuliu thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT xiaoyuliu thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT xiaoyuliu thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT yuanyuanpeng thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT yuanyuanpeng thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT yuanyuanpeng thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT yinglangwan thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT jinhuichen thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT jinhuichen thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse AT jinhuichen thirdgenerationsequencingrevealslncrnaregulatedhspgenesinthepopulusxcanadensismoenchheatstressresponse |