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Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control

BACKGROUND: Self-incompatibility (SI) is under genetic control and prevents inbreeding depression in angiosperms. SI mechanisms are quite complicated and still poorly understood in many plants. Tea (Camellia sinensis L.) belonging to the family of Theaceae, exhibits high levels of SI and high hetero...

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Autores principales: Zhang, Cheng-Cai, Wang, Li-Yuan, Wei, Kang, Wu, Li-Yun, Li, Hai-Lin, Zhang, Fen, Cheng, Hao, Ni, De-Jiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4869358/
https://www.ncbi.nlm.nih.gov/pubmed/27183979
http://dx.doi.org/10.1186/s12864-016-2703-5
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author Zhang, Cheng-Cai
Wang, Li-Yuan
Wei, Kang
Wu, Li-Yun
Li, Hai-Lin
Zhang, Fen
Cheng, Hao
Ni, De-Jiang
author_facet Zhang, Cheng-Cai
Wang, Li-Yuan
Wei, Kang
Wu, Li-Yun
Li, Hai-Lin
Zhang, Fen
Cheng, Hao
Ni, De-Jiang
author_sort Zhang, Cheng-Cai
collection PubMed
description BACKGROUND: Self-incompatibility (SI) is under genetic control and prevents inbreeding depression in angiosperms. SI mechanisms are quite complicated and still poorly understood in many plants. Tea (Camellia sinensis L.) belonging to the family of Theaceae, exhibits high levels of SI and high heterozygosity. Uncovering the molecular basis of SI of the tea plant may enhance breeding and simplify genomics research for the whole family. RESULTS: The growth of pollen tubes following selfing and crossing was observed using fluorescence microscopy. Self-pollen tubes grew slower than cross treatments from 24 h to 72 h after pollination. RNA-seq was employed to explore the molecular mechanisms of SI and to identify SI-related genes in C. sinensis. Self and cross-pollinated styles were collected at 24 h, 48 h and 72 h after pollination. Six RNA-seq libraries (SP24, SP48, SP72, CP24 CP48 and CP72; SP = self-pollinated, CP = cross-pollinated) were constructed and separately sequenced. In total, 299.327 million raw reads were generated. Following assembly, 63,762 unigenes were identified, and 27,264 (42.76 %) unigenes were annotated in five public databases: NR, KOG, KEGG, Swiss-Port and GO. To identify SI-related genes, the fragments per kb per million mapped reads (FPKM) values of each unigene were evaluated. Comparisons of CP24 vs. SP24, CP48 vs. SP48 and CP72 vs. SP72 revealed differential expression of 3,182, 3,575 and 3,709 genes, respectively. Consequently, several ubiquitin-mediated proteolysis, Ca(2+) signaling, apoptosis and defense-associated genes were obtained. The temporal expression pattern of genes following CP and SP was analyzed; 6 peroxidase, 1 polyphenol oxidase and 7 salicylic acid biosynthetic process-related genes were identified. The RNA-seq data were validated by qRT-PCR of 15 unigenes. Finally, a unigene (CL25983Contig1) with strong homology to the S-RNase was analyzed. It was mainly expressed in styles, with dramatically higher expression in self-pollinated versus cross-pollinated tissues at 24 h post-pollination. CONCLUSIONS: The present study reports the transcriptome of styles after cross- and self-pollination in tea and offers novel insights into the molecular mechanism behind SI in C. sinensis. We believe that this RNA-seq dataset will be useful for improvement in C. sinensis as well as other plants in the Theaceae family. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2703-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-48693582016-05-18 Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control Zhang, Cheng-Cai Wang, Li-Yuan Wei, Kang Wu, Li-Yun Li, Hai-Lin Zhang, Fen Cheng, Hao Ni, De-Jiang BMC Genomics Research Article BACKGROUND: Self-incompatibility (SI) is under genetic control and prevents inbreeding depression in angiosperms. SI mechanisms are quite complicated and still poorly understood in many plants. Tea (Camellia sinensis L.) belonging to the family of Theaceae, exhibits high levels of SI and high heterozygosity. Uncovering the molecular basis of SI of the tea plant may enhance breeding and simplify genomics research for the whole family. RESULTS: The growth of pollen tubes following selfing and crossing was observed using fluorescence microscopy. Self-pollen tubes grew slower than cross treatments from 24 h to 72 h after pollination. RNA-seq was employed to explore the molecular mechanisms of SI and to identify SI-related genes in C. sinensis. Self and cross-pollinated styles were collected at 24 h, 48 h and 72 h after pollination. Six RNA-seq libraries (SP24, SP48, SP72, CP24 CP48 and CP72; SP = self-pollinated, CP = cross-pollinated) were constructed and separately sequenced. In total, 299.327 million raw reads were generated. Following assembly, 63,762 unigenes were identified, and 27,264 (42.76 %) unigenes were annotated in five public databases: NR, KOG, KEGG, Swiss-Port and GO. To identify SI-related genes, the fragments per kb per million mapped reads (FPKM) values of each unigene were evaluated. Comparisons of CP24 vs. SP24, CP48 vs. SP48 and CP72 vs. SP72 revealed differential expression of 3,182, 3,575 and 3,709 genes, respectively. Consequently, several ubiquitin-mediated proteolysis, Ca(2+) signaling, apoptosis and defense-associated genes were obtained. The temporal expression pattern of genes following CP and SP was analyzed; 6 peroxidase, 1 polyphenol oxidase and 7 salicylic acid biosynthetic process-related genes were identified. The RNA-seq data were validated by qRT-PCR of 15 unigenes. Finally, a unigene (CL25983Contig1) with strong homology to the S-RNase was analyzed. It was mainly expressed in styles, with dramatically higher expression in self-pollinated versus cross-pollinated tissues at 24 h post-pollination. CONCLUSIONS: The present study reports the transcriptome of styles after cross- and self-pollination in tea and offers novel insights into the molecular mechanism behind SI in C. sinensis. We believe that this RNA-seq dataset will be useful for improvement in C. sinensis as well as other plants in the Theaceae family. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2703-5) contains supplementary material, which is available to authorized users. BioMed Central 2016-05-17 /pmc/articles/PMC4869358/ /pubmed/27183979 http://dx.doi.org/10.1186/s12864-016-2703-5 Text en © Zhang et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Zhang, Cheng-Cai
Wang, Li-Yuan
Wei, Kang
Wu, Li-Yun
Li, Hai-Lin
Zhang, Fen
Cheng, Hao
Ni, De-Jiang
Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control
title Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control
title_full Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control
title_fullStr Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control
title_full_unstemmed Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control
title_short Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control
title_sort transcriptome analysis reveals self-incompatibility in the tea plant (camellia sinensis) might be under gametophytic control
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4869358/
https://www.ncbi.nlm.nih.gov/pubmed/27183979
http://dx.doi.org/10.1186/s12864-016-2703-5
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