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Systematic identification and characterization of long non-coding RNAs involved in cytoplasmic male sterility in pepper (Capsicum annuum L.)

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Abstract

Long non-coding RNAs (lncRNAs) participate in many biological processes and play extremely important regulatory roles in animals and plants. However, little is known about lncRNAs and their functions in cytoplasmic male sterility (CMS) during the developmental process of floral buds in pepper. In the present study, we systematically identified lncRNAs in the pepper CMS line (9704A) and maintainer line (9704B) using high-throughput sequencing and bioinformatic analyses. A total of 10,655 putative lncRNAs were identified during the developmental process of floral buds, and 262, 298 and 905 differentially expressed lncRNAs (DELs) were obtained in three stages, respectively. Moreover, 1137 unique DELs were identified between 9704A and 9704B, and their cis and trans target protein-coding genes were predicted. We used Gene ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses to decipher the potential functions of DELs. The cell and cellular process GO terms were significantly enriched, and KEGG pathway analysis showed enrichments in the pathways for starch and sucrose metabolism genes, pentose and glucuronate interconversions, all of which were highly associated with pollen development. Besides, a regulatory network about the lncRNAs and the protein-coding genes involved in the formation of CMS was constructed. Our findings laid a foundation for further studies on the function of lncRNAs in pollen development and provided valuable insights into the regulatory mechanism underlying CMS.

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Data Availability

All of the RNA-Seq data generated in this study is available from the SRA-Archive (http://www.ncbi.nlm.nih.gov/sra) under the study accession number: SRP186136. The other supporting data are included as Additional files.

References

  • An N, Fan S, Wang YB, Zhang LZ, Gao C, Zhang D, Han MY (2018) Genome-wide identification, characterization and expression analysis of long non-coding RNAs in different tissues of apple. Gene 666:44–57

    Article  CAS  PubMed  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ariel F, Jegu T, Latrasse D, Romero-Barrios N, Christ A, Benhamed M, Crespi M (2014) Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol Cell 55:383–396

    Article  CAS  PubMed  Google Scholar 

  • Ariizumi T, Toriyama K (2012) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62:437–460

    Article  CAS  Google Scholar 

  • Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21:1453–1472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borodina T, Adjaye J, Sultan M (2011) Chapter five—A strand-specific library preparation protocol for RNA sequencing. Methods Enzymol 500:79–98

    Article  CAS  PubMed  Google Scholar 

  • Cabili MN, Cole T, Loyal G, Magdalena K, Barbara TV, Aviv R, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Gene Dev 25:1915–1927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casero D, Sandoval S, Seet CS, Scholes J, Zhu Y, Ha VL, Luong A, Parekh C, Crooks GM (2015) Long non-coding RNA profiling of human lymphoid progenitor cells reveals transcriptional divergence of B cell and T cell lineages. Nat Immunol 16:1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chekanova JA, Gregory BD, Reverdatto SV, Chen H, Kumar R, Hooker T, Yazaki J, Li P, Skiba N, Peng Q, Alonso J, Brukhin V, Grossniklaus U, Ecker JR, Belostotsky DA (2007) Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131:1340–1353

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    Article  CAS  PubMed  Google Scholar 

  • Chen GH, Ye XY, Zhang SY, Zhu SD, Yuan LY, Hou JF, Wang CG (2018) Comparative transcriptome analysis between fertile and CMS flower buds in Wucai (Brassica campestris L.). BMC Genomics 19:908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen SF, Zhou YQ, Chen YR, Gu J (2018) fastp:an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cole T, Adam R, Loyal G, Geo P, Daehwan K, Kelley DR, Harold P, Salzberg SL, Rinn JL, Lior P (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  Google Scholar 

  • Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, Mcpherson A, Szcześniak MW, Gaffney DJ, Elo LL, Zhang XG, Mortazavi A (2016) A survey of best practices for RNA-seq data analysis. Genome Biol 17:13. https://doi.org/10.1186/s13059-016-0881-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui J, Luan YS, Jiang N, Bao H, Meng J (2017) Comparative transcriptome analysis between resistant and susceptible tomato allows the identification of lncRNA16397 conferring resistance to Phytophthora infestans by co-expressing glutaredoxin. Plant J 89:577

    Article  CAS  PubMed  Google Scholar 

  • Ding JH, Lu Q, Ouyang YD, Mao HL, Zhang PB, Yao JL, Xu CG, Li XH, Xiao JH, Zhang QF (2012) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci USA 109(7):2654–2659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferguson AC, Pearce S, Band LR, Yang C, Ferjentsikova I, King J, Yuan Z, Zhang D, Wilson ZA (2017) Biphasic regulation of the transcription factor ABORTED MICROSPORES (AMS) is essential for tapetum and pollen development in Arabidopsis. New Phytol 213:778–790

    Article  CAS  PubMed  Google Scholar 

  • Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142:1004–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo WJ, Ho THD (2008) An abscisic acid-induced protein, HVA22, Inhibits gibberellin-mediated programmed cell death in cereal aleurone cells. Plant Physiol 147:1710–1722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heungsop S, Hwa-Soo S, Chen RJ, Harrison MJ (2010) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45:712–726

    Google Scholar 

  • Huang L, Cao J, Ye W, Liu T, Ye L Y (2008) Transcriptional differences between the male-sterile mutant bcms and wild-type Brassica campestris ssp. chinensis reveal genes related to pollen development. Plant Biol 10:342–355

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Dong H, Zhou D, Li M, Liu YH, Zhang F, Feng YY, Yu DL, Lin S, Cao JS (2018) Systematic identification of long non-coding RNAs during pollen development and fertilization in Brassica rapa. Plant J 96:203–222

    Article  CAS  PubMed  Google Scholar 

  • Ietswaart R, Wu Z, Dean C (2012) Flowering time control: another window to the connection between antisense RNA and chromatin. Trends Genet 28:445–453

    Article  CAS  PubMed  Google Scholar 

  • Jae Bok H, Sibum S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79

    Article  CAS  Google Scholar 

  • Jiang H, Wong WH (2009) Statistical inferences for isoform expression in RNA-SEq. Bioinformatics 25:1026–1032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin JJ, Liu J, Wang H, Wong L, Chua NH (2013) PLncDB: plant long non-coding RNA database. Bioinformatics 29:1068–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang CY, Liu ZC (2015) Global identification and analysis of long non-coding RNAs in diploid strawberry Fragaria vesca during flower and fruit development. BMC Genomics 16:815

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kanneganti V, Gupta AK (2008) Wall associated kinases from plants—an overview. Physiol Mol Biol Plants 14:109–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawanabe T, Ariizumi T, Kawai-Yamada M, Uchimiya H, Toriyama K (2006) Abolition of the tapetum suicide program ruins microsporogenesis. Plant cell Physiol 47:784–787

    Article  CAS  PubMed  Google Scholar 

  • Kornienko AE, Guenzl PM, Barlow DP, Pauler FM (2013) Gene regulation by the act of long non-coding RNA transcription. BMC Biol 11:59–59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee SLJ, Warmke HE (1979) Organelle size and number in fertile and T-cytoplasmic male‐sterile corn. Am J Bot 66:141–148

    Article  Google Scholar 

  • Lei K, Yong Z, Zhi-Qiang Y, Xiao-Qiao L, Shu-Qi Z, Liping W, Ge G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349

    Article  Google Scholar 

  • Li H, Ye YQ, Zhang YC, Zhang AH, Liu TT, Cao JS (2009) BcMF9, a novel polygalacturonase gene, is required for both Brassica campestris intine and exine formation. Ann Bot 104:1339–1351

    Article  CAS  Google Scholar 

  • Li S, Ge FR, Xu M, Zhao XY, Huang GQ, Zhou LZ, Wang JG, Kombrink A, McCormick S, Zhang XS, Zhang Y (2013) Arabidopsis COBRA-LIKE 10, a GPI-anchored protein, mediates directional growth of pollen tubes. Plant J 74:486–497

    Article  CAS  PubMed  Google Scholar 

  • Li L, Eichten SR, Shimizu R, Petsch K, Yeh CT, Wu W, Chettoor AM, Givan SA, Cole RA, Fowler JE, Evans MMS, Scanlon MJ, Yu JM, Schnable PS, Timmermans MCP, Springer NM, Muehlbauer GJ (2014) Genome-wide discovery and characterization of maize long non-coding RNAs. Genome Biol 15:R40

    Article  PubMed  PubMed Central  Google Scholar 

  • Li JJ, Han SH, Ding XL, He TT, Dai JY, Yang SP, Gai JY (2015) Comparative transcriptome analysis between the cytoplasmic male sterile line NJCMS1A and Its maintainer NJCMS1B in soybean (Glycine max (L.) Merr.). PLoS ONE 10:e0126771

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liao Q, Liu CN, Yuan XY, Kang SL, Miao RY, Xiao H, Zhao GG, Luo HT, Bu DC, Zhao HT, Skogerbø G, Wu ZD, Zhao Y (2011) Large-scale prediction of long non-coding RNA functions in a coding–non-coding gene co-expression network. Nucleic Acids Res 39:3864–3878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Pang CY, Wei HL, Song MZ, Meng YY, Ma JH, Fan SL, Yu SX (2015) iTRAQ-facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild-type cotton (Gossypium hirsutum L.). J Proteomics 126:68–81

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Liu ZY, Li CY, Zhang Y, Feng H (2016) Comparative transcriptome analysis of fertile and sterile buds from a genetically male sterile line of Chinese cabbage. Vitro Cell Dev Biol Plant 52:130–139

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–△△Ct Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma JX, Yan BX, Qu YY, Qin FF, Yang YT, Hao XJ, Yu JJ, Zhao Q, Zhu DY, Ao GM (2010) Zm401, a short-open reading-frame mRNA or noncoding RNA, is essential for tapetum and microspore development and can regulate the floret formation in maize. J Cell Biochem 105:136–146

    Article  CAS  Google Scholar 

  • Mao XZ, Cai T, Olyarchuk JG, Wei LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793

    Article  CAS  PubMed  Google Scholar 

  • Mark T, Peter L (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822

    Article  CAS  Google Scholar 

  • Markovic O, Janecek S (2001) Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution. Protein Eng 14:615–631

    Article  CAS  PubMed  Google Scholar 

  • Mattick JS, Rinn JL (2015) Discovery and annotation of long noncoding RNAs. Nat Struct Mol Biol 22:5

    Article  CAS  PubMed  Google Scholar 

  • Maurice B, Hepler PK (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17:3219–3226

    Article  Google Scholar 

  • Mehler MF, Mattick JS (2010) Non-coding RNAs in the nervous system. J Physiol 575:333–341

    Article  CAS  Google Scholar 

  • Mistry J, Bateman A, Finn RD (2007) Predicting active site residue annotations in the Pfam database. BMC Bioinformatics 8:298–298

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Orly W, Chang HY (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21:354–361

    Article  CAS  Google Scholar 

  • Ou LJ, Liu ZB, Zhang ZQ, Wei G, Zhang YP, Kang LY, Yang BZ, Yang S, Lv JH, Liu YH, Chen WC, Dai XZ, Li XF, Zhou SD, Ma YQ, Zou XX (2017) Noncoding and coding transcriptome analysis reveals the regulation roles of long noncoding RNAs in fruit development of hot pepper (Capsicum annuum L.). Plant Growth Regul 83:1–16

    Article  CAS  Google Scholar 

  • Pei XL, Jing ZG, Zheng T, Zhu YL (2017) Comparative transcriptome analysis provides insight into differentially expressed genes related to cytoplasmic male sterility in broccoli (Brassica oleracea var. italica). Sci Hortic 217:234–242

    Article  CAS  Google Scholar 

  • Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philipp K, Jill C, Sujit D, Nix DA, Radharani D, Willingham AT, Stadler PF, Jana H, JRg H, Hofacker IL (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316:1484–1488

    Article  CAS  Google Scholar 

  • Qin C, Yu CS, Shen YO, Fang XD, Chen L, Min JM, Cheng JW, Zhao SC, Xu M, Luo Y, Yang YL, Wu ZM, Mao LK, Wu HY, Ling-Hu CY, Zhou HK, Lin HJ, Gonzalez-Morales S, Trejo-Saavedra DL, Tian H, Tang X, Zhao MJ, Huang ZY, Zhou AW, Yao XM, Cui JJ, Li WQ, Chen Z, Feng YQ, Niu YC, Bi SM, Yang XW, Li WP, Cai HM, Luo XR, Montes-Hernandez S, Leyva-Gonzalez MA, Xiong ZQ, He XJ, Bai LJ, Tan S, Tang XQ, Liu D, Liu JW, Zhang SX, Chen MS, Zhang L, Zhang L, Zhang YC, Liao WQ, Zhang Y, Wang M, Lv XD, Wen B, Liu HJ, Luan HM, Zhang YG, Yang S, Wang XD, Xu JH, Li XQ, Li SC, Wang JY, Palloix A, Bosland PW, Li YR, Krogh A, Rivera-Bustamante RF, Herrera-Estrella L, Yin Y, Yu JP, Hu KL, Zhang ZM (2014) Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc Natl Acad Sci USA 111:5135–5140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saiprasad Goud P, Maxim G, Sung-Bong S, Richardson DN, Reddy ASN (2010) Organ-specific, developmental, hormonal and stress regulation of expression of putative pectate lyase genes in Arabidopsis. New Phytol 174:537–550

    Google Scholar 

  • Shen YF, Sun S, Hua SJ, Shen EH, Ye CY, Cai DG, Timko MP, Zhu QH, Fan LJ (2017) Analysis of transcriptional and epigenetic changes in hybrid vigor of allopolyploid Brassica napus uncovers key roles for small RNAs. Plant J 91(5):874–893

    Article  CAS  PubMed  Google Scholar 

  • Shen EH, Zhu XT, Hua SJ, Chen HY, Ye CY, Zhou LH, Liu Q, Zhu QH, Fan LJ, Chen X (2018) Genome-wide identification of oil biosynthesis-related long non-coding RNAs in allopolyploid Brassica napus. BMC Genomics 19:745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song XD, Brus DJ, Liu F, Li DC, Zhao YG, Yang JL, Zhang GL (2016) Mapping soil organic carbon content by geographically weighted regression: a case study in the Heihe River Basin, China. Geoderma 261:11–22

    Article  CAS  Google Scholar 

  • Subburaj S, Jeon Y, Tu LH, Jin YT, Kumari S, Lee GJ (2018) Genome-wide identification, functional prediction and expression profiling of long non-coding RNAs in Camelina sativa. Plant Growth Regul 86:1–15

    Article  CAS  Google Scholar 

  • Sun L, Luo HT, Bu DC, Zhao GG, Yu KT, Zhang CH, Liu YN, Chen RS, Zhao Y (2013) Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res 41:e166–e166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swiezewski S, Liu FQ, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature 462:799–802

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Chung PJ, Liu J, Jang IC, Kean MJ, Xu J, Chua NH (2014) Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res 24:444–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang MJ, Yuan DJ, Tu LL, Gao WH, He YH, Hu HY, Wang PC, Liu N, Lindsey K, Zhang XL (2015a) Long noncoding RNAs and their proposed functions in fibre development of cotton (Gossypium spp.). New Phytol 207:1181–1197

    Article  CAS  PubMed  Google Scholar 

  • Wang TZ, Liu M, Zhao MG, Chen R, Zhang WH (2015) Identification and characterization of long non-coding RNAs involved in osmotic and salt stress in Medicago truncatula using genome-wide high-throughput sequencing. BMC Plant Biol 15:131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang S, Wang C, Zhang XX, Chen X, Liu JJ, Jia XF, Jia SQ (2016) Transcriptome de novo assembly and analysis of differentially expressed genes related to cytoplasmic male sterility in cabbage. Plant Physiol Biochem 105:224–232

    Article  PubMed  CAS  Google Scholar 

  • Wei MM, Song MZ, Fan SL, Yu SX (2013) Transcriptomic analysis of differentially expressed genes during anther development in genetic male sterile and wild type cotton by digital gene-expression profiling. BMC Genomics 14:97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu ZM, Cheng JW, Qin C, Hu ZQ, Yin CX, Hu KL (2013) Differential proteomic analysis of anthers between cytoplasmic male sterile and maintainer lines in Capsicum annuum L. Int J Mol Sci 14:22982–22996

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xin MM, Wang Y, Yao YY, Song N, Hu Z, Qin D, Xie CJ, Peng HR, Ni ZF, Sun QX (2011) Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol 11:61–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu HM, Kong XD, Chen F, Huang JX, Lou XY, Zhao JY (2015) Transcriptome analysis of Brassica napus pod using RNA-Seq and identification of lipid-related candidate genes. BMC Genomics 16:858

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yadav S, Yadav PK, Yadav D, Yadav KDS (2009) Pectin lyase: a review. Process Biochem 44:1–10

    Article  CAS  Google Scholar 

  • Yang Y, Bao SY, Zhou XH, Liu J, Zhuang Y (2018) The key genes and pathways related to male sterility of eggplant revealed by comparative transcriptome analysis. BMC Plant Biol 18:209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14–R14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan QL, Song C, Gao LY, Zhang HH, Yang CC, Sheng J, Ren J, Chen D, Wang Y (2018) Transcriptome de novo assembly and analysis of differentially expressed genes related to cytoplasmic male sterility in onion. Plant Physiol Bioch 125:35

    Article  CAS  Google Scholar 

  • Zhou X, Liu ZY, Ji RQ, Feng H (2017) Comparative transcript profiling of fertile and sterile flower buds from multiple-allele-inherited male sterility in Chinese cabbage (Brassica campestris L. ssp. pekinensis). Mol Genet Genomics 2017(Suppl):1–24

    CAS  Google Scholar 

  • Zhu BZ, Yang YF, Li R, Fu DQ, Wen LW, Luo YB, Zhu HL (2015) RNA sequencing and functional analysis implicate the regulatory role of long non-coding RNAs in tomato fruit ripening. J Exp Bot 66:4483–4495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu L, Zhu J, Liu YF, Chen YJ, Li YL, Huang LR, Chen SS, Li T, Dang YH, Chen T (2015) Methamphetamine induces alterations in the long non-coding RNAs expression profile in the nucleus accumbens of the mouse. BMC Neurosci 16:1–13

    Article  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the China Agriculture Research System (Grant No. CARS-24-A-05) and the National Natural Science Foundation of China (31760575). The funding bodies themselves did not participate in the design of the study or the collection, analysis, and interpretation of data, or in writing the manuscript.

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ZXX, OLJ and CWC conceived and designed the experiments. LJH wrote the manuscript. LJH, LZB, and YBZ performed the experiments. DMH, LYH and WJ analyzed the data. ZZQ and MYQ revised the manuscript for the language. All authors read and approved the final manuscript.

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Correspondence to Wenchao Chen, Lijun Ou or Xuexiao Zou.

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Junheng Lv and Zhoubin Liu contributed equally to this work and should be considered as co-first authors.

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10725_2020_605_MOESM1_ESM.tif

Supplementary material 1 (TIF 554.3 kb) Fig. S1. GO enrichment analysis for differentially expressed target protein-coding genes in cis between 9704A and 9704B

10725_2020_605_MOESM2_ESM.tif

Supplementary material 2 (TIF 902.1 kb) Fig. S2. GO enrichment analysis for differentially expressed target protein-coding genes in trans between 9704A and 9704B

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Lv, J., Liu, Z., Yang, B. et al. Systematic identification and characterization of long non-coding RNAs involved in cytoplasmic male sterility in pepper (Capsicum annuum L.). Plant Growth Regul 91, 277–288 (2020). https://doi.org/10.1007/s10725-020-00605-4

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