The long noncoding RNA FRILAIR regulates strawberry fruit ripening by functioning as a noncanonical target mimic

English version

Autoři: Yajun Tang ^aff001; Zhipeng Qu ^aff004; Jiajun Lei ^aff005; Reqing He ^aff002; David L. Adelson ^aff004; Youlin Zhu ^aff002; Zhenbiao Yang ^aff003; Dong Wang ^aff002
Působiště autorů: College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, China ^aff001; Key Laboratory of Molecular Biology and Gene Engineering in Jiangxi Province, College of Life Science, Nanchang University, Nanchang, China ^aff002; FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China ^aff003; Department of Molecular and Biomedical Science, School of Biological Sciences, The University of Adelaide, Adelaide, Australia ^aff004; College of Horticulture, Shenyang Agricultural University, Shenyang, China ^aff005
Vyšlo v časopise: The long noncoding RNA FRILAIR regulates strawberry fruit ripening by functioning as a noncanonical target mimic. PLoS Genet 17(3): e1009461. doi:10.1371/journal.pgen.1009461
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009461

Souhrn

Long noncoding RNAs (lncRNAs) are emerging as important regulators in plant development, but few of them have been functionally characterized in fruit ripening. Here, we have identified 25,613 lncRNAs from strawberry ripening fruits based on RNA-seq data from poly(A)-depleted libraries and rRNA-depleted libraries, most of which exhibited distinct temporal expression patterns. A novel lncRNA, FRILAIR harbours the miR397 binding site that is highly conserved in diverse strawberry species. FRILAIR overexpression promoted fruit maturation in the Falandi strawberry, which was consistent with the finding from knocking down miR397, which can guide the mRNA cleavage of both FRILAIR and LAC11a (encoding a putative laccase-11-like protein). Moreover, LAC11a mRNA levels were increased in both FRILAIR overexpressing and miR397 knockdown fruits, and accelerated fruit maturation was also found in LAC11a overexpressing fruits. Overall, our study demonstrates that FRILAIR can act as a noncanonical target mimic of miR397 to modulate the expression of LAC11a in the strawberry fruit ripening process.

Klíčová slova:

Biosynthesis – Cloning – Fruits – Gene expression – Leaves – Long non-coding RNA – MicroRNAs – RNA sequencing

Zdroje

1. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, et al. (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Molecular cell 39: 925–938. doi: 10.1016/j.molcel.2010.08.011 20797886

2. Spitale RC, Tsai MC, Chang HY (2011) RNA templating the epigenome: long noncoding RNAs as molecular scaffolds. Epigenetics 6: 539–543. doi: 10.4161/epi.6.5.15221 21393997

3. Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annual review of biochemistry 81: 145–166. doi: 10.1146/annurev-biochem-051410-092902 22663078

4. Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, et al. (2012) Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491: 454–457. doi: 10.1038/nature11508 23064229

5. Bazin J, Baerenfaller K, Gosai SJ, Gregory BD, Crespi M, Bailey-Serres J (2017) Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation. Proceedings of the National Academy of Sciences 114: E10018–E10027. doi: 10.1073/pnas.1708433114 29087317

6. Cui J, Luan Y, 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 Journal 89: 577–589. doi: 10.1111/tpj.13408 27801966

7. Kang C, Liu Z (2015) Global identification and analysis of long non-coding RNAs in diploid strawberry Fragaria vesca during flower and fruit development. BMC genomics 16: 1–15. doi: 10.1186/1471-2164-16-1 25553907

8. Wu J, Wang D, Liu Y, Wang L, Qiao X, Zhang S (2014) Identification of miRNAs involved in pear fruit development and quality. BMC genomics 15. doi: 10.1186/1471-2164-15-953 25366381

9. Zhang YC, Yu Y, Wang CY, Li ZY, Liu Q, Xu J, et al. (2013) Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nature biotechnology 31: 848–852. doi: 10.1038/nbt.2646 23873084

10. Zhu B, Yang Y, Li R, Fu D, Wen L, Luo Y, et al. (2015) RNA sequencing and functional analysis implicate the regulatory role of long non-coding RNAs in tomato fruit ripening. Journal of experimental botany 66: 4483–4495. doi: 10.1093/jxb/erv203 25948705

11. Zhang G, Chen D, Zhang T, Duan A, Zhang J, He C (2018) Transcriptomic and functional analyses unveil the role of long non-coding RNAs in anthocyanin biosynthesis during sea buckthorn fruit ripening. DNA Research 25: 465–476. doi: 10.1093/dnares/dsy017 29873696

12. Civello PM, Martínez GA, Chaves AR, Añón MC (1997) Heat Treatments Delay Ripening and Postharvest Decay of Strawberry Fruit. Journal of Agricultural and Food Chemistry 45: 4589–4594.

13. Luo H, Dai C, Li Y, Feng J, Liu Z, Kang C (2018) Reduced Anthocyanins in Petioles codes for a GST anthocyanin transporter that is essential for the foliage and fruit coloration in strawberry. Journal of experimental botany 69: 2595–2608. doi: 10.1093/jxb/ery096 29538703

14. Cheng JF, Niu QF, Zhang B, Chen KS, Yang RH, Zhu JK, et al. (2018) Downregulation of RdDM during strawberry fruit ripening. Genome biology 19. doi: 10.1186/s13059-018-1587-x 30514401

15. Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, et al. (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiology 157: 188–199. doi: 10.1104/pp.111.177311 21734113

16. Liao X, Li M, Liu B, Yan M, Yu X, Zi H, et al. (2018) Interlinked regulatory loops of ABA catabolism and biosynthesis coordinate fruit growth and ripening in woodland strawberry. Proceedings of the National Academy of Sciences 115: E11542–E11550. doi: 10.1073/pnas.1812575115 30455308

17. Csorba T, Questa JI, Sun Q, Dean C (2014) Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proceedings of the National Academy of Sciences 111: 16160–16165. doi: 10.1073/pnas.1419030111 25349421

18. Smargon AA, Cox DBT, Pyzocha NK, Zheng K, Slaymaker IM, Gootenberg JS, et al. (2017) Cas13b Is a Type VI-B CRISPR-Associated RNA-Guided RNase Differentially Regulated by Accessory Proteins Csx27 and Csx28. Molecular cell 65: 618–630. doi: 10.1016/j.molcel.2016.12.023 28065598

19. Zhou J, Wang G, Liu Z (2018) Efficient genome editing of wild strawberry genes, vector development and validation. Plant biotechnology journal 16: 1868–1877. doi: 10.1111/pbi.12922 29577545

20. Lu T, Cui L, Zhou Y, Zhu C, Fan D, Gong H, et al. (2015) Transcriptome-wide investigation of circular RNAs in rice. RNA (New York, NY) 21: 2076–2087. doi: 10.1261/rna.052282.115 26464523

21. Griffiths-Jones S (2004) The microRNA Registry. Nucleic acids research 32: D109–D111. doi: 10.1093/nar/gkh023 14681370

22. Risso D, Ngai J, Speed TP, Dudoit S (2014) Normalization of RNA-seq data using factor analysis of control genes or samples. Nature biotechnology 32: 896–902. doi: 10.1038/nbt.2931 25150836

23. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC bioinformatics 9.

24. Fu DQ, Zhu BZ, Zhu HL, Jiang WB, Luo YB (2005) Virus‐induced gene silencing in tomato fruit. The Plant Journal 43: 299–308. doi: 10.1111/j.1365-313X.2005.02441.x 15998315

25. Yang R, Li P, Mei H, Wang D, Sun J, Yang C, et al. (2019) Fine-Tuning of MiR528 Accumulation Modulates Flowering Time in Rice. Molecular plant 12: 1103–1113. doi: 10.1016/j.molp.2019.04.009 31059825

26. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, et al. (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics 39: 1033–1037. doi: 10.1038/ng2079 17643101

27. Vidot K, Rivard C, Van Vooren G, Siret R, Lahaye M (2020) Metallic ions distribution in texture and phenolic content contrasted cider apples. Postharvest Biology and Technology 160.

28. Jia D, Mao Q, Chen Y, Liu Y, Chen Q, Wu W, et al. (2017) Insect symbiotic bacteria harbour viral pathogens for transovarial transmission. Nature Microbiology 2: 1–7. doi: 10.1038/nmicrobiol.2017.25 28263320

29. Wang D, Qu ZP, Yang L, Zhang QZ, Liu ZH, Trung D, et al. (2017) Transposable elements (TEs) contribute to stress‐related long intergenic noncoding RNA s in plants. Plant Journal 90: 133–146.

30. Darwish O, Shahan R, Liu Z, Slovin JP, Alkharouf NW (2015) Re-annotation of the woodland strawberry (Fragaria vesca) genome. BMC genomics 16. doi: 10.1186/s12864-015-1221-1 25623424

31. Vladimir S, Sargent DJ, Crowhurst RN, Mockler TC, Otto F, Delcher AL, et al. (2011) The genome of woodland strawberry (Fragaria vesca). Nature Genetics 43: 109–116. doi: 10.1038/ng.740 21186353

32. Shao M, Kingsford C (2017) Accurate assembly of transcripts through phase-preserving graph decomposition. Nature biotechnology 35: 1167–1169. doi: 10.1038/nbt.4020 29131147

33. Hu P, Li G, Zhao X, Zhao F, Li L, Zhou H (2018) Transcriptome profiling by RNA-Seq reveals differentially expressed genes related to fruit development and ripening characteristics in strawberries (Fragaria× ananassa). PeerJ 6.

34. Sánchez-Sevilla JF, Vallarino JG, Osorio S, Bombarely A, Posé D, Merchante C, et al. (2017) Gene expression atlas of fruit ripening and transcriptome assembly from RNA-seq data in octoploid strawberry (Fragaria× ananassa). Scientific reports 7.

35. Xue C, Yao JL, Qin MF, Zhang MY, Allan AC, Wang DF, et al. (2019) PbrmiR397a regulates lignification during stone cell development in pear fruit. Plant biotechnology journal 17: 103–117. doi: 10.1111/pbi.12950 29754465

36. Jiang N, Cui J, Shi Y, Yang G, Zhou X, Hou X, et al. (2019) Tomato lncRNA23468 functions as a competing endogenous RNA to modulate NBS-LRR genes by decoying miR482b in the tomato-Phytophthora infestans interaction. Horticulture research 6: 1–11. doi: 10.1038/s41438-018-0066-6 30603088

37. Edger PP, Poorten TJ, Vanburen R, Hardigan MA, Colle M, Mckain MR, et al. (2019) Origin and evolution of the octoploid strawberry genome. Nature Genetics 51: 541–547. doi: 10.1038/s41588-019-0356-4 30804557

38. Xia R, Ye S, Liu Z, Meyers BC, Liu Z (2015) Novel and Recently Evolved MicroRNA Clusters Regulate Expansive F-BOX Gene Networks through Phased Small Interfering RNAs in Wild Diploid Strawberry. Plant Physiol 169: 594–610. doi: 10.1104/pp.15.00253 26143249

39. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in Drosophila. Genome biology 5. doi: 10.1186/gb-2003-5-1-r1 14709173

40. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, et al. (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147: 358–369. doi: 10.1016/j.cell.2011.09.028 22000014

41. Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D (2010) A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS genetics 6. doi: 10.1371/journal.pgen.1001031 20661442

42. Pillet J, Yu H-W, Chambers AH, Whitaker VM, Folta KM (2015) Identification of candidate flavonoid pathway genes using transcriptome correlation network analysis in ripe strawberry (Fragaria× ananassa) fruits. Journal of experimental botany 66: 4455–4467. doi: 10.1093/jxb/erv205 25979996

43. Lu S, Li Q, Wei H, Chang MJ, Tunlaya-Anukit S, Kim H, et al. (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proceedings of the National Academy of Sciences 110: 10848–10853. doi: 10.1073/pnas.1308936110 23754401

44. Bryan AC, Jawdy S, Gunter L, Gjersing E, Sykes R, Hinchee MA, et al. (2016) Knockdown of a laccase in Populus deltoides confers altered cell wall chemistry and increased sugar release. Plant Biotechnology Journal 14: 2010–2020. doi: 10.1111/pbi.12560 26997157

45. Montero TM, Mollá EM, Esteban RM, López-Andréu FJ (1996) Quality attributes of strawberry during ripening. Scientia Horticulturae 65: 239–250.

46. Yamaki S (2010) Metabolism and accumulation of sugars translocated to fruit and their regulation. Journal of the Japanese Society for Horticultural Science 79: 1–15.

47. Turlapati PV, Kim KW, Davin LB, Lewis NG (2011) The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta 233: 439–470. doi: 10.1007/s00425-010-1298-3 21063888

Článek Natural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila

Článek DNA polymerase theta suppresses mitotic crossing over

Článek Integrative genomic analysis of early neurogenesis reveals a temporal genetic program for differentiation and specification of preplate and Cajal-Retzius neurons

Článek Gene disruption by structural mutations drives selection in US rice breeding over the last century

Článek Behavior of dicentric chromosomes in budding yeast

Článek Assessing the co-variability of DNA methylation across peripheral cells and tissues: Implications for the interpretation of findings in epigenetic epidemiology

Článek Characterization of C9orf72 haplotypes to evaluate the effects of normal and pathological variations on its expression and splicing

Článek Analysis of the SNARE Stx8 recycling reveals that the retromer-sorting motif has undergone evolutionary divergence

Článek activin-2 is required for regeneration of polarity on the planarian anterior-posterior axis

Článek The capacity of origins to load MCM establishes replication timing patterns

Článek Doublesex regulates fruitless expression to promote sexual dimorphism of the gonad stem cell niche

Článek AMPK-dependent and -independent coordination of mitochondrial function and muscle fiber type by FNIP1