Skip to main content
SpringerLink
Log in

Identification of microRNAs and their target genes associated with chasmogamous and cleistogamous flower development in Viola prionantha

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Differentially expressed microRNAs were found associated with the development of chasmogamous and cleistogamous flowers in Viola prionantha, revealing potential roles of microRNAs in the developmental evolution of dimorphic flowers.

Abstract

In Viola prionantha, chasmogamous (CH) flowers are induced by short daylight, while cleistogamous (CL) flowers are triggered by long daylight. How environmental factors and microRNAs (miRNAs) affect dimorphic flower formation remains unknown. In this study, small RNA sequencing was performed on CH and CL floral buds at different developmental stages in V. prionantha, differentially expressed miRNAs (DEmiRNAs) were identified, and their target genes were predicted. In CL flowers, Viola prionantha miR393 (vpr-miR393a/b) and vpr-miRN3366 were highly expressed, while in CH flowers, vpr-miRN2005, vpr-miR172e-2, vpr-miR166m-3, vpr-miR396f-2, and vpr-miR482d-2 were highly expressed. In the auxin-activated signaling pathway, vpr-miR393a/b and vpr-miRN2005 could target Vpr-TIR1/AFB and Vpr-ARF2, respectively, and other DEmiRNAs could target genes involved in the regulation of transcription, e.g., Vpr-AP2-7. Moreover, Vpr-UFO and Vpr-YAB5, the main regulators in petal and stamen development, were co-expressed with Vpr-TIR1/AFB and Vpr-ARF2 and showed lower expression in CL flowers than in CH flowers. Some V. prionantha genes relating to the stress/defense responses were co-expressed with Vpr-TIR1/AFB, Vpr-ARF2, and Vpr-AP2-7 and highly expressed in CL flowers. Therefore, in V. prionantha, CH–CL flower development may be regulated by the identified DEmiRNAs and their target genes, thus providing the first insight into the formation of dimorphic flowers in Viola.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

Additional information may be found online in the Supporting Information section at the end of the article. The raw sequencing data of mRNAs has been deposited in the NGDC in this article and can be found in BIG Data Center (https://ngdc.cncb.ac.cn/) as a BioProject PRJCA008547. The raw sequencing data of small RNAs has been deposited in zenodo (https://zenodo.org/records/10695147) as a BioProject https://doi.org/10.5281/zenodo.10695147.

Abbreviations

CH:

Chasmogamous

CL:

Cleistogamous

SD:

Short daylight

LD:

Long daylight

DEmiRNAs:

Differentially expressed miRNAs

GO:

Gene Ontology

References

  • Ahmad M, Uniyal SK, Batish DR, Rathee S, Sharma P, Singh HP (2021) Flower phenological events and duration pattern is influenced by temperature and elevation in Dhauladhar mountain range of Lesser Himalaya. Ecol Indic 129:107902

    Google Scholar 

  • Anwar N, Ohta M, Yazawa T, Sato Y, Li C, Tagiri A, Sakuma M, Nussbaumer T, Bregitzer P, Pourkheirandish M, Wu J, Komatsuda T (2018) miR172 downregulates the translation of cleistogamy 1 in barley. Ann Bot 122:251–265

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blazquez MA, Ferrándiz C, Madueño F, Parcy F (2006) How floral meristems are built. Plant Mol Biol 60:855–870

    CAS  PubMed  Google Scholar 

  • Breakfield NW, Corcoran DL, Petricka JJ, Shen J, Sae-Seaw J, Rubio-Somoza I, Weigel D, Ohler U, Benfey PN (2012) High-resolution experimental and computational profiling of tissue specific known and novel miRNAs in Arabidopsis. Genome Res 22:163–176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    CAS  PubMed  Google Scholar 

  • Chen IC, Lee SC, Pan SM, Hsieh HL (2007) GASA4, a GA-stimulated gene, participates in light signaling in Arabidopsis. Plant Sci 172:1062–1071

    CAS  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    CAS  PubMed  Google Scholar 

  • Cortés-Palomec AC, Ballard HE Jr (2006) Influence of annual fluctuations in environmental conditions on chasmogamous flower production in Viola striata. J Torrey Bot Soc 133:312–320

    Google Scholar 

  • Culley TM, Klooster MR (2007) The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms. Bot Rev 73:1–30

    Google Scholar 

  • Dai XB, Zhao PX (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res 46:W49–W54

    CAS  PubMed  PubMed Central  Google Scholar 

  • Du W, Lu Y, Li Q, Luo S, Shen S, Li N, Chen X (2022) TIR1/AFB proteins: active players in abiotic and biotic stress signaling. Front Plant Sci 13:1083409

    PubMed  PubMed Central  Google Scholar 

  • Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574

    CAS  PubMed  Google Scholar 

  • Fahlgren N, Carrington JC (2010) miRNA target prediction in plants. Methods Mol Biol 592:51–57

    CAS  PubMed  Google Scholar 

  • Guo L, Shen JJ, Zhang CJ, Guo Q, Liang HY, Hou XG (2022) Characterization and bioinformatics analysis of ptc-miR396g-5p in response to drought stress of Paeonia ostii. Noncoding RNA Res 7:150–158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo PR, Wu LL, Wang Y, Liu D, Li JA (2023) Effects of drought stress on the morphological structure and flower organ physiological characteristics of Camellia oleifera flower buds. Plants 12:2585

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iglesias MJ, Terrile MC, Windels D, Lombardo MC, Bartoli CG, Vazquez F, Estelle M, Casalongué CA (2014) MiR393 regulation of auxin signaling and redox-related components during acclimation to salinity in Arabidopsis. PLoS ONE 9:e107678

    PubMed  PubMed Central  Google Scholar 

  • Jagadeeswaran G, Li YF, Sunkar R (2014) Redox signaling mediates the expression of a sulfate-deprivation-inducible microRNA395 in Arabidopsis. Plant J 77:85–96

    CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    CAS  PubMed  Google Scholar 

  • Kagawa T, Wada M, Shimazaki K (2001) phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660

    PubMed  Google Scholar 

  • Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    PubMed  PubMed Central  Google Scholar 

  • Lardi M, Liu Y, Giudice G, Ahrens CH, Zamboni N, Pessi G (2018) Metabolomics and Transcriptomics Identify Multiple Downstream Targets of Paraburkholderia phymatum σ54 During Symbiosis with Phaseolus vulgaris. Int J Mol Sci 19:1049

    PubMed  PubMed Central  Google Scholar 

  • Le Corff J (1993) Effects of light and nutrient availability on chasmogamy and cleistogamy in an understory tropical herb, Calathea micans (Marantaceae). Am J Bot 80:1392–1399

    Google Scholar 

  • Li QX, Huo QD, Wang J, Zhao J, Sun K, He CY (2016a) Expression of B-class MADS-box genes in response to variations in photoperiod is associated with chasmogamous and cleistogamous flower development in Viola philippica. BMC Plant Biol 6:151

    Google Scholar 

  • Li ZX, Li SG, Zhang LF, Han SY, Li WF, Xu HY, Yang WH, Liu YL, Fan YR, Qi LW (2016b) Over-expression of miR166a inhibits cotyledon formation in somatic embryos and promotes lateral root development in seedlings of Larix leptolepis. Plant Cell Tiss Org 127:461–473

    CAS  Google Scholar 

  • Li WQ, Jia YL, Liu FQ, Wang FQ, Fan FJ, Wang J, Zhu JY, Xu Y, Zhong WG, Yang J (2019) Integration analysis of small RNA and degradome sequencing reveals microRNAs responsive to Dickeya zeae in resistant rice. Int J Mol Sci 20:222

    PubMed  PubMed Central  Google Scholar 

  • Li QX, Li JG, Zhang L, Pan CC, Yang N, Sun K, He CY (2021) Gibberellins are required for dimorphic flower development in Viola philippica. Plant Sci 303:110749

    CAS  PubMed  Google Scholar 

  • Li C, Nong WY, Zhao SC, Lin X, Xie YC, Cheung MY, Xiao ZX, Wong AYP, Chan TF, Hui JHL, Lam HM (2022a) Differential microRNA expression, microRNA arm switching, and microRNA: long noncoding RNA interaction in response to salinity stress in soybean. BMC Genomics 23:65

    PubMed  PubMed Central  Google Scholar 

  • Li QX, Li KP, Zhang ZR, Li JG, Wang B, Zhang ZM, Zhu YY, Pan CC, Sun K, He CY (2022b) Transcriptomic comparison sheds new light on regulatory networks for dimorphic flower development in response to photoperiod in Viola prionantha. BMC Plant Biol 22:336

    PubMed  PubMed Central  Google Scholar 

  • Lin CK, Lee NY, Huang PL, Do YY (2016) Gene structure and expression characteristics of the auxin receptor TIR1 ortholog in Momordica charantia and developmental analysis of its promoter in transgenic plants. J Plant Biochem Biotechnol 25:253–262

    CAS  Google Scholar 

  • Lin W, Gupta SK, Arazi T, Spitzer-Rimon B (2021) MIR172d is required for floral organ identity and number in tomato. Int J Mol Sci 22:4659

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu JN, Ma XM, Yan LP, Liang Q, Fang HC, Wang CX, Dong YH (2022) MicroRNA and degradome profiling uncover defense response of fraxinus velutina torr. to salt stress. Front Plant Sci 13:847853

    PubMed  PubMed Central  Google Scholar 

  • Lord EM (1981) Cleistogamy: a tool for the study of floral morphogenesis, function and evolution. Bot Rev 47:421–449

    Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    PubMed  PubMed Central  Google Scholar 

  • Ma J, Zhao P, Liu S, Yang Q, Guo H (2020) The control of developmental phase transitions by microRNAs and their targets in seed plants. Int J Mol Sci 21:1971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Masuda M, Yahara T (1994) Reproductive ecology of a cleistogamous annual, Impatiens nolitangere L., occurring under different environmental conditions. Ecol Res 9:67–75

    Google Scholar 

  • Mayers AM, Lord EM (1983) Comparative flower development in the cleistogamous species Viola odorata. I. A growth rate study. Am J Bot 70:1548–1555

    Google Scholar 

  • Millar AA, Lohe A, Wong G (2019) Biology and function of miR159 in plants. Plants 8:255

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minter TC, Lord EM (1983) Effects of water stress, abscisic acid, and gibberellic acid on flower production and differentiation in the cleistogamous species Collomia grandiflora Dougl. ex Lindl. (Polemoniaceae). Am J Bot 70:618–624

    CAS  Google Scholar 

  • Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80

    CAS  PubMed  Google Scholar 

  • Naira SK, Wanga N, Turuspekova Y, Pourkheirandisha M, Sinsuwongwata S, Chena G, Sameria M, Tagiria A, Hondab I, Watanabeb Y, Kanamoric H, Wickerd T, Steine N, Nagamuraa Y, Matsumotoa T, Komatsudaa T (2010) Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage. Proc Natl Acad Sci USA 107:490–495

    Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    CAS  PubMed  Google Scholar 

  • Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46

    CAS  PubMed  Google Scholar 

  • Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pertea M, Pertea G, Antonescu C, Chang T, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qin B, Chen QP, Lou ZC (1994) Active constituents of Viola prionantha Bge. J Chin Pharm Sci 3:91–96

    CAS  Google Scholar 

  • Reed JW (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 6:420–425

    CAS  PubMed  Google Scholar 

  • Reeves PH, Ellis CM, Ploense SE, Wu MF, Yadav V, Tholl D, Chételat A, Haupt I, Kennerley BJ, Hodgens C, Farmer EE, Nagpal P, Reed JW (2012) A regulatory network for coordinated flower maturation. PLoS Genet 8:e1002506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rieu P, Turchi L, Thévenon E, Zarkadas E, Nanao M, Chahtane H, Tichtinsky G, Lucas J, Blanc-Mathieu R, Zubieta C, Schoehn G, Parcy F (2023) The F-box protein UFO controls flower development by redirecting the master transcription factor LEAFY to new cis-elements. Nat Plants 9:315–329

    CAS  PubMed  Google Scholar 

  • Rubinovich L, Weiss D (2010) The Arabidopsis cysteine-rich protein GASA4 promotes GA responses and exhibits redox activity in bacteria and in planta. Plant J 64:1018–1027

    CAS  PubMed  Google Scholar 

  • Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261

    CAS  PubMed  Google Scholar 

  • Shi HT, Ye TT, Han N, Bian HW, Liu XD, Chan ZL (2015) Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J Integr Plant Biol 57:628–640

    CAS  PubMed  Google Scholar 

  • Su Z, Ma X, Guo H, Sukiran NL, Guo B, Assmann SM, Ma H (2013) Flower development under drought stress: morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis. Plant Cell 25:3785–3807

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sukiran NL, Ma JC, Ma H, Su Z (2019) ANAC019 is required for recovery of reproductive development under drought stress in Arabidopsis. Plant Mol Biol 99:161–174

    CAS  PubMed  Google Scholar 

  • Sun F, Guo G, Du J, Guo W, Peng H, Ni Z, Sun Q, Yao Y (2014) Whole-genome discovery of miRNAs and their targets in wheat (Triticum aestivum L.). BMC Plant Biol 14:142

    PubMed  PubMed Central  Google Scholar 

  • Tabata R, Ikezaki M, Fujibe T, Aida M, Tian C, Ueno Y, Yamamoto KT, Machida Y, Nakamura K, Ishiguro S (2010) Arabidopsis AUXIN RESPONSE FACTOR6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant Cell Physiol 51:164–175

    CAS  PubMed  Google Scholar 

  • Tang M, Bai X, Niu LJ, Chai X, Chen MS, Xu ZF (2018) miR172 regulates both vegetative and reproductive development in the perennial woody plant Jatropha curcas. Plant Cell Physiol 59:2549–2563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:3657–3668

    CAS  PubMed  Google Scholar 

  • Wu HJ, Ma YK, Chen T, Wang M, Wang XJ (2012) PsRobot: a web-based plant small RNA meta analysis toolbox. Nucleic Acids Res 40:W22–W28

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu F, Zhang D, Muvunyi BP, Yan Q, Zhang Y, Yan Z, Cao M, Wang Y, Zhang J (2018) Analysis of microRNA reveals cleistogamous and chasmogamous floret divergence in dimorphic plant. Sci Rep 8:6287

    PubMed  PubMed Central  Google Scholar 

  • Xu J, Li J, Cui L, Zhang T, Wu Z, Zhu PY, Meng YJ, Zhang KJ, Yu XQ, Lou QF, Chen JF (2017) New insights into the roles of cucumber TIR1 homologs and miR393 in regulating fruit/seed set development and leaf morphogenesis. BMC Plant Biol 17:130

    PubMed  PubMed Central  Google Scholar 

  • Yan S, Gen C, Ding L, Chen Z, Liu X, Wang H, Zhao W, Ning K, Zhao J, Tesfamichael K, Wang Q, Zhang X (2016) Different cucumber CsYUC genes regulate response to abiotic stresses and flower development. Sci Rep 6:20760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang F, Liang G, Liu D, Yu D (2009) Arabidopsis miR396 mediates the development of leaves and flowers in transgenic tobacco. J Plant Biol 52:475–481

    CAS  Google Scholar 

  • Yang F, Lu C, Wei Y, Wu J, Ren R, Gao J, Ahmad S, Jin J, Xv Y, Liang G, Zhu G (2022) Organ-specific gene expression reveals the role of the Cymbidium ensifolium- miR396/growth-regulating factors module in flower development of the orchid plant Cymbidium ensifolium. Front Plant Sci 12:799778

    PubMed  PubMed Central  Google Scholar 

  • Yu G, Wang L, Han Y, He Q (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS: J Plant Biol 16:284–287

    CAS  Google Scholar 

  • Zeng XC, Xu YZ, Jiang JJ, Zhang FQ, Ma L, Wu DW, Wang YP, Sun WC (2018) Identification of cold stress responsive microRNAs in two winter turnip rape (Brassica rapa L.) by high throughput sequencing. BMC Plant Biol 18:52

    PubMed  PubMed Central  Google Scholar 

  • Zhang J, Zhang H, Srivastava AK, Pan Y, Bai J, Fang J, Shi H, Zhu JK (2018) Knockdown of rice microRNA166 confers drought resistance by causing leaf rolling and altering stem xylem development. Plant Physiol 176:2082–2094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang R, Min Y, Holappa D, Walcher-Chevillet CL, Duan XS, Donaldson E, Kong HZ, Kramer EM (2020) A role for the auxin response factors ARF6 and ARF8 homologs in petal spur elongation and nectary maturation in Aquilegia. New Phytol 227:1392–1405

    CAS  PubMed  Google Scholar 

  • Zhang J, Wu F, Yan Q, John UP, Cao M, Xu P, Zhang Z, Ma T, Zong X, Li J, Liu R, Zhang Y, Zhao Y, Kanzana G, Lv Y, Nan Z, Spangenberg G, Wang Y (2021) The genome of Cleistogenes songorica provides a blueprint for functional dissection of dimorphic flower differentiation and drought adaptability. Plant Biotechnol J 19:532–547

    CAS  PubMed  Google Scholar 

  • Zhao Q, Sun C, Liu DD, Hao YJ, You CX (2015) Ectopic expression of the apple Md-miR172e gene alters flowering time and floral organ identity in Arabidopsis. Plant Cell Tiss Organ Cult 123:535–546

    CAS  Google Scholar 

  • Zheng ZH, Wang NQ, Jalajakumari M, Blackman L, Shen EH, Verma S, Wang MB, Millar AA (2020) miR159 represses a constitutive pathogen defense response in tobacco. Plant Physiol 182:2182–2198

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu QH, Helliwell CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62:487–495

    CAS  PubMed  Google Scholar 

  • Zhu QH, Fan L, Liu Y, Xu H, Llewellyn D, Wilson I (2013) miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLoS ONE 8:e84390

    PubMed  PubMed Central  Google Scholar 

  • Zhu M, Wang Z, Yang Y, Wang Z, Mu W, Liu J (2023) Multi-omics reveal differentiation and maintenance of dimorphic flowers in an alpine plant on the Qinghai-Tibet Plateau. Mol Ecol 32:1411–1424

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Stefan de Folter and the two anonymous reviewers for their pertinent and constructive suggestions to improve this paper. This work was supported by the grants (32160055, 31930007, and 32360059) from the National Natural Science Foundation of China and grant (21JR7RA140) from the Natural Science Foundation of Gansu province.

Funding

The National Natural Science Foundation of China, 32160055, Qiaoxia Li, Innovative Research Group Project of the National Natural Science Foundation of China, 31930007, Chaoying He, the National Natural Science Foundation of China, 32360059, Qiaoxia Li.

Author information

Authors and Affiliations

  1. Life Science College, Northwest Normal University, Anning East Road 967, Anning, Lanzhou, 730070, Gansu, China

    Qiaoxia Li, Zuoming Zhang, Yuanyuan Zhu & Kun Sun

  2. State Key Laboratory of Plant Diversity and Specialty Crops / State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Beijing, 100093, China

    Kunpeng Li & Chaoying He

  3. China National Botanical Garden, Beijing, 100093, China

    Kunpeng Li & Chaoying He

  4. College of Life Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China

    Kunpeng Li & Chaoying He

Authors
  1. Qiaoxia Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zuoming Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kunpeng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuanyuan Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kun Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chaoying He
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

QXL conceived and designed the work. ZZM, KPL, KS, QXL and CYH analyzed the data. ZMZ and QXL performed all experiments. ZMZ and YYZ cultured the seedlings of V. prionantha. ZMZ and QXL are involved in gene expression analyses. QXL and CYH wrote the manuscript. All authors have read and approved the manuscript.

Corresponding authors

Correspondence to Qiaoxia Li or Chaoying He.

Ethics declarations

Competing interests

The authors declare that they have no conflict of interests.

Additional information

Communicated by Stefan de Folter.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 774 KB)

Supplementary file2 (XLSX 418 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Q., Zhang, Z., Li, K. et al. Identification of microRNAs and their target genes associated with chasmogamous and cleistogamous flower development in Viola prionantha. Planta 259, 116 (2024). https://doi.org/10.1007/s00425-024-04398-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-024-04398-y

Keywords

Search

Navigation