Abstract
Main conclusion
It was proved for the first time that the miR172e–LbrAP2 module regulated the vegetative growth phase transition in Lilium, which provided a new approach to shorten the juvenile stage of Lilium, improved the reproduction rate, and reduced the propagation cost of Lilium commercial bulbs.
Abstract
Lilium is an ornamental bulb plant that takes at least 3 years to cultivate into commercial seed bulbs under natural conditions. The aim of this study was to shorten the Lilium expansion cycle. In this study, the growth cycle of lily tubers induced by low temperature of 15 °C was significantly shorter than that of tubers grown at a conventional temperature. Quantitative real-time PCR analysis showed that the expression patterns of miR172e and LbrAP2 were negatively correlated. GUS histochemical staining confirmed that miR172e and LbrAP2 in tobacco leaves interacted with each other after co-transformation. The shear sites of miR172e and its target gene, LbrAP2, upon binding, were identified by RLM 5′ RACE analysis. In addition, miR172e and LbrAP2 showed opposite expression patterns after the transformation of Arabidopsis. miR172e overexpression accelerated the transition from juvenile to adult plants, whereas LbrAP2 overexpression inhibited this process, thus indicating that miR172e negatively regulated the target gene LbrAP2. Upregulation of the transcription factor LbrAP2 delayed the phase transition of plants, whereas miR172 inhibited the transcriptional translation of LbrAP2, thereby accelerating the phase transition. Low-temperature treatment of Lilium bulbs can shorten Lilium development, which provides a new approach to accelerating Lilium commercial bulb breeding and reducing breeding costs.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.
Abbreviations
- AP2:
-
APETALA2
- ERF:
-
ETHYLENE RESPONSIVE FACTOR
- SPL:
-
SQUAMOSA PROMOTER BINDING PROTEIN-LIKE
References
Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61(6):1001–1013. https://doi.org/10.1111/j.1365-313X.2010.04148.x
Anwar M, Wang G, Wu J, Waheed S, Allan AC, Zeng L (2018) Ectopic overexpression of a novel R2R3-MYB, NtMYB2 from Chinese narcissus represses anthocyanin biosynthesis in tobacco. Molecules (basel, Switzerland) 23(4):781. https://doi.org/10.3390/molecules23040781
Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233. https://doi.org/10.1016/j.cell.2009.01.002
Chen Y, Zhao MN, Wang XS, Cui JT, Ge W, Zhang KZ (2022) Key microRNAs and target genes involved in regulating maturation in Lilium. Ornam Plant Res 2:9. https://doi.org/10.48130/OPR-2022-0009
Feng K, Hou XL, Xing GM et al (2020) Advances in AP2/ERF super-family transcription factors in plant. Crit Rev Biotechnol 40(6):750–776. https://doi.org/10.1080/07388551.2020.1768509
Foley SW, Kramer MC, Gregory BD (2017) RNA structure, binding, and coordination in Arabidopsis. Wires 8(5):e1426. https://doi.org/10.1002/wrna.1426
Freytes SN, Canelo M, Cerdán PD (2021) Regulation of flowering time: when and where? Curr Opin Plant Biol 63:102049. https://doi.org/10.1016/j.pbi.2021.102049
Gao J, Chen H, Yang H, He Y, Tian Z, Li J (2018) A brassinosteroid responsive miRNA-target module regulates gibberellin biosynthesis and plant development. New Phytol 220(2):488–501. https://doi.org/10.1111/nph.15331
Ge W, Cui JT, Shao Y, Bian XT, Jia YH, Zhang KZ (2018) Temperature change shortens maturation time in Lilium with evidence for molecular mechanisms. Mol Breed 38:1–10. https://doi.org/10.1007/s11032-018-0904-0
Grebe M (2012) The patterning of epidermal hairs in Arabidopsis—updated. Curr Opin Plant Biol 15(1):31–37. https://doi.org/10.1016/j.pbi.2011.10.010
Hu Z, Liu T, Cao J (2019) Functional similarity and difference among Bra-MIR319 family in plant development. Genes 10(12):952. https://doi.org/10.3390/genes10120952
Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138(19):4117–4129. https://doi.org/10.1242/dev.063511
Íñiguez LP, Nova-Franco B, Hernández G (2015) Novel players in the AP2-miR172 regulatory network for common bean nodulation. Plant Signal Behav 10(10):e1062957. https://doi.org/10.1080/15592324.2015.1062957
Jodder J (2021) Regulation of pri-MIRNA processing: mechanistic insights into the miRNA homeostasis in plant. Plant Cell Rep 40(5):783–798. https://doi.org/10.1007/s00299-020-02660-7
Jozefczuk J, Adjaye J (2011) Quantitative real-time PCR-based analysis of gene expression. Methods Enzymol 500:99–109. https://doi.org/10.1016/B978-0-12-385118-5.00006-2
Jung JH, Seo PJ, Kang SK, Park CM (2011) miR172 signals are incorporated into the miR156 signaling pathway at the SPL3/4/5 genes in Arabidopsis developmental transitions. Plant Mol Biol 76(1–2):35–45. https://doi.org/10.1007/s11103-011-9759-z
Jung JH, Lee S, Yun J, Lee M, Park CM (2014) The miR172 target TOE3 represses AGAMOUS expression during Arabidopsis floral patterning. Plant Sci 215–216:29–38. https://doi.org/10.1016/j.plantsci.2013.10.010
Kidokoro S, Shinozaki K, Yamaguchi-Shinozak K (2022) Transcriptional regulatory network of plant cold-stress responses. Trends Plant Sci 27(9):922–935. https://doi.org/10.1016/j.tplants.2022.01.008
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Lee DY, An G (2012) Two AP2 family genes, SUPERNUMERARY BRACT (SNB) and OsINDETERMINATE SPIKELET 1 (OsIDS1), synergistically control inflorescence architecture and floral meristem establishment in rice. Plant J 69(3):445–461. https://doi.org/10.1111/j.1365-313X.2011.04804.x
Lee YS, Lee DY, Cho LH, An G (2014) Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice (new York, N.y.) 7(1):31. https://doi.org/10.1186/s12284-014-0031-4
Li JW, Zhang XC, Wang MR, Bi WL, Faisal M, da Silva JAT, Volk GM, Wang QC (2019a) Development, progress and future prospects in cryobiotechnology of Lilium spp. Plant Methods 15:125. https://doi.org/10.1186/s13007-019-0506-9
Li Z, An X, Zhu T et al (2019b) Discovering and constructing ceRNA-miRNA-target gene regulatory networks during anther development in maize. Int J Mol Sci 20(14):3480. https://doi.org/10.3390/ijms20143480
Lian H, Wang L, Ma N et al (2021) Redundant and specific roles of individual MIR172 genes in plant development. PLoS Biol 19(2):e3001044. https://doi.org/10.1371/journal.pbio.3001044
Luo X, Yin M, He Y (2021) Molecular genetic understanding of photoperiodic regulation of flowering time in Arabidopsis and soybean. Int J Mol Sci 23(1):466. https://doi.org/10.3390/ijms23010466
Ma X, Feng F, Zhang Y, Elesawi IE, Xu K, Li T et al (2019) A novel rice grain size gene OsSNB was identified by genome-wide association study in natural population. PLoS Genet 15(5):e1008191. https://doi.org/10.1371/journal.pgen.1008191
Ma Y, Xue H, Zhang F, Jiang Q, Yang S, Yue P, Wang F, Zhang Y, Li L, He P, Zhang Z (2021) The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression. Plant Biotechnol J 19(2):311–323. https://doi.org/10.1111/pbi.13464
Megha S, Basu U, Kav NNV (2018) Regulation of low temperature stress in plants by microRNAs. Plant Cell Environ 41(1):1–15. https://doi.org/10.1111/pce.12956
Merel LG, Geert JDK, Anton C (2003) Phase change in lily bulblets regenerated in vitro. Physiol Plant 119(4):590–597. https://doi.org/10.1046/j.1399-3054.2003.00214.x
Miculan M, Nelissen H, Ben Hassen M et al (2021) A forward genetics approach integrating genome-wide association study and expression quantitative trait locus mapping to dissect leaf development in maize (Zea mays). Plant J 107(4):1056–1071. https://doi.org/10.1111/tpj.15364
Ohto M, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K (2001) Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol 127(1):252–261. https://doi.org/10.1104/pp.127.1.252
Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Warthmann N, Allen E, Dezulian T, Huson D, Carrington JC, Weigel D (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13:115–125. https://doi.org/10.1016/j.devcel.2007.04.012
Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genet Dev 19(4):374–378. https://doi.org/10.1016/j.gde.2009.06.001
Rao S, Li Y, Chen J (2021) Combined analysis of microRNAs and target genes revealed miR156-SPLs and miR172-AP2 are involved in a delayed flowering phenomenon after chromosome doubling in black goji (Lycium ruthencium). Front Genet 12:706930. https://doi.org/10.3389/fgene.2021.706930
Seo PJ, Ryu J, Kang SK, Park CM (2011) Modulation of sugar metabolism by an INDETERMINATE DOMAIN transcription factor contributes to photoperiodic flowering in Arabidopsis. Plant J 65(3):418–429. https://doi.org/10.1111/j.1365-313X.2010.04432.x
Seo PJ, Park MJ, Park CM (2013) Alternative splicing of transcription factors in plant responses to low temperature stress: mechanisms and functions. Planta 237(6):1415–1424. https://doi.org/10.1007/s00425-013-1882-4
Shi R, Xu W, Liu T, Cai C, Li S (2021) VrLELP controls flowering time under short-day conditions in Arabidopsis. J Plant Res 134(1):141–149. https://doi.org/10.1007/s10265-020-01235-7
Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68(12):2013–2037. https://doi.org/10.1007/s00018-011-0673-y
Tripathi RK, Bregitzer P, Singh J (2018) Genome-wide analysis of the SPL/miR156 module and its interaction with the AP2/miR172 unit in barley. Sci Rep 8(1):7085. https://doi.org/10.1038/s41598-018-25349-0
Waheed S, Anwar M, Saleem MA, Wu J, Tayyab M, Hu Z (2021) The critical role of small RNAs in regulating plant innate immunity. Biomolecules 11(2):184. https://doi.org/10.3390/biom11020184
Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749. https://doi.org/10.1016/j.cell.2009.06.014
Wollmann H, Mica E, Todesco M, Long JA, Weigel D (2010) On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137(21):3633–3642. https://doi.org/10.1242/dev.036673
Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750–759. https://doi.org/10.1016/j.cell.2009.06.031
Wu Y, Sun M, Li S, Min R, Gao C, Lyu Q, Ren Z, Xia Y (2021) Molecular cloning, characterization and expression analysis of three key starch synthesis-related genes from the bulb of a rare lily germplasm, Lilium brownii var. giganteum. J Zhejiang Univ Sci B 22(6):476–491. https://doi.org/10.1631/jzus.B2000545
Xie Z, Nolan TM, Jiang H, Yin Y (2019) AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Front Plant Sci 10:228. https://doi.org/10.3389/fpls.2019.00228
Xiong JS, Zheng D, Zhu HY, Chen JQ, Na R, Cheng ZM (2018) Genome-wide identification and expression analysis of the SPL gene family in woodland strawberry Fragaria vesca. Genome 61(9):675–683. https://doi.org/10.1139/gen-2018-0014
Yang FX, Zhu GF, Wang Z, Liu HL, Huang D (2015) A putative miR172-targeted CeAPETALA2-like gene is involved in floral patterning regulation of the orchid Cymbidium ensifolium. Genet Mol Res 14(4):12049–12061. https://doi.org/10.4238/2015.October.5.18
Zheng C, Ye M, Sang M, Wu R (2019) A regulatory network for miR156-SPL module in Arabidopsis thaliana. Int J Mol Sci 20(24):6166. https://doi.org/10.3390/ijms20246166
Zhu QH, Helliwell CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62(2):487–495. https://doi.org/10.1093/jxb/erq295
Acknowledgements
We are grateful to Dr. Yian Pu of the Institute of Tropical Biotechnology, Chinese Academy of Tropical Agricultural Sciences (ITBB, CATAS) for providing the vector.
Funding
This study was supported by the Beijing Innovation Consortium of Agriculture Research System (project number: BAIC09-2022).
Author information
Authors and Affiliations
Contributions
Conceived and designed the experiments: JF, YW, and KZ. Analyzed the data: JF and WG. Wrote the paper: JF. Revised the paper: JC and JF. All the authors contributed to the article and approved the submitted version.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
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.
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.
About this article
Cite this article
Feng, J., Wang, Y., Ge, W. et al. Regulatory mechanism of the miR172e–LbrAP2 module during the vegetative growth phase transition in Lilium. Planta 259, 26 (2024). https://doi.org/10.1007/s00425-023-04308-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04308-8