Multiple Functions of MiRNAs in Brassica napus L.
Abstract
:1. Introduction
2. MiRNAs and Development Regulation in B. napus
3. MiRNAs and Abiotic Stress in B. napus
Stress | MicroRNAs | References |
---|---|---|
Salt and drought stress | Multiple miRNAs | [109,111] |
Drought stress | miR169 | [110] |
Cadmium stress | miR158, miR167, miR395, etc. | [112,113,114,115,116,117,118] |
Nutrient stress | miR395, miR398, miR399, etc. | [120,121,122,123] |
Vascular disease | miR168 | [125] |
Sclerotinia rot | miR159, miR5139, miR390, etc. | [126,127,128] |
Clubroot disease | Multiple miRNAs | [129] |
4. MiRNAs and Biotic Stress in B. napus
5. Discussion and Future Perspectives
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Tian, C.; Zhou, X.; Liu, Q.; Peng, J.; Zhang, Z.; Song, H.; Ding, Z.; Zhran, M.A.; Eissa, M.A.; Kheir, A.M.S.; et al. Increasing yield, quality and profitability of winter oilseed rape (Brassica napus) under combinations of nutrient levels in fertiliser and planting density. Crop Pasture Sci. 2020, 71, 1010–1019. [Google Scholar] [CrossRef]
- Fu, D.; Jiang, L.; Mason, A.S.; Xiao, M.; Zhu, L.; Li, L.; Zhou, Q.; Shen, C.; Huang, C. Research progress and strategies for multifunctional rapeseed: A case study of China. J. Integr. Agric. 2016, 15, 1673–1684. [Google Scholar] [CrossRef] [Green Version]
- Zhu, M.; Monroe, J.G.; Suhail, Y.; Villiers, F.; Mullen, J.; Pater, D.; Hauser, F.; Jeon, B.W.; Bader, J.S.; Kwak, J.M.; et al. Molecular and systems approaches towards drought-tolerant canola crops. New Phytol. 2016, 210, 1169–1189. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dresselhaus, T.; Hückelhoven, R. Biotic and abiotic stress responses in crop plants. Agron J. 2018, 8, 267. [Google Scholar] [CrossRef] [Green Version]
- Lohani, N.; Jain, D.; Singh, M.B.; Bhalla, P.L. Engineering multiple abiotic stress tolerance in canola, Brassica napus. Front. Plant Sci. 2020, 11, 3. [Google Scholar] [CrossRef] [PubMed]
- So, K.K.Y.; Duncan, R.W. Breeding canola (Brassica napus L.) for protein in feed and food. Plants 2021, 10, 2220. [Google Scholar] [CrossRef] [PubMed]
- Guo, Z.; Wang, X.; Wang, Y.; Li, W.; Gal-On, A.; Ding, S. Identification of a new host factor required for antiviral RNAi and amplification of viral siRNAs. Plant Physiol. 2017, 176, 1587–1597. [Google Scholar] [CrossRef]
- Wu, P.H.; Zamore, P.D. Defining the functions of PIWI-interacting RNAs. Nat. Rev. Mol. Cell Bio. 2021, 22, 239–240. [Google Scholar] [CrossRef]
- Zhang, L.; Xiang, Y.; Chen, S.; Shi, M.; Jiang, X.; He, Z.; Gao, S. Mechanisms of microRNA biogenesis and stability control in plants. Front. Plant Sci. 2022, 13, 844149. [Google Scholar] [CrossRef]
- Cui, C.; Wang, J.; Zhao, J.; Fang, Y.; He, X.; Guo, H.; Duan, C. A brassica miRNA regulates plant growth and immunity through distinct modes of action. Mol. Plant. 2020, 13, 231–245. [Google Scholar] [CrossRef]
- Begum, Y. Regulatory role of microRNAs (miRNAs) in the recent development of abiotic stress tolerance of plants. Gene 2022, 821, 146283. [Google Scholar] [CrossRef] [PubMed]
- Chand Jha, U.; Nayyar, H.; Mantri, N.; Siddique, K.H.M. Non-Coding RNAs in legumes: Their emerging roles in regulating biotic/abiotic stress responses and plant growth and development. Cells 2021, 10, 1674. [Google Scholar] [CrossRef] [PubMed]
- Lee, R.C.; Feinbaum, R.L.; Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75, 843–854. [Google Scholar] [CrossRef]
- Ambros, V.; Bartel, B.; Bartel, D.P.; Burge, C.B.; Carrington, J.C.; Chen, X.; Dreyfuss, G.; Eddy, S.R.; Griffiths-Jones, S.; Marshall, M.; et al. A uniform system for microRNA annotation. RNA 2003, 9, 277–279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Griffiths-Jones, S.; Grocock, R.J.; van Dongen, S.; Bateman, A.; Enright, A.J. MiRBase: MicroRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 2006, 34, 140–144. [Google Scholar] [CrossRef]
- Liu, H.; Jin, T.; Liao, R.; Wan, L.; Xu, B.; Zhou, S.; Guan, J. miRFANs: An integrated database for Arabidopsis thaliana microRNA function annotations. BMC Plant Biol. 2012, 12, 68. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.; Liu, X.; Zhang, S.; Liang, S.; Luan, W.; Ma, X. TarDB: An online database for plant miRNA targets and miRNA-triggered phased siRNAs. BMC Genom. 2021, 22, 348. [Google Scholar] [CrossRef]
- Chen, C.; Li, J.; Feng, J.; Liu, B.; Feng, L.; Yu, X.; Li, G.; Zhai, J.; Meyers, B.C.; Xia, R. sRNAanno—A database repository of uniformly annotated small RNAs in plants. Hortic. Res. 2021, 8, 45. [Google Scholar] [CrossRef]
- Yu, B.; Yang, Z.; Li, J.; Minakhina, S.; Yang, M.; Padgett, R.W.; Steward, R.; Chen, X. Methylation as a crucial step in plant microRNA biogenesis. Science 2005, 307, 932–935. [Google Scholar] [CrossRef] [Green Version]
- O’Brien, J.; Hayder, H.; Zayed, Y.; Peng, C. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front. Endocrinol. 2018, 9, 402. [Google Scholar] [CrossRef]
- Han, M.H.; Goud, S.; Song, L.; Fedoroff, N. The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl. Acad. Sci. USA 2004, 101, 1093–1098. [Google Scholar] [CrossRef] [Green Version]
- Machida, S.; Chen, H.; Adam Yuan, Y. Molecular insights into miRNA processing by Arabidopsis thaliana SERRATE. Nucleic Acids Res. 2011, 39, 7828–7836. [Google Scholar] [CrossRef]
- Dolata, J.; Taube, M.; Bajczyk, M.; Jarmolowski, A.; Szweykowska-Kulinska, Z.; Bielewicz, D. Regulation of plant microprocessor function in shaping microRNA landscape. Front. Plant Sci. 2018, 9, 753. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Addo-Quaye, C.; Eshoo, T.W.; Bartel, D.P.; Axtell, M.J. Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr. Biol. 2008, 18, 758–762. [Google Scholar] [CrossRef] [Green Version]
- Reinhart, B.J.; Weinstein, E.G.; Rhoades, M.W.; Bartel, B.; Bartel, D.P. MicroRNAs in plants. Gene Dev. 2002, 16, 1616–1626. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Juarez, M.T.; Kui, J.S.; Thomas, J.; Heller, B.A.; Timmermans, M.C. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 2004, 428, 84–88. [Google Scholar] [CrossRef] [PubMed]
- Liu, B.; Li, P.; Li, X.; Liu, C.; Cao, S.; Chu, C.; Cao, X. Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol. 2005, 139, 296–305. [Google Scholar] [CrossRef] [Green Version]
- Park, W.; Li, J.; Song, R.; Messing, J.; Chen, X. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 2002, 12, 1484–1495. [Google Scholar] [CrossRef] [Green Version]
- Bollman, K.M.; Aukerman, M.J.; Park, M.Y.; Hunter, C.; Berardini, T.Z.; Poethig, R.S. HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 2003, 130, 1493–1504. [Google Scholar] [CrossRef] [Green Version]
- Liu, P.P.; Montgomery, T.A.; Fahlgren, N.; Kasschau, K.D.; Nonogaki, H.; Carrington, J.C. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J. 2007, 52, 133–146. [Google Scholar] [CrossRef]
- Kim, J.Y.; Lee, H.J.; Jung, H.J.; Maruyama, K.; Suzuki, N.; Kang, H. Overexpression of microRNA395c or 395e affects differently the seed germination of Arabidopsis thaliana under stress conditions. Planta 2010, 232, 1447–1454. [Google Scholar] [CrossRef] [PubMed]
- Juarez, M.; Timmermans, M. MiRNAs specify dorsoventral polarity during leaf development. Dev. Biol. 2004, 271, 551–552. [Google Scholar]
- Emery, J.F.; Floyd, S.K.; Alvarez, J.; Eshed, Y.; Hawker, N.P.; Izhaki, A.; Baum, S.F.; Bowman, J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 2003, 13, 1768–1774. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bao, N.; Lye, K.W.; Barton, M.K. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev. Cell. 2004, 7, 653–662. [Google Scholar] [CrossRef]
- Mallory, A.C.; Reinhart, B.J.; Jones-Rhoades, M.W.; Tang, G.; Zamore, P.D.; Barton, M.K.; Bartel, D.P. MicroRNA control of PHABULOSA in leaf development: Importance of pairing to the microRNA 5’ region. Embo J. 2004, 23, 3356–3364. [Google Scholar] [CrossRef] [Green Version]
- Williams, L.; Grigg, S.P.; Xie, M.; Christensen, S.; Fletcher, J.C. Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 2005, 132, 3657–3668. [Google Scholar] [CrossRef] [Green Version]
- Yang, J.H.; Han, S.J.; Yoon, E.K.; Lee, W.S. Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res. 2006, 34, 1892–1899. [Google Scholar] [CrossRef] [Green Version]
- Rodriguez, R.E.; Mecchia, M.A.; Debernardi, J.M.; Schommer, C.; Weigel, D.; Palatnik, J.F. Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 2010, 137, 103–112. [Google Scholar] [CrossRef] [Green Version]
- Palatnik, J.F.; Allen, E.; Wu, X.; Schommer, C.; Schwab, R.; Carrington, J.C.; Weigel, D. Control of leaf morphogenesis by microRNAs. Nature 2003, 425, 257–263. [Google Scholar] [CrossRef] [Green Version]
- Nonogaki, H. MicroRNA gene regulation cascades during early stages of plant development. Plant Cell Physiol. 2010, 51, 1840–1846. [Google Scholar] [CrossRef] [Green Version]
- Lauter, N.; Kampani, A.; Carlson, S.; Goebel, M.; Moose, S.P. microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc. Natl. Acad. Sci. USA 2005, 102, 9412–9417. [Google Scholar] [CrossRef] [PubMed]
- Sun, C.; Zhao, Q.; Liu, D.; You, C.; Hao, Y. Ectopic expression of the apple Md-miRNA156h gene regulates flower and fruit development in Arabidopsis. Plant Cell. 2013, 112, 343–351. [Google Scholar] [CrossRef]
- Baker, C.C.; Sieber, P.; Wellmer, F.; Meyerowitz, E.M. The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr. Biol. 2005, 15, 303–315. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aukerman, M.J.; Sakai, H. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell. 2003, 15, 2730–2741. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, Q.H.; Upadhyaya, N.M.; Gubler, F.; Helliwell, C.A. Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol. 2009, 9, 149. [Google Scholar] [CrossRef] [Green Version]
- Jung, J.H.; Lee, S.; Yun, J.; Lee, M.; Park, C.M. The miR172 target TOE3 represses AGAMOUS expression during Arabidopsis floral patterning. Plant Sci. 2014, 215–216, 29–38. [Google Scholar] [CrossRef]
- Khanna-Chopra, R. Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma 2012, 249, 469–481. [Google Scholar] [CrossRef]
- Zhang, Y.; Yin, S.; Tu, Y.; Mei, H.; Yang, Y. A novel microRNA, SlymiR208, promotes leaf senescence via regulating cytokinin biosynthesis in tomato. Physiol Plant. 2020, 169, 143–155. [Google Scholar] [CrossRef]
- Li, Z.; Peng, J.; Wen, X.; Guo, H. Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell. 2013, 25, 3311–3328. [Google Scholar] [CrossRef] [Green Version]
- Qiu, K.; Li, Z.; Yang, Z.; Chen, J.; Wu, S.; Zhu, X.; Gao, S.; Gao, J.; Ren, G.; Kuai, B.; et al. EIN3 and ORE1 accelerate degreening during ethylene-mediated leaf senescence by directly activating chlorophyll catabolic genes in Arabidopsis. PLoS Genet. 2015, 11, e1005399. [Google Scholar] [CrossRef]
- Zhang, B.; Pan, X.; Cobb, G.P.; Anderson, T.A. Plant microRNA: A small regulatory molecule with big impact. Dev. Biol. 2006, 289, 3–16. [Google Scholar] [CrossRef] [PubMed]
- Esmaeili, F.; Shiran, B.; Fallahi, H.; Mirakhorli, N.; Budak, H.; Martínez-Gómez, P. In silico search and biological validation of microRNAs related to drought response in peach and almond. Funct. Integr. Genom. 2017, 17, 189–201. [Google Scholar] [CrossRef] [PubMed]
- Ding, Y.; Tao, Y.; Zhu, C. Emerging roles of microRNAs in the mediation of drought stress response in plants. J. Exp. Bot. 2013, 64, 3077–3086. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.; Li, Z.; Xiong, L. A plant microRNA regulates the adaptation of roots to drought stress. FEBS Lett. 2012, 586, 1742–1747. [Google Scholar] [CrossRef] [Green Version]
- Gao, P.; Bai, X.; Yang, L.; Lv, D.; Pan, X.; Li, Y.; Cai, H.; Ji, W.; Chen, Q.; Zhu, Y. Osa-MIR393: A salinity- and alkaline stress-related microRNA gene. Mol. Biol. Rep. 2011, 38, 237–242. [Google Scholar] [CrossRef]
- Shi, G.; Fu, J.; Rong, L.; Zhang, P.; Guo, C.; Xiao, K. TaMIR1119, a miRNA family member of wheat (Triticum aestivum), is essential in the regulation of plant drought tolerance. J. Integr. Agric. 2018, 17, 2369–2378. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.; Ye, Y.; Xu, M.; Feng, L.; Xu, L.A. Roles of the SPL gene family and miR156 in the salt stress responses of tamarisk (Tamarix chinensis). BMC Plant Biol. 2019, 19, 370. [Google Scholar] [CrossRef] [Green Version]
- Giacomelli, J.I.; Weigel, D.; Chan, R.L.; Manavella, P.A. Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytol. 2012, 195, 766–773. [Google Scholar] [CrossRef]
- Sunkar, R.; Zhu, J.K. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell. 2004, 16, 2001–2019. [Google Scholar] [CrossRef] [Green Version]
- Dong, C.; Pei, H. Over-expression of miR397 improves plant tolerance to cold stress in Arabidopsis thaliana. J. Plant Biol. 2014, 57, 209–217. [Google Scholar] [CrossRef]
- Thiebaut, F.; Rojas, C.A.; Almeida, K.L.; Grativol, C.; Domiciano, G.C.; Lamb, C.R.; Engler Jde, A.; Hemerly, A.S.; Ferreira, P.C. Regulation of miR319 during cold stress in sugarcane. Plant Cell Environ. 2012, 35, 502–512. [Google Scholar] [CrossRef] [PubMed]
- Lv, D.K.; Bai, X.; Li, Y.; Ding, X.D.; Ge, Y.; Cai, H.; Ji, W.; Wu, N.; Zhu, Y.M. Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 2010, 459, 39–47. [Google Scholar] [CrossRef]
- Wang, S.T.; Sun, X.L.; Hoshino, Y.; Yu, Y.; Jia, B.; Sun, Z.W.; Sun, M.Z.; Duan, X.B.; Zhu, Y.M. MicroRNA319 positively regulates cold tolerance by targeting OsPCF6 and OsTCP21 in rice (Oryza sativa L.). PLoS ONE 2014, 9, e91357. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Valiollahi, E.; Farsi, M.; Kakhki, A.M. Sly-miR166 and Sly-miR319 are components of the cold stress response in Solanum lycopersicum. Plant Biotechnol. Rep. 2014, 8, 349–356. [Google Scholar] [CrossRef]
- Lv, D.W.; Zhen, S.; Zhu, G.R.; Bian, Y.W.; Chen, G.X.; Han, C.X.; Yu, Z.T.; Yan, Y.M. High-throughput sequencing reveals H2O2 stress-associated microRNAs and a potential regulatory network in Brachypodium distachyon seedlings. Front. Plant Sci. 2016, 7, 1567. [Google Scholar] [CrossRef] [Green Version]
- Bai, Q.; Wang, X.; Chen, X.; Shi, G.; Liu, Z.; Guo, C.; Xiao, K. Wheat miRNA TaemiR408 acts as an essential mediator in plant tolerance to Pi deprivation and salt stress via modulating stress-associated physiological processes. Front. Plant Sci. 2018, 9, 499. [Google Scholar] [CrossRef]
- Gifford, M.L.; Dean, A.; Gutierrez, R.A.; Coruzzi, G.M.; Birnbaum, K.D. Cell-specific nitrogen responses mediate developmental plasticity. Proc. Natl. Acad. Sci. USA 2008, 105, 803–808. [Google Scholar] [CrossRef] [Green Version]
- Chauhan, S.; Yogindran, S.; Rajam, M.V. Role of miRNAs in biotic stress reactions in plants. Ind. J. Plant Physiol. 2017, 22, 514–529. [Google Scholar] [CrossRef]
- Zhu, X.; He, S.; Fang, D.; Guo, L.; Zhou, X.; Guo, Y.; Gao, L.; Qiao, Y. High-throughput sequencing-based identification of Arabidopsis miRNAs induced by phytophthora capsici Infection. Front. Microbiol. 2020, 11, 1094. [Google Scholar] [CrossRef]
- Zhao, X.; Shan, Y.; Zhao, Y.; Wang, A.; Wang, Z. A novel Arabidopsis miRNA, ath-miR38-3P, is involved in response to Sclerotinia sclerotiorum infection. J. Integr. Agric. 2016, 15, 2556–2562. [Google Scholar] [CrossRef]
- Xie, S.; Jiang, H.; Xu, Z.; Xu, Q.; Cheng, B. Small RNA profiling reveals important roles for miRNAs in Arabidopsis response to Bacillus velezensis FZB42. Gene 2017, 629, 9–15. [Google Scholar] [CrossRef] [PubMed]
- Xin, M.; Wang, Y.; Yao, Y.; Xie, C.; Peng, H.; Ni, Z.; Sun, Q. Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol. 2010, 10, 123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feng, J.; Liu, S.; Wang, M.; Lang, Q.; Jin, C. Identification of microRNAs and their targets in tomato infected with Cucumber mosaic virus based on deep sequencing. Planta 2014, 240, 1335–1352. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Bao, Y.; Shan, D.; Wang, Z.; Song, X.; Wang, Z.; Wang, J.; He, L.; Wu, L.; Zhang, Z.; et al. Magnaporthe oryzae induces the expression of a microRNA to suppress the immune response in rice. Plant Physiol. 2018, 177, 352–368. [Google Scholar] [CrossRef] [Green Version]
- Zhu, Q.H.; Fan, L.; Liu, Y.; Xu, H.; Llewellyn, D.; Wilson, I. miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLoS ONE 2013, 8, e84390. [Google Scholar] [CrossRef] [Green Version]
- Yang, L.; Mu, X.; Liu, C.; Cai, J.; Shi, K.; Zhu, W.; Yang, Q. Overexpression of potato miR482e enhanced plant sensitivity to Verticillium dahliae infection. J. Integr. Plant Biol. 2015, 57, 1078–1088. [Google Scholar] [CrossRef]
- Su, Y.; Li, H.G.; Wang, Y.; Li, S.; Wang, H.L.; Yu, L.; He, F.; Yang, Y.; Feng, C.H.; Shuai, P.; et al. Poplar miR472a targeting NBS-LRRs is involved in effective defence against the necrotrophic fungus Cytospora chrysosperma. J. Exp. Bot. 2018, 69, 5519–5530. [Google Scholar] [CrossRef]
- Yan, J.; Zhang, H.; Zheng, Y.; Ding, Y. Comparative expression profiling of miRNAs between the cytoplasmic male sterile line MeixiangA and its maintainer line MeixiangB during rice anther development. Planta 2015, 241, 109–123. [Google Scholar] [CrossRef]
- Yu, Y.; Sun, F.; Chen, N.; Sun, G.; Wang, C.Y.; Wu, D.X. MiR396 regulatory network and its expression during grain development in wheat. Protoplasma 2021, 258, 103–113. [Google Scholar] [CrossRef]
- Silva, E.M.; Silva GFFe Bidoia, D.B.; Silva Azevedo, M.; Jesus, F.A.; Pino, L.E.; Peres, L.E.P.; Carrera, E.; López-Díaz, I.; Nogueira, F.T.S. MicroRNA159-targeted SlGAMYB transcription factors are required for fruit set in tomato. Plant J. 2017, 92, 95–109. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Z.; Wei, L.; Zou, X.; Tao, Y.; Liu, Z.; Zheng, Y. Submergence-responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann. Bot. 2008, 102, 509–519. [Google Scholar] [CrossRef] [PubMed]
- Csukasi, F.; Donaire, L.; Casanal, A.; Martinez-Priego, L.; Botella, M.A.; Medina-Escobar, N.; Llave, C.; Valpuesta, V. Two strawberry miR159 family members display developmental-specific expression patterns in the fruit receptacle and cooperatively regulate Fa-GAMYB. New Phytol. 2012, 195, 47–57. [Google Scholar] [CrossRef] [PubMed]
- Ortiz-Morea, F.A.; Vicentini, R.; Silva, G.F.; Silva, E.M.; Carrer, H.; Rodrigues, A.P.; Nogueira, F.T. Global analysis of the sugarcane microtranscriptome reveals a unique composition of small RNAs associated with axillary bud outgrowth. J. Exp. Bot. 2013, 64, 2307–2320. [Google Scholar] [CrossRef] [PubMed]
- Xing, L.; Zhang, D.; Zhao, C.; Li, Y.; Ma, J.; An, N.; Han, M. Shoot bending promotes flower bud formation by miRNA-mediated regulation in apple (Malus domestica Borkh.). Plant Biotechnol. J. 2016, 14, 749–770. [Google Scholar] [CrossRef] [Green Version]
- Yang, Z.; Zhu, P.; Kang, H.; Liu, L.; Cao, Q.; Sun, J.; Dong, T.; Zhu, M.; Li, Z.; Xu, T. High-throughput deep sequencing reveals the important role that microRNAs play in the salt response in sweet potato (Ipomoea batatas L.). BMC Genom. 2020, 21, 164. [Google Scholar] [CrossRef] [Green Version]
- Li, X.; Bian, H.; Song, D.; Ma, S.; Han, N.; Wang, J.; Zhu, M. Flowering time control in ornamental gloxinia (Sinningia speciosa) by manipulation of miR159 expression. Ann. Bot. 2013, 111, 791–799. [Google Scholar] [CrossRef] [Green Version]
- Xu, P.; Zhu, Y.; Zhang, Y.; Jiang, J.; Yang, L.; Mu, J.; Yu, X.; He, Y. Global analysis of the genetic variations in miRNA-targeted sites and their correlations with agronomic traits in rapeseed. Front. Genet. 2021, 12, 741858. [Google Scholar] [CrossRef]
- Xu, M.Y.; Dong, Y.; Zhang, Q.X.; Zhang, L.; Luo, Y.Z.; Sun, J.; Fan, Y.L.; Wang, L. Identification of miRNAs and their targets from Brassica napus by high-throughput sequencing and degradome analysis. BMC Genom. 2012, 13, 421. [Google Scholar] [CrossRef] [Green Version]
- Xie, F.L.; Huang, S.Q.; Guo, K.; Xiang, A.L.; Zhu, Y.Y.; Nie, L.; Yang, Z.M. Computational identification of novel microRNAs and targets in Brassica napus. FEBS Lett. 2007, 581, 1464–1474. [Google Scholar] [CrossRef] [Green Version]
- Cheng, H.; Hao, M.; Wang, W.; Mei, D.; Tong, C.; Wang, H.; Liu, J.; Fu, L.; Hu, Q. Genomic identification, characterization and differential expression analysis of SBP-box gene family in Brassica napus. BMC Plant Biol. 2016, 16, 196. [Google Scholar] [CrossRef] [Green Version]
- Cheng, H.; Hao, M.; Wang, W.; Mei, D.; Wells, R.; Liu, J.; Wang, H.; Sang, S.; Tang, M.; Zhou, R.; et al. Integrative RNA- and miRNA-profile analysis reveals a likely role of BR and auxin signaling in branch angle regulation of B. napus. Int. J. Mol. Sci. 2017, 18, 887. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Ping, X.; Cao, Y.; Jian, H.; Gao, Y.; Wang, J.; Tan, Y.; Xu, X.; Lu, K.; Li, J.; et al. Genome-wide exploration and characterization of miR172/euAP2 genes in Brassica napus L. for likely role in flower organ development. BMC Plant Biol. 2019, 19, 336. [Google Scholar] [CrossRef] [Green Version]
- Jiang, J.; Xu, P.; Li, Y.; Li, Y.; Zhou, X.; Jiang, M.; Zhang, J.; Zhu, J.; Wang, W.; Yang, L. Identification of miRNAs and their target genes in genic male sterility lines in Brassica napus by small RNA sequencing. BMC Plant Biol. 2021, 21, 520. [Google Scholar] [CrossRef] [PubMed]
- Korbes, A.P.; Machado, R.D.; Guzman, F.; Almerao, M.P.; de Oliveira, L.F.; Loss-Morais, G.; Turchetto-Zolet, A.C.; Cagliari, A.; dos Santos Maraschin, F.; Margis-Pinheiro, M.; et al. Identifying conserved and novel microRNAs in developing seeds of Brassica napus using deep sequencing. PLoS ONE 2012, 7, e50663. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Chen, L.; Zhang, X.; Liu, T.; Niu, S.; Wen, J.; Yi, B.; Ma, C.; Tu, J.; Fu, T.; et al. Identification of miRNAs that regulate silique development in Brassica napus. Plant Sci. 2018, 269, 106–117. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Huo, Q.; Yang, H.; Jian, H.; Qu, C.; Lu, K.; Li, J. Joint RNA-Seq and miRNA profiling analyses to reveal molecular mechanisms in regulating thickness of pod canopy in Brassica napus. Genes 2019, 10, 591. [Google Scholar] [CrossRef] [Green Version]
- Huang, D.; Koh, C.; Feurtado, J.A.; Tsang, E.W.; Cutler, A.J. MicroRNAs and their putative targets in Brassica napus seed maturation. BMC Genom. 2013, 14, 140. [Google Scholar] [CrossRef] [Green Version]
- Wei, W.; Li, G.; Jiang, X.; Wang, Y.; Ma, Z.; Niu, Z.; Wang, Z.; Geng, X. Small RNA and degradome profiling involved in seed development and oil synthesis of Brassica napus. PLoS ONE 2018, 13, e0204998. [Google Scholar] [CrossRef] [Green Version]
- Tan, M.; Niu, J.; Peng, D.Z.; Cheng, Q.; Luan, M.B.; Zhang, Z.Q. Clone and function verification of the OPR gene in Brassica napus related to linoleic acid synthesis. BMC Plant Biol. 2022, 22, 192. [Google Scholar] [CrossRef]
- Zhao, Y.T.; Wang, M.; Fu, S.X.; Yang, W.C.; Qi, C.K.; Wang, X.J. Small RNA profiling in two Brassica napus cultivars identifies microRNAs with oil production- and development-correlated expression and new small RNA classes. Plant Physiol. 2012, 158, 813–823. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.; Jian, H.; Wang, T.; Wei, L.; Li, J.; Li, C.; Liu, L. Identification of microRNAs actively involved in fatty acid biosynthesis in developing Brassica napus seeds using high-throughput sequencing. Front. Plant Sci. 2016, 7, 1570. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Qiao, Y.; Zhang, J.; Shi, W.; Zhang, J. Genome wide identification of microRNAs involved in fatty acid and lipid metabolism of Brassica napus by small RNA and degradome sequencing. Gene 2017, 619, 61–70. [Google Scholar] [CrossRef] [PubMed]
- Singroha, G.; Sharma, P.; Sunkur, R. Current status of microRNA-mediated regulation of drought stress responses in cereals. Physiol Plant. 2021, 172, 1808–1821. [Google Scholar] [CrossRef] [PubMed]
- Cheng, X.; He, Q.; Tang, S.; Wang, H.; Zhang, X.; Lv, M.; Liu, H.; Gao, Q.; Zhou, Y.; Wang, Q.; et al. The miR172/IDS1 signaling module confers salt tolerance through maintaining ROS homeostasis in cereal crops. New Phytol. 2021, 230, 1017–1033. [Google Scholar] [CrossRef] [PubMed]
- Lantzouni, O.; Alkofer, A.; Falter-Braun, P.; Schwechheimer, C. Growth-regulating factors interact with DELLAs and regulate growth in cold stress. Plant Cell. 2020, 32, 1018–1034. [Google Scholar] [CrossRef] [PubMed]
- Pegler, J.L.; Oultram, J.M.J.; Nguyen, D.Q.; Grof, C.P.L.; Eamens, A.L. MicroRNA-mediated responses to cadmium stress in Arabidopsis thaliana. Plants 2021, 10, 130. [Google Scholar] [CrossRef]
- Eshkiki, E.M.; Hajiahmadi, Z.; Abedi, A.; Kordrostami, M.; Jacquard, C. In Silico analyses of autophagy-related genes in rapeseed (Brassica napus L.) under different abiotic stresses and in various tissues. Plants 2020, 9, 1393. [Google Scholar] [CrossRef]
- Jatan, R.; Lata, C. Role of microRNAs in abiotic and biotic stress resistance in plants. Proc. Indian Natl. Sci. Acad. 2019, 85, 553–567. [Google Scholar]
- Jian, H.; Wang, J.; Wang, T.; Wei, L.; Li, J.; Liu, L. Identification of rapeseed microRNAs involved in early stage seed germination under salt and drought stresses. Front. Plant Sci. 2016, 7, 658. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Duan, Y.; Sun, N.; Wang, L.; Feng, S.; Fang, Y.; Wang, Y. The miR169n-NF-YA8 regulation module involved in drought resistance in Brassica napus L. Plant Sci. 2021, 313, 111062. [Google Scholar] [CrossRef]
- Megha, S.; Basu, U.; Joshi, R.K.; Kav, N.N.V. Physiological studies and genome-wide microRNA profiling of cold-stressed Brassica napus. Plant Physiol. Biochem. 2018, 132, 1–17. [Google Scholar] [CrossRef] [PubMed]
- Huang, S.Q.; Xiang, A.L.; Che, L.L.; Chen, S.; Li, H.; Song, J.B.; Yang, Z.M. A set of miRNAs from Brassica napus in response to sulphate deficiency and cadmium stress. Plant Biotechnol. J. 2010, 8, 887–899. [Google Scholar] [CrossRef] [PubMed]
- Jian, H.; Yang, B.; Zhang, A.; Ma, J.; Ding, Y.; Chen, Z.; Li, J.; Xu, X.; Liu, L. Genome-wide identification of microRNAs in response to cadmium stress in oilseed rape (Brassica napus L.) using high-throughput sequencing. Int. J. Mol. Sci. 2018, 19, 1431. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fu, Y.; Mason, A.S.; Zhang, Y.; Lin, B.; Xiao, M.; Fu, D.; Yu, H. MicroRNA-mRNA expression profiles and their potential role in cadmium stress response in Brassica napus. BMC Plant Biol. 2019, 19, 570. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Z.S.; Song, J.B.; Yang, Z.M. Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium. J. Exp. Bot. 2012, 63, 4597–4613. [Google Scholar] [CrossRef] [Green Version]
- Meng, J.G.; Zhang, X.D.; Tan, S.K.; Zhao, K.X.; Yang, Z.M. Genome-wide identification of Cd-responsive NRAMP transporter genes and analyzing expression of NRAMP 1 mediated by miR167 in Brassica napus. Biometals 2017, 30, 917–931. [Google Scholar] [CrossRef]
- Zhang, L.W.; Song, J.B.; Shu, X.X.; Zhang, Y.; Yang, Z.M. miR395 is involved in detoxification of cadmium in Brassica napus. J. Hazard Mater. 2013, 250–251, 204–211. [Google Scholar] [CrossRef]
- Zhang, X.D.; Sun, J.Y.; You, Y.Y.; Song, J.B.; Yang, Z.M. Identification of Cd-responsive RNA helicase genes and expression of a putative BnRH 24 mediated by miR158 in canola (Brassica napus). Ecotoxicol. Environ. Saf. 2018, 157, 159–168. [Google Scholar] [CrossRef]
- He, X.; Zhang, H.; Ye, X.; Hong, J.; Ding, G. Nitrogen assimilation related genes in Brassica napus: Systematic characterization and expression analysis identified hub genes in multiple nutrient stress responses. Plants 2021, 10, 2160. [Google Scholar] [CrossRef]
- Buhtz, A.; Springer, F.; Chappell, L.; Baulcombe, D.C.; Kehr, J. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J. 2008, 53, 739–749. [Google Scholar] [CrossRef]
- Pant, B.D.; Buhtz, A.; Kehr, J.; Scheible, W.R. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 2008, 53, 731–738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buhtz, A.; Pieritz, J.; Springer, F.; Kehr, J. Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol. 2010, 10, 64. [Google Scholar] [CrossRef] [PubMed]
- Pant, B.D.; Musialak-Lange, M.; Nuc, P.; May, P.; Buhtz, A.; Kehr, J.; Walther, D.; Scheible, W.R. Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol. 2009, 150, 1541–1555. [Google Scholar] [CrossRef] [Green Version]
- Hua, Y.P.; Zhou, T.; Huang, J.Y.; Yue, C.P.; Song, H.X.; Guan, C.Y.; Zhang, Z.H. Genome-wide differential DNA methylation and miRNA expression profiling reveals epigenetic regulatory mechanisms underlying nitrogen-limitation-triggered adaptation and use efficiency enhancement in allotetraploid rapeseed. Int. J. Mol. Sci. 2020, 21, 8453. [Google Scholar] [CrossRef]
- Shen, D.; Suhrkamp, I.; Wang, Y.; Liu, S.; Menkhaus, J.; Verreet, J.A.; Fan, L.; Cai, D. Identification and characterization of microRNAs in oilseed rape (Brassica napus) responsive to infection with the pathogenic fungus Verticillium longisporum using Brassica AA (Brassica rapa) and CC (Brassica oleracea) as reference genomes. New Phytol. 2014, 204, 577–594. [Google Scholar] [CrossRef] [PubMed]
- Cao, J.Y.; Xu, Y.P.; Zhao, L.; Li, S.S.; Cai, X.Z. Tight regulation of the interaction between Brassica napus and Sclerotinia sclerotiorum at the microRNA level. Plant Mol. Biol. 2016, 92, 39–55. [Google Scholar] [CrossRef]
- Jian, H.; Ma, J.; Wei, L.; Liu, P.; Zhang, A.; Yang, B.; Li, J.; Xu, X.; Liu, L. Integrated mRNA, sRNA, and degradome sequencing reveal oilseed rape complex responses to Sclerotinia sclerotiorum (Lib.) infection. Sci. Rep. 2018, 8, 10987. [Google Scholar] [CrossRef] [Green Version]
- Regmi, R.; Newman, T.E.; Kamphuis, L.G.; Derbyshire, M.C. Identification of B. napus small RNAs responsive to infection by a necrotrophic pathogen. BMC Plant Biol. 2021, 21, 366. [Google Scholar] [CrossRef]
- Verma, S.S.; Rahman, M.H.; Deyholos, M.K.; Basu, U.; Kav, N.N. Differential expression of miRNAs in Brassica napus root following infection with Plasmodiophora brassicae. PLoS ONE 2014, 9, e86648. [Google Scholar] [CrossRef]
- Depotter, J.R.L.; Deketelaere, S.; Inderbitzin, P.; Tiedemann, A.V.; Höfte, M.; Subbarao, K.V.; Wood, T.A.; Thomma, B.P.H.J. Verticillium longisporum, the invisible threat to oilseed rape and other brassicaceous plant hosts. Mol. Plant Pathol. 2016, 17, 1004–1016. [Google Scholar] [CrossRef] [Green Version]
- Jian, W.A.; Sy, A.; Li, L.A.; Dl, A.; Sr, A.; Wz, A.; Wm, A.; Pc, A.; Qs, B.; Yf, B. Host-induced gene silencing of multiple pathogenic factors of Sclerotinia sclerotiorum confers resistance to sclerotinia rot in Brassica napus. Crop J. 2021, 10, 661–671. [Google Scholar]
- Navarro, L.; Dunoyer, P.; Jay, F.; Arnold, B.; Dharmasiri, N.; Estelle, M.; Voinnet, O.; Jones, J.D. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312, 436–439. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chalhoub, B.; Denoeud, F.; Liu, S.; Parkin, I.A.P.; Tang, H.; Wang, X.; Chiquet, J.; Belcram, H.; Tong, C.; Samans, B.; et al. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 2014, 345, 950–953. [Google Scholar] [CrossRef] [PubMed]
- Dai, X.; Zhuang, Z.; Zhao, P.X. psRNATarget: A plant small RNA target analysis server (2017 release). Nucleic Acids Res. 2018, 46, 49–54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, C.; Liu, C.; Jiang, A.; Zhao, Q.; Zhang, Y.; Hu, W. miRNA and degradome sequencing identify miRNAs and their target genes involved in the browning inhibition of fresh-cut apples by hydrogen sulfide. J. Agric. Food Chem. 2020, 68, 8462–8470. [Google Scholar] [CrossRef]
- Kunert, K.J.; Vorster, B.J.; Fenta, B.A.; Kibido, T.; Dionisio, G.; Foyer, C.H. Drought stress responses in soybean roots and nodules. Front. Plant Sci. 2016, 7, 1015. [Google Scholar] [CrossRef] [Green Version]
- Zilli, J.É.; Pacheco, R.S.; Gianluppi, V.; Smiderle, O.J.; Urquiaga, S.; Hungria, M. Biological N2 fixation and yield performance of soybean inoculated with Bradyrhizobium. Nutr. Cycl. Agroecosys. 2021, 119, 323–336. [Google Scholar] [CrossRef]
- Ngalimat, M.S.; Mohd Hata, E.; Zulperi, D.; Ismail, S.I.; Ismail, M.R.; Mohd Zainudin, N.A.I.; Saidi, N.B.; Yusof, M.T. Plant growth-promoting bacteria as an emerging tool to manage bacterial rice pathogens. Microorganisms 2021, 9, 682. [Google Scholar] [CrossRef]
- Mamet, S.D.; Helgason, B.L.; Lamb, E.G.; McGillivray, A.; Stanley, K.G.; Robinson, S.J.; Aziz, S.U.; Vail, S.; Siciliano, S.D. Phenology-dependent root bacteria enhance yield of Brassica napus. Soil. Biol. Biochem. 2022, 166, 108468. [Google Scholar] [CrossRef]
- Dai, C.; Li, Y.; Li, L.; Du, Z.; Lin, S.; Tian, X.; Li, S.; Yang, B.; Yao, W.; Wang, J.; et al. An efficient agrobacterium-mediated transformation method using hypocotyl as explants for Brassica napus. Mol. Breed. 2020, 40, 96. [Google Scholar] [CrossRef]
- Li, F.; Wang, W.; Zhao, N.; Xiao, B.; Cao, P.; Wu, X.; Ye, C.; Shen, E.; Qiu, J.; Zhu, Q.H.; et al. Regulation of nicotine biosynthesis by an endogenous target mimicry of microRNA in tobacco. Plant Physiol. 2015, 169, 1062–1071. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.; Zhang, J.; Yan, J.; Gou, F.; Mao, Y.; Tang, G.; Botella, J.R.; Zhu, J.K. Short tandem target mimic rice lines uncover functions of miRNAs in regulating important agronomic traits. Proc. Natl. Acad. Sci. USA 2017, 114, 5277–5282. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Franco-Zorrilla, J.M.; Valli, A.; Todesco, M.; Mateos, I.; Puga, M.I.; Rubio-Somoza, I.; Leyva, A.; Weigel, D.; García, J.A.; Paz-Ares, J. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 2007, 39, 1033–1037. [Google Scholar] [CrossRef] [PubMed]
- Tang, G.; Yan, J.; Gu, Y.; Qiao, M.; Fan, R.; Mao, Y.; Tang, X. Construction of short tandem target mimic (STTM) to block the functions of plant and animal microRNAs. Methods 2012, 58, 118–125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gupta, S.K.; Vishwakarma, A.; Kenea, H.D.; Galsurker, O.; Cohen, H.; Aharoni, A.; Arazi, T. CRISPR/Cas9 mutants of tomato microRNA164 genes uncover their functional specialization in development. Plant Physiol. 2021, 187, 1636–1652. [Google Scholar] [CrossRef]
- Lin, Y.; Zhu, Y.; Cui, Y.; Chen, R.; Chen, Z.; Li, G.; Fan, M.; Chen, J.; Li, Y.; Guo, X.; et al. Derepression of specific miRNA-target genes in rice using CRISPR/Cas9. J. Exp. Bot. 2021, 72, 7067–7077. [Google Scholar] [CrossRef] [PubMed]
- Zheng, M.; Zhang, L.; Tang, M.; Liu, J.; Liu, H.; Yang, H.; Fan, S.; Terzaghi, W.; Wang, H.; Hua, W. Knockout of two BnaMAX1 homologs by CRISPR/Cas9-targeted mutagenesis improves plant architecture and increases yield in rapeseed (Brassica napus L.). Plant Biotechnol. J. 2020, 18, 644–654. [Google Scholar] [CrossRef] [Green Version]
- Fan, S.; Zhang, L.; Tang, M.; Cai, Y.; Liu, J.; Liu, H.; Liu, J.; Terzaghi, W.; Wang, H.; Hua, W.; et al. CRISPR/Cas9-targeted mutagenesis of the BnaA03.BP gene confers semi-dwarf and compact architecture to rapeseed (Brassica napus L.). Plant Biotechnol. J. 2021, 19, 2383–2385. [Google Scholar] [CrossRef]
- Zaman, Q.U.; Wen, C.; Yuqin, S.; Mengyu, H.; Desheng, M.; Jacqueline, B.; Baohong, Z.; Chao, L.; Qiong, H. Characterization of SHATTERPROOF homoeologs and CRISPR-Cas9-mediated genome editing enhances pod-shattering resistance in Brassica napus L. Crispr J. 2021, 4, 360–370. [Google Scholar] [CrossRef]
- Zaman, Q.U.; Chu, W.; Hao, M.; Shi, Y.; Sun, M.; Sang, S.F.; Mei, D.; Cheng, H.; Liu, J.; Li, C.; et al. CRISPR/Cas9-mediated multiplex genome editing of JAGGED Gene in Brassica napus L. Biomolecules 2019, 9, 725. [Google Scholar] [CrossRef] [Green Version]
- Khan, M.H.U.; Hu, L.; Zhu, M.; Zhai, Y.; Khan, S.U.; Ahmar, S.; Amoo, O.; Zhang, K.; Fan, C.; Zhou, Y. Targeted mutagenesis of EOD3 gene in Brassica napus L. regulates seed production. J. Cell. Physiol. 2021, 236, 1996–2007. [Google Scholar] [CrossRef] [PubMed]
- Xie, T.; Chen, X.; Guo, T.; Rong, H.; Chen, Z.; Sun, Q.; Batley, J.; Jiang, J.; Wang, Y. Targeted knockout of BnTT2 Homologues for yellow-seeded Brassica napus with reduced flavonoids and improved fatty acid composition. J. Agric. Food Chem. 2020, 68, 5676–5690. [Google Scholar] [CrossRef] [PubMed]
- Raza, A.; Razzaq, A.; Mehmood, S.S.; Hussain, M.A.; Wei, S.; He, H.; Zaman, Q.U.; Xuekun, Z.; Hasanuzzaman, M. Omics: The way forward to enhance abiotic stress tolerance in Brassica napus L. GM Crops Food. 2021, 12, 251–281. [Google Scholar] [CrossRef] [PubMed]
Functions | MicroRNAs | References |
---|---|---|
Branch angle regulation | Multiple miRNAs | [90,91] |
Flower development | miR172 | [92] |
Male sterility | miR159 | [93] |
Silique development | miR160, miR2111, miR399, miR827, and miR408 | [95] |
Thickness of pod canopy | miR159, miR6029, and miR827 | [96] |
Seed development | Multiple miRNAs | [94,97,100] |
Fatty acid and content | Multiple miRNAs | [98,99,101,102] |
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Li, J.; Li, Y.; Wang, R.; Fu, J.; Zhou, X.; Fang, Y.; Wang, Y.; Liu, Y. Multiple Functions of MiRNAs in Brassica napus L. Life 2022, 12, 1811. https://doi.org/10.3390/life12111811
Li J, Li Y, Wang R, Fu J, Zhou X, Fang Y, Wang Y, Liu Y. Multiple Functions of MiRNAs in Brassica napus L. Life. 2022; 12(11):1811. https://doi.org/10.3390/life12111811
Chicago/Turabian StyleLi, Jian, Yangyang Li, Rongyuan Wang, Jiangyan Fu, Xinxing Zhou, Yujie Fang, Youping Wang, and Yaju Liu. 2022. "Multiple Functions of MiRNAs in Brassica napus L." Life 12, no. 11: 1811. https://doi.org/10.3390/life12111811