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MIR159 regulates multiple aspects of stamen and carpel development and requires dissection and delimitation of differential downstream regulatory network for manipulating fertility traits

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Abstract

Unravelling genetic networks regulating developmental programs are key to devising and implementing genomics assisted trait modification strategies. It is crucial to understand the role of small RNAs, and the basis of their ability to modify traits. MIR159 has been previously reported to cause defects in anther development in Arabidopsis; however, the complete spectrum and basis of the defects remained unclear. The present study was therefore undertaken to comprehensively investigate the role of miR159 from Brassica juncea in modulating vegetative and reproductive traits. Owing to the polyploid nature of Brassica, paralogous and homeologous copies of MIR159A, MIR159B, and, MIR159C were identified and analysis of the precursor uncovered extensive structural and sequence variation. The MIR159 locus with mature miR159 with perfect target complimentarily with MYB65, was cloned from Brassica juncea var. Varuna for functional characterization by generating constitutively over-expressing lines in Arabidopsis thaliana Col-0. Apart from statistically significant difference in multiple vegetative traits, drastic differences were observed in stamen and pistil. Over-expression of miR159a led to shortening of filament length and loss of tetradynamous condition. Anthers were apiculate, with improper lobe formation, and unsynchronized cellular growth between connective tissue and another lobe development. Analysis revealed arrested meiosis/cytokinesis in microspores, and altered lignin deposition pattern in endothecial walls thus affecting anther dehiscence. In the gynoecium, flaccid, dry stigmatic papillae, and large embryo sac in the female gametophyte was observed. Over-expression of miR159a thus severely affected pollination and seed-set. Analysis of the transcriptome data revealed components of regulatory networks of anther and carpel developmental pathway, and lignin metabolism that are affected. Expression analysis allowed us to position the miR159a-MYB65 module in the genetic network of stamen development, involved in pollen-grain maturation; in GA-mediated regulation of stamen development, and in lignin metabolism. The study, on one hand indicates role of miR159a-MYB65 in regulating multiple aspects of reproductive organ development that can be manipulated for trait modification, but also raises several unaddressed questions such as relationship between miR159a and male-meiosis, miR159a and filament elongation for future investigations.

Accession numbers: KC204951-KC204960.

Project number PRJNA1035268.

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References

  • Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131(14):3357–3365

    CAS  PubMed  Google Scholar 

  • Alexander MP (1969) Differential staining of aborted and non-aborted pollen. Biot Histochem 44:117–122

    CAS  Google Scholar 

  • Allen RS, Li J, Stahle MI, Dubroué A, Gubler F, Millar AA (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis MIR159 family. Proc Natl Acad Sci USA 104(41):16371–16376

    CAS  PubMed  PubMed Central  Google Scholar 

  • Allen RS, Li J, Alonso-Peral MM, White RG, Gubler F, Millar AA (2010) MIR159 regulation of most conserved targets in Arabidopsis has negligible phenotypic effects. Silence 1(1):18

    PubMed  PubMed Central  Google Scholar 

  • Alonso-Peral MM, Li J, Li Y, Allen RS, Schnippenkoetter W, Ohms S, White RG, Millar AA (2010) The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol 154(2):757–771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Alvarez-Buylla ER, Benítez M, Corvera-Poiré A, Cador ÁC, de Folter S, de Buen AG, Piñeyro-Nelson A (2010) Flower development. The Arabidopsis Book 8:e0127

    PubMed  PubMed Central  Google Scholar 

  • Anand S, Lal M, Das S (2019) Comparative genomics reveals origin of MIR159A–MIR159B paralogy, and complexities of PTGS interaction between miR159 and target GA-MYBs in Brassicaceae. Mole Genet Genom 294:693–714

    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(5):1453–1472

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhardwaj E, Lal M, Anand S, Das S (2020) Independent recurrent evolution of MICRORNA genes converging onto similar non-canonical organisation across green plant lineages is driven by local and segmental duplication events in species, family and lineages. Plant Sci 301:110661

    CAS  PubMed  Google Scholar 

  • Blázquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404(6780):889

    PubMed  Google Scholar 

  • Boavida LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52(3):570–582

    CAS  PubMed  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1(1):37–52

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bray N, Dubchak I, Pachter L (2003) AVID: a global alignment program. Genome Res 13:97

    CAS  PubMed  PubMed Central  Google Scholar 

  • Browse J, Wallis JG (2019) Arabidopsis flowers unlocked the mechanism of jasmonate signaling. Plants 8(8):285

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cecchetti V, Altamura MM, Brunetti P, Petrocelli V, Falasca G, Ljung K, Cardarelli M (2013) Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. Plant J 74(3):411–422

    CAS  PubMed  Google Scholar 

  • Cecchetti V, Celebrin D, Napoli N, Ghelli R, Brunetti P, Costantino P, Cardarelli M (2017) An auxin maximum in the middle layer controls stamen development and pollen maturation in Arabidopsis. New Phytol 213(3):1194–1207

    CAS  PubMed  Google Scholar 

  • Chahtane H, Vachon G, Le Masson M, Thévenon E, Périgon S, Mihajlovic N, Kalinina A, Michard R, Moyroud E, Monniaux M, Sayou C (2013) A variant of LEAFY reveals its capacity to stimulate meristem development by inducing RAX1. Plant J 74(4):678–689

    CAS  PubMed  Google Scholar 

  • Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5(3):e1000440

    PubMed  PubMed Central  Google Scholar 

  • Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 2005 Nov 27;33(20):e179. https://doi.org/10.1093/nar/gni178

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    CAS  PubMed  Google Scholar 

  • Cominelli E, Tonelli C (2009) A new role for plant R2R3-MYB transcription factors in cell cycle regulation. Cell Res 19(11):1231–1232

    PubMed  Google Scholar 

  • Couronne O, Poliakov A, Bray N, Ishkhanov T, Ryaboy D, Rubin E, Pachter L, Dubchak I (2003) Strategies and tools for whole-genome alignments. Genome Res 13(1):73–80

    CAS  PubMed  PubMed Central  Google Scholar 

  • Csukasi F, Donaire L, Casañal A, Martínez-Priego L, Botella MA, Medina-Escobar N et al (2012) Two strawberry miR159 family members display developmental-specific expression patterns in the fruit receptacle and cooperatively regulate Fa-GAMYB. New Phytol 195(1):47–57

    CAS  PubMed  Google Scholar 

  • Dhaka N, Sharma R (2021) MicroRNA-mediated regulation of agronomically important seed traits: a treasure trove with shades of grey! Crit Rev Biotechnol 41(4):594–608

    CAS  PubMed  Google Scholar 

  • Dhakate P, Shivaraj SM, Singh A (2014) Design of artificial miRNA for redundant silencing of Brassica SHP1 and SHP2: transient assay-based validation of transcript cleavage from polyploid Brassicas. Acta Physiol Plant 36(8):2125–2135

    CAS  Google Scholar 

  • Ding N, Zhang B (2023) microRNA production in Arabidopsis. Front Plant Sci 14:1096772

    PubMed  PubMed Central  Google Scholar 

  • Ditt RF, Nester EW, Comai L (2001) Plant gene expression response to Agrobacterium tumefaciens. Proc Natl Acad Sci USA 98(19):10954–10959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong Q, Hu B, Zhang C (2022) microRNAs and their roles in plant development. Front Plant Sci 13:824240

    PubMed  PubMed Central  Google Scholar 

  • Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55(1):123–142

    Google Scholar 

  • Feng B, Lu D, Ma X, Peng Y, Sun Y, Ning G, Ma H (2012) Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J 72:612–624

    CAS  PubMed  Google Scholar 

  • Franks RG (2016) Histological analysis of the Arabidopsis gynoecium and ovules using chloral hydrate clearing and differential interference contrast light microscopy. Methods Mol Biol 1457:1–7. https://doi.org/10.1007/978-1-4939-3795-0_1

  • Garighan J, Dvorak E, Estevan J, Loridon K, Huettel B, Sarah G, Andrés F (2021) The identification of small RNAs differentially expressed in apple buds reveals a potential role of the Mir159-MYB regulatory module during dormancy. Plants 10(12):2665

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gocal GF, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP et al (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127(4):1682–1693

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5(10):1217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57(11):876–891

    PubMed  PubMed Central  Google Scholar 

  • Gu JN, Zhu J, Yu Y, Teng XD, Lou Y, Xu XF, Yang ZN (2014) DYT1 directly regulates the expression of TDF1 for tapetum development and pollen wall formation in Arabidopsis. Plant J 80(6):1005–1013

    CAS  PubMed  Google Scholar 

  • Gubler F, Jacobsen JV (1992) Gibberellin-responsive elements in the promoter of a barley high-pI α-amylase gene. Plant Cell 4:1435–1441

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell 7(11):1879–1891

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gubler F, Raventos D, Keys M, Watts R, Mundy J, Jacobsen JV (1999) Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J 17(1):1–9

    CAS  PubMed  Google Scholar 

  • Guo C, Xu Y, Shi M, Lai Y, Wu X, Wang H et al (2017) Repression of miR156 by miR159 regulates the timing of the juvenile-to-adult transition in Arabidopsis. Plant Cell 29(6):1293–1304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Z, Shen X, Xiang X, Cao J (2019) Evolution of MIR159/319 genes in Brassica campestris and their function in pollen development. Plant Mol Biol 101:537–550

    CAS  PubMed  Google Scholar 

  • Huang H, Gao H, Liu B, Qi T, Tong J, Xiao L et al (2017) Arabidopsis MYB24 regulates jasmonate-mediated stamen development. Front Plant Sci 8:1525

    PubMed  PubMed Central  Google Scholar 

  • Jain A, Das S (2016) Synteny and comparative analysis of miRNA retention, conservation, and structure across Brassicaceae reveals lineage- and sub-genome-specific changes. Funct Integr Genom 16:253–268

    CAS  Google Scholar 

  • Jain A, Anand S, Singh NK, Das S (2018) Sequence and functional characterization of mirna164 promoters from Brassica shows copy number dependent regulatory diversification among homeologs. Funct Integr Genom 18(4):369–383

    CAS  Google Scholar 

  • Jiang J, Lv M, Liang Y, Ma Z, Cao J (2014) Identification of novel and conserved miRNAs involved in pollen development in Brassica campestris ssp. chinensis by high-throughput sequencing and degradome analysis. BMC Genom 15(1):146

    Google Scholar 

  • Joshi G, Chauhan C, Das S (2021) Sequence and functional analysis of MIR319 promoter homologs from Brassica juncea reveals regulatory diversification and altered expression under stress. Mole Genet Genom 296:731–749

    CAS  Google Scholar 

  • Kang L, Qian L, Zheng M et al (2021) Genomic insights into the origin, domestication and diversification of Brassica juncea. Nat Genet 53:1392–1402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lal M, Bhardwaj E, Chahar N, Yadav S, Das S (2022) Comprehensive analysis of 1R-and 2R-MYBs reveals novel genic and protein features, complex organisation, selective expansion and insights into evolutionary tendencies. Funct Integr Genom 22(3):371–405

    CAS  Google Scholar 

  • Latchman DS (1997) Transcription factors: an overview. Int J Biochem Cell Biol 29(12):1305–1312

    CAS  PubMed  Google Scholar 

  • Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1(1): e6. 109–118

  • Li J, Reichel M, Millar AA (2014) Determinants beyond both complementarity and cleavage govern microR159 efficacy in Arabidopsis. PLoS Genet 10(3):e1004232

    PubMed  PubMed Central  Google Scholar 

  • Li C, Ng CKY, Fan LM (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot 114:80–91

    CAS  Google Scholar 

  • Li Y, Alonso-Peral M, Wong G, Wang MB, Millar AA (2016) Ubiquitous miR159 repression of MYB33/65 in Arabidopsis rosettes is robust and is not perturbed by a wide range of stresses. BMC Plant Biol 16(1):179

    PubMed  PubMed Central  Google Scholar 

  • Li J, Han G, Sun C, Sui N (2019) Research advances of MYB transcription factors in plant stress resistance and breeding. Plant Sig Behav 14(8):1613131

    Google Scholar 

  • Liang Y, Tan ZM, Zhu L, Niu QK, Zhou JJ, Li M, Ye D (2013) MYB97, MYB101 and MYB120 function as male factors that control pollen tube-synergid interaction in Arabidopsis thaliana fertilization. PLoS Genet 9(11):e1003933

    PubMed  PubMed Central  Google Scholar 

  • Liu B, De Storme N, Geelen D (2017) Gibberellin induces diploid pollen formation by interfering with meiotic cytokinesis. Plant Physiol 173(1):338–353

    CAS  PubMed  Google Scholar 

  • Luo Y, Guo Z, Li L (2013) Evolutionary conservation of microRNA regulatory programs in plant flower development. Dev Biol 380(2):133–144

    CAS  PubMed  Google Scholar 

  • Maier A, Schrader A, Kokkelink L, Falke C, Welter B, Iniesto E et al (2013) Light and the E3 ubiquitin ligase COP 1/SPA control the protein stability of the MYB transcription factors PAP 1 and PAP 2 involved in anthocyanin accumulation in Arabidopsis. Plant J 74(4):638–651

    CAS  PubMed  Google Scholar 

  • Martin RC, Asahina M, Liu PP, Kristof JR, Coppersmith JL, Pluskota WE, Kumar MA (2010) The microRNA156 and microRNA172 gene regulation cascades at post-germinative stages in Arabidopsis. Seed Sci Res 20(2):79–87

    CAS  Google Scholar 

  • Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17(3):705–721

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mu RL, Cao YR, Liu YF, Lei G, Zou HF, Liao Y et al (2009) An R2R3-type transcription factor gene AtMYB59 regulates root growth and cell cycle progression in Arabidopsis. Cell Res 19(11):1291–1304

    CAS  PubMed  Google Scholar 

  • Murray F, Kalla R, Jacobsen J, Gubler F (2003) A role for HvGAMYB in anther development. Plant J 33(3):481–491

    CAS  PubMed  Google Scholar 

  • Naqvi AR, Haq QM, Mukherjee SK (2010) MicroRNA profiling of tomato leaf curl new Delhi virus (tolcndv) infected tomato leaves indicates that deregulation of mir159/319 and mir172 might be linked with leaf curl disease. Virol J 7(1):281

    PubMed  PubMed Central  Google Scholar 

  • Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Carrington JC (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13(1):115–125

    CAS  PubMed  Google Scholar 

  • Perumal S, Koh CS, Jin L, Buchwaldt M, Higgins EE, Zheng C, Sankoff D, Robinson SJ, Kagale S, Navabi ZK, Tang L, Horner KN, He Z, Bancroft I, Chalhoub B, Sharpe AG, Parkin IAP (2020) A high-contiguity Brassica nigra genome localizes active centromeres and defines the ancestral Brassica genome. Nat Plants 6(8):929–941

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson R, Slovin JP, Chen C (2010) A simplified method for differential staining of aborted and non-aborted pollen grains. Int J Plant Biol 1(2):e13

    Google Scholar 

  • Phan HA, Iacuone S, Li SF, Parish RW (2011) The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana. Plant Cell 23(6):2209–2224

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press 198:322

    Google Scholar 

  • Salinas-Grenet H, Herrera-Vásquez A, Parra S, Cortez A, Gutiérrez L, Pollmann S, Blanco-Herrera F (2018) Modulation of auxin levels in pollen grains affects stamen development and anther dehiscence in Arabidopsis. Int J Mol Sci 19(9):2480

    PubMed  PubMed Central  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schommer C, Bresso EG, Spinelli SV, Palatnik JF (2012) Role of microRNA miR319 in plant development. MicroRNAs in plant development and stress responses. Springer, Berlin, Heidelberg, pp 29–47

    Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527

    CAS  PubMed  Google Scholar 

  • Shivanna KR, Rangaswamy NS (1992) Tests for pollen viability. In: Shivanna KR, Rangaswamy NS (eds) Pollen biology: a laboratory manual. Springer, Berlin, Heidelberg, pp 33–38

  • Sirohi G, Kusumanjali K, Kumar R, Jain A, Srivastava PS, Das S (2018) Synteny analysis and functional characterization of miR165a from Brassica species. Acta Physiol Plant 40:16

    Google Scholar 

  • Skriver K, Olsen FL, Rogers JC, Mundy J (1991) cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc Natl Acad Sci USA 88:7266–7270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2(8):755–767

    CAS  PubMed  PubMed Central  Google Scholar 

  • Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genom Biol 7(Suppl 1):10.1-10.12

    Google Scholar 

  • Song QX, Liu YF, Hu XY, Zhang WK, Ma B, Chen SY, Zhang JS (2011) Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol 11(1):5

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song S, Qi T, Huang H, Xie D (2013) Regulation of stamen development by coordinated actions of jasmonate, auxin, and gibberellin in Arabidopsis. Mol Plant 6(4):1065–1073

    CAS  PubMed  Google Scholar 

  • Song X, Li Y, Cao X, Qi Y (2019) MicroRNAs and their regulatory roles in plant-environment interactions. Annu Rev Plant Biol 70:489–525

    CAS  PubMed  Google Scholar 

  • Tian T, Liu Y, Yan H, You Q, Yi X, Du Z et al (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucl Acids Res 45(W1):W122–W129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R et al (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47(3):427–444

    CAS  PubMed  Google Scholar 

  • Tsukaya H (2008) Controlling size in multicellular organs: focus on the leaf. PLoS Biol 6(7):e174

    PubMed  PubMed Central  Google Scholar 

  • Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) A highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3(1):1–12

    Google Scholar 

  • Wang S, Chen JG (2014) Regulation of cell fate determination by single-repeat R3 MYB transcription factors in Arabidopsis. Front Plant Sci 5:133

    PubMed  PubMed Central  Google Scholar 

  • Warthmann N, Das S, Lanz C, Weigel D (2008) Comparative analysis of miR319A locus in Arabidopsis and related Brassicaceae. Mole Biol Evol 25:892–902

    CAS  Google Scholar 

  • Weigel D, Glazebrook J (2002) Arabidopsis: A laboratory manual. CSHL press

  • Wilson ZA, Song J, Taylor B, Yang C (2011) The final split: the regulation of anther dehiscence. J Exp Bot 62(5):1633–1649

    CAS  PubMed  Google Scholar 

  • Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133(21):4211–4218

    CAS  PubMed  Google Scholar 

  • Xue T, Liu Z, Dai X, Xiang F (2017) Primary root growth in Arabidopsis thaliana is inhibited by the miR159 mediated repression of MYB33, MYB65 and MYB101. Plant Sci 262:182–189

    CAS  PubMed  Google Scholar 

  • Yan H, Pei X, Zhang H, Li X, Zhang X, Zhao M et al (2021) MYB-mediated regulation of anthocyanin biosynthesis. Int J Mol Sci 22(6):3103

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang T, Xue L, An L (2007) Functional diversity of miRNA in plants. Plant Sci 172(3):423–432

    CAS  Google Scholar 

  • Yang J, Liu X, Xu B, Zhao N, Yang X, Zhang M (2013) Identification of miRNAs and their targets using high-throughput sequencing and degradome analysis in cytoplasmic male-sterile and its maintainer fertile lines of Brassica juncea. BMC Genom 14(1):9

    Google Scholar 

  • Yang J, Wang J, Li Z, Li X, He Z, Zhang L, Zhang M (2021) Genomic signatures of vegetable and oilseed allopolyploid Brassica juncea and genetic loci controlling the accumulation of glucosinolates. Plant Biotech J 19(12):2619–2628

    CAS  Google Scholar 

  • Yao X, Chen J, Zhou J, Yu H, Ge C, Zhang M, Gao X, Dai X, Yang ZN, Zhao Y (2019) An essential role for miRNA167 in maternal control of embryonic and seed development. Plant Physiol 180(1):453–464

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhan J, Meyers BC (2023) Plant small RNAs: their biogenesis, regulatory roles, and functions. Annu Rev Plant Biol 74:21–51

    CAS  PubMed  Google Scholar 

  • Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289(1):3–16

    CAS  PubMed  Google Scholar 

  • Zhang Z, Guo J, Cai X, Li Y, Xi X, Lin R, Wu J (2021) Improved reference genome annotation of Brassica rapa by PacBio RNA sequencing. bioRxiv 2021–11

  • Zhang Z, Guo J, Cai X, Li Y, Xi X, Lin R, Liang J, Wang X, Wu J (2022) Improved reference genome annotation of Brassica rapa by Pacific biosciences RNA sequencing. Front Plant Sci 13:841618

    PubMed  PubMed Central  Google Scholar 

  • Zhao P, Wang F, Deng Y, Zhong F, Tian P, Lin D, Huang T (2022) Sly-miR159 regulates fruit morphology by modulating GA biosynthesis in tomato. Plant Biotech J 20(5):833–845

    CAS  Google Scholar 

  • Zheng Z, Reichel M, Deveson I, Wong G, Li J, Millar AA (2017) Target RNA secondary structure is a major determinant of miR159 efficacy. Plant Physiol 174(3):1764–1778

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Z, Wang N, Jalajakumari M, Blackman L, Shen E, Verma S, Millar AA (2020) miR159 represses a constitutive pathogen defense response in tobacco. Plant Physiol 182(4):2182–2198

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acids Res 31(13):3406–3415

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The study was initiated as a part of a network program by DBT under the coordinatorship of Prof. Sudhir Sopory (ICGEB), and co-coordinatorship of Prof. Sunil Mukherjee (ICGEB). This research was supported by DBT, Govt. of India Grants BT/PR31101/AGIII/103/1100/2018 and BT/PR628/AGR/36/674/2011 to SD. JRF/SRF from DBT to SA and EB; from UGC to AJ and ML; and, from CSIR to RS, EP and TS is gratefully acknowledged. SD would also like to acknowledge Delhi University for the financial and infrastructural support through IoE Grants. AS would like to acknowledge DBT for financial assistance through DBT Grant BT/PR628/AGR/36/674/2011, and TERI-SAS for infrastructural support.

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  1. Department of Botany, University of Delhi, Delhi, 110 007, India

    Saurabh Anand, Mukund Lal, Ekta Bhardwaj, Richa Shukla, Ekta Pokhriyal, Aditi Jain & Sandip Das

  2. Department of Biotechnology, Jamia Hamdard, Hamdard Nagar, New Delhi, Delhi, 110 062, India

    P. S. Srivastava

  3. TERI School of Advanced Studies, Plot No. 10, Institutional Area, Vasant Kunj, New Delhi, 110 070, India

    Tanu Sri & Anandita Singh

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SD, PSS, AS, and SA designed the study. SA generated transgenic lines, and performed all phenotypic and molecular analysis with the help of of ML and EB; SA and ML generated and analysed transcriptome data with the help of RS and EP; EB, RS and EP generated data on synteny and comparative genomics; AJ and TS validated over-expression in transgenic lines and analysed the data; SA, ML, EB, RS, EP and SD wrote the MS. All authors have read and approve of the manuscripts.

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Correspondence to Sandip Das.

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Anand, S., Lal, M., Bhardwaj, E. et al. MIR159 regulates multiple aspects of stamen and carpel development and requires dissection and delimitation of differential downstream regulatory network for manipulating fertility traits. Physiol Mol Biol Plants 29, 1437–1456 (2023). https://doi.org/10.1007/s12298-023-01377-7

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