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MicroRNA775 Targets a Probable β-(1,3)-Galactosyltransferase to Regulate Growth and Development in Arabidopsis thaliana

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Abstract

MicroRNAs are critical regulators of gene expression in plants and other organisms, and are involved in regulating plethora of developmental processes. Evolutionarily, miRNAs can be ancient and conserved across species or recently evolved and young, which are not conserved across diverse plant groups. MicroRNA775 (miR775) is a non-conserved miRNA identified only in Arabidopsis thaliana (A. thaliana). Here, we investigated the functional significance of miR775 in A. thaliana and observed that miR775 targets a probable β-(1,3)-galactosyltransferase gene at post transcriptional level. Phenotypic analysis of miR775 over-expression lines and the target mutant suggested miR775 regulates rosette size by elongating petiole length and increasing leaf area. Further, the expression of miR775 was found to be up-regulated in response to UV-B and hypoxia. Our results also suggest that miR775 regulated β-(1,3)-galactosyltransferase may involve in regulating the β-(1,3)-galactan content of arabinogalactans. Collectively, our findings establish a role of miR775 in regulating growth and development in A. thaliana.

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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

    Article  CAS  PubMed  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant, Cell Environ 24(12):1337–1344

    Article  CAS  Google Scholar 

  • Basu D, Tian L, Wang W, Bobbs S, Herock H, Travers A, Showalter AM (2015a) A small multigene hydroxyproline-O-galactosyltransferase family functions in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. BMC Plant Biol 15(1):295

    Article  PubMed  PubMed Central  Google Scholar 

  • Basu D, Wang W, Ma S, DeBrosse T, Poirier E, Emch K, Soukup E, Tian L, Showalter AM (2015b) Two hydroxyproline galactosyltransferases, GALT5 and GALT2, function in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. PLoS ONE 10(5):e0125624

    Article  PubMed  PubMed Central  Google Scholar 

  • Bond DM, Wilson IW, Dennis ES, Pogson BJ, Jean Finnegan E (2009) Vernalization insensitive 3 (VIN3) is required for the response of Arabidopsis thaliana seedlings exposed to low oxygen conditions. Plant J 59(4):576–587

    Article  CAS  PubMed  Google Scholar 

  • Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J (2005) Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96(4):647–660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao M, Yin Z, Hao D, Zhang J, Song H, Ning A, Xu X, Yu D (2014) Variation in Rubisco activase (RCAβ) gene promoters and expression in soybean [Glycine max (L.) Merr.]. J Expl Botany 65(1):47–59

    Article  CAS  Google Scholar 

  • Chiou T-J, Aung K, Lin S-I, Wu C-C, Chiang S-F, Su C-l (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18(2):412–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung PJ, Park BS, Wang H, Liu J, Jang I-C, Chua N-H (2016) Light-inducible miR163 targets PXMT1 transcripts to promote seed germination and primary root elongation in Arabidopsis. Plant Physiol 170(3):1772–1782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23(2):431–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:155–159

    Article  Google Scholar 

  • Daudi A, O’Brien JA (2012) Detection of hydrogen peroxide by DAB staining in Arabidopsis leaves. Bio Protoc 2(18):1–4

    Article  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J-F, Guindon S, Lefort V, Lescot M (2008) Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469

    Article  Google Scholar 

  • Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol 105(4):1075–1087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2(2):e219

    Article  PubMed  PubMed Central  Google Scholar 

  • Felippes FF, Weigel D (2009) Triggering the formation of tasiRNAs in Arabidopsis thaliana: the role of microRNA miR173. EMBO Rep 10(3):264–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Mol Plant 9(10):1353–1365

    Article  CAS  PubMed  Google Scholar 

  • Geshi N, Johansen JN, Dilokpimol A, Rolland A, Belcram K, Verger S, Kotake T, Tsumuraya Y, Kaneko S, Tryfona T (2013) A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis. Plant J 76(1):128–137

    CAS  PubMed  Google Scholar 

  • Giuliano G, Pichersky E, Malik V, Timko M, Scolnik P, Cashmore A (1988) An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci 85(19):7089–7093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H-S, Xie Q, Fei J-F, Chua N-H (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17(5):1376–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, Dennis ES, Sauter M, Dolferus R (2010) Arabidopsis RAP2. 2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol 153(2):757–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Ouyang X, Yang P, Lau OS, Li G, Li J, Chen H, Deng XW (2012) Arabidopsis FHY3 and HY5 positively mediate induction of COP1 transcription in response to photomorphogenic UV-B light. Plant Cell 24(11):4590–4606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jefferson R (1989) The GUS reporter gene system. Nature 342(6251):837–838

    Article  CAS  PubMed  Google Scholar 

  • Kitazawa K, Tryfona T, Yoshimi Y, Hayashi Y, Kawauchi S, Antonov L, Tanaka H, Takahashi T, Kaneko S, Dupree P (2013) β-Galactosyl Yariv reagent binds to the β-1, 3-galactan of arabinogalactan proteins. Plant Physiol 161(3):1117–1126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Körner C (2007) The use of ‘altitude’in ecological research. Trends Ecol Evol 22(11):569–574

    Article  PubMed  Google Scholar 

  • Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22(11):3574–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62(6):1046–1057

    CAS  PubMed  Google Scholar 

  • Liang G, Ai Q, Yu D (2015) Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis. Sci Rep 5:11813

    Article  PubMed  PubMed Central  Google Scholar 

  • Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie A (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Prot 1:387–396

    Article  CAS  Google Scholar 

  • Logemann E, Hahlbrock K (2002) Crosstalk among stress responses in plants: pathogen defense overrides UV protection through an inversely regulated ACE/ACE type of light-responsive gene promoter unit. Proc Natl Acad Sci 99(4):2428–2432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu C, Kulkarni K, Souret FF, MuthuValliappan R, Tej SS, Poethig RS, Henderson IR, Jacobsen SE, Wang W, Green PJ (2006) MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res 16(10):1276–1288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Z, Jiang J, Hu Z, Lyu T, Yang Y, Jiang J, Cao J (2017) Over-expression of miR158 causes pollen abortion in Brassica campestris ssp chinensis. Plant Mol Biol 93(3):313–326

    Article  CAS  PubMed  Google Scholar 

  • Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their auxin response factor targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22(4):1104–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra SK, Khan MH, Misra S, Dixit VK, Gupta S, Tiwari S, Gupta SC, Chauhan PS (2020) Drought tolerant Ochrobactrum sp. inoculation performs multiple roles in maintaining the homeostasis in Zea mays L. subjected to deficit water stress. Plant Physiol Biochem 150:1–14

    Article  CAS  PubMed  Google Scholar 

  • Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson IW (2010) Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot 61(1):165–177

    Article  CAS  PubMed  Google Scholar 

  • Montgomery TA, Yoo SJ, Fahlgren N, Gilbert SD, Howell MD, Sullivan CM, Alexander A, Nguyen G, Allen E, Ahn JH (2008) AGO1-miR173 complex initiates phased siRNA formation in plants. Proc Natl Acad Sci 105(51):20055–20062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci 106(52):22534–22539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narciso JO, Zeng W, Ford K, Lampugnani ER, Humphries J, Austarheim I, van de Meene A, Bacic A, Doblin MS (2021) Biochemical and functional characterization of GALT8, an Arabidopsis GT31 β-(1, 3)-galactosyltransferase that influences seedling development. Front Plant Sci 12:886

    Article  Google Scholar 

  • Nibbering P, Castilleux R, Wingsle G, Niittylä T (2021) Golgi-localized GALT7 and GALT8 participate in cellulose biosynthesis. bioRxiv

  • Ogawa-Ohnishi M, Matsubayashi Y (2015) Identification of three potent hydroxyproline O-galactosyltransferases in Arabidopsis. Plant J 81(5):736–746

    Article  CAS  PubMed  Google Scholar 

  • Popper ZA (2011) Extraction and detection of arabinogalactan proteins. In: The Plant Cell Wall. Springer 245–254

  • Qin LX, Chen Y, Zeng W, Li Y, Gao L, Li DD, Bacic A, Xu WL, Li XB (2017) The cotton β-galactosyltransferase 1 (GalT1) that galactosylates arabinogalactan proteins participates in controlling fiber development. Plant J 89(5):957–971

    Article  CAS  PubMed  Google Scholar 

  • Qu Y, Egelund J, Gilson PR, Houghton F, Gleeson PA, Schultz CJ, Bacic A (2008) Identification of a novel group of putative Arabidopsis thaliana β-(1, 3)-galactosyltransferases. Plant Mol Biol 68(1–2):43–59

    Article  CAS  PubMed  Google Scholar 

  • Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20(24):3407–3425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in Plants. Genes Dev 16(13):1616–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat Protoc 3(6):1101

    Article  CAS  PubMed  Google Scholar 

  • Sharma D, Tiwari M, Pandey A, Bhatia C, Sharma A, Trivedi PK (2016) MicroRNA858 is a potential regulator of phenylpropanoid pathway and plant development. Plant Physiol 171(2):944–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Showalter AM, Basu D (2016) Glycosylation of arabinogalactan-proteins essential for development in Arabidopsis. Commun Integr Biol 9(3):e0125624

    Article  Google Scholar 

  • Strasser R, Bondili JS, Vavra U, Schoberer J, Svoboda B, Glössl J, Léonard R, Stadlmann J, Altmann F, Steinkellner H (2007) A unique β1, 3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19(7):2278–2292

    Article  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki T, Narciso JO, Zeng W, van de Meene A, Yasutomi M, Takemura S, Lampugnani ER, Doblin MS, Bacic A, Ishiguro S (2017) KNS4/UPEX1: a type II arabinogalactan β-(1, 3)-galactosyltransferase required for pollen exine development. Plant Physiol 173(1):183–205

    Article  CAS  PubMed  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP (2015) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43(D1):D447–D452

    Article  CAS  PubMed  Google Scholar 

  • Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47(D1):D607–D613

    Article  CAS  PubMed  Google Scholar 

  • Team RC (2017) R: A Language and Environment for Statistical Computing. 887 R Foundation for Statistical Computing, Vienna, Austria. URL https: //www 888

  • Tripathi AM, Singh A, Singh R, Verma AK, Roy S (2019) Modulation of miRNA expression in natural populations of A thaliana along a wide altitudinal gradient of Indian Himalayas. Sci Rep 9(1):1–16

    Article  Google Scholar 

  • Vaucheret H, Vazquez F, Crété P, Bartel DP (2004) The action of argonaute1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18(10):1187–1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velasquez SM, Ricardi MM, Dorosz JG, Fernandez PV, Nadra AD, Pol-Fachin L, Egelund J, Gille S, Harholt J, Ciancia M (2011) O-glycosylated cell wall proteins are essential in root hair growth. Science 332(6036):1401–1403

    Article  CAS  PubMed  Google Scholar 

  • Vergara R, Parada F, Rubio S, Pérez FJ (2012) Hypoxia induces H2O2 production and activates antioxidant defence system in grapevine buds through mediation of H2O2 and ethylene. J Exp Bot 63(11):4123–4131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687

    Article  CAS  PubMed  Google Scholar 

  • Walker JC, Howard EA, Dennis ES, Peacock WJ (1987) DNA sequences required for anaerobic expression of the maize alcohol dehydrogenase 1 gene. Proc Natl Acad Sci 84(19):6624–6628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J-W, Wang L-J, Mao Y-B, Cai W-J, Xue H-W, Chen X-Y (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17(8):2204–2216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willats WG, McCartney L, Knox JP (2001) In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta 213(1):37–44

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539–3547

    Article  CAS  PubMed  Google Scholar 

  • Wu M-F, 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

    Article  CAS  PubMed  Google Scholar 

  • Xie Z, Kasschau KD, Carrington JC (2003) Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr Biol 13(9):784–789

    Article  CAS  PubMed  Google Scholar 

  • Yang C-Y (2014) Ethylene and hydrogen peroxide are involved in hypoxia signaling that modulates AtERF73/HRE1 expression. Plant Signal Behav 9(5):877–885

    Article  Google Scholar 

  • Zhang H, Li L (2013) SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in A rabidopsis. Plant J 74(1):98–109

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Guo Z, Zhuang Y, Suo Y, Du J, Gao Z, Pan J, Li L, Wang T, Xiao L (2021) MicroRNA775 Regulates Intrinsic Leaf Size and Reduces Cell Wall Pectin Levels by Targeting a Galactosyltransferase Gene in Arabidopsis. Plant Cell 9:e226

    Google Scholar 

  • Zhao Y, Lin S, Qiu Z, Cao D, Wen J, Deng X, Wang X, Lin J, Li X (2015) MicroRNA857 is involved in the regulation of secondary growth of vascular tissues in Arabidopsis. Plant Physiol 169(4):2539–2552

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61(15):4157–4168

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge the financial support of Council of Scientific and Industrial Research (CSIR), New Delhi and partly by Department of Biotechnology (DBT), Government of India, New Delhi, India. PM and AKV also acknowledge the University Grant Commission (UGC), New Delhi for providing the fellowship.

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PM, AS, AKV and RS conducted the experiments. SKM conducted GC–MS analysis. PM analysed the results and wrote the manuscript with SR. All authors read and approved the manuscript. SR designed and arranged fund for the experiments.

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Correspondence to Sribash Roy.

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Mishra, P., Singh, A., Verma, A.K. et al. MicroRNA775 Targets a Probable β-(1,3)-Galactosyltransferase to Regulate Growth and Development in Arabidopsis thaliana. J Plant Growth Regul 41, 3271–3284 (2022). https://doi.org/10.1007/s00344-021-10511-2

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