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Genome-wide identification of auxin-responsive microRNAs in the poplar stem

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Abstract

Background

Wood (secondary xylem) of forests is a material of great economic importance. Wood development is strictly controlled by both the phytohormone auxin and microRNAs (miRNAs). Currently, the regulatory mechanisms underlying wood formation by auxin-associated miRNAs remain unclear.

Objective

This report was designed to identify auxin-responsive miRNAs during wood formation.

Methods

Morphological observation of wood development in the poplar stems was performed under the treatment of different concentrations (0 mg/L, CK; 5 mg/L, Low; 10 mg/L, High) of indol-3-butyric acid (IBA). Using a small RNA sequencing strategy, the effect of IBA treatment on miRNAs expression was genome-widely analyzed.

Results

In this study, we found that wood development of poplar was promoted by low concentration of IBA treatment but inhibited by high concentration of IBA treatment. Stringent bioinformatic analysis led to identification of 118 known and 134 novel miRNAs candidates. Sixty-nine unique developmental-related miRNAs, corresponding to 269 target genes, exhibited specific expression patterns in response to auxin, as was consistent with the influence of auxin application on wood formation. Three novel miRNAs had the most number (≥ 9) of target genes, belonging to SPL, GRF and ARF gene families. The evolutionary relationships and tissue expression patterns of 41 SPL, GRF and ARF genes in poplar were thus analyzed. Of them, four representative members and corresponding miRNAs were confirmed using RT-qPCR.

Conclusions

Our results may be helpful for a better understanding of auxin-induced regulation of wood formation in tree species.

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Data archiving statement

The small RNA raw data are available at the Sequence Read Archive under PRJNA850678. Data openly available in a public repository.

References

  • Carrió-Seguí À, Ruiz-Rivero O, Villamayor-Belinchón L, Puig S, Perea-García A, Penarrubia L (2019) The altered expression of microRNA408 influences the Arabidopsis response to iron deficiency. Front Plant Sci 10:324

    PubMed  PubMed Central  Google Scholar 

  • Chai G, Qi G, Cao Y, Wang Z, Yu L, Tang X, Yu Y, Wang D, Kong Y, Zhou G (2014) Poplar PdC3H17 and PdC3H18 are direct targets of PdMYB3 and PdMYB21, and positively regulate secondary wall formation in Arabidopsis and poplar. New Phytol 203(2):520–534

    CAS  PubMed  Google Scholar 

  • Dai Z, Wang J, Yang X, Lu H, Miao X, Shi Z (2018) Modulation of plant architecture by the miR156f-OsSPL7-OsGH3.8 pathway in rice. J Exp Bot 69(21):5117–5130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Q, Zeng J, He X (2014) Deep sequencing on a genome-wide scale reveals diverse stage-specific microRNAs in cambium during dormancy-release induced by chilling in poplar. BMC Plant Biol 14:267

    PubMed  PubMed Central  Google Scholar 

  • Ding Q, Zeng J, He XQ (2016) MiR169 and its target PagHAP2-6 regulated by ABA are involved in poplar cambium dormancy. J Plant Physiol 198:1–9

    CAS  PubMed  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 

  • Du J, Miura E, Robischon M, Martinez C, Groover A (2011) The Populus class III HD ZIP transcription factor popcorona affects cell differentiation during secondary growth of woody stems. PLoS ONE 6(2):e17458

    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, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of miRNA genes. PLoS ONE 2(2):e219

    PubMed  PubMed Central  Google Scholar 

  • Fan D, Li C, Fan C, Hu J, Li J, Yao S, Lu W, Yan Y, Luo K (2020) MicroRNA6443-mediated regulation of FERULATE 5-HYDROXYLASE gene alters lignin composition and enhances saccharification in Populus tomentosa. New Phytol 226(2):410–425

    CAS  PubMed  Google Scholar 

  • Fang L, Wang Y (2021) MicroRNAs in woody plants. Front Plant Sci 12:686831

    PubMed  PubMed Central  Google Scholar 

  • Fu Y, Win P, Zhang H, Li C, Shen Y, He F, Luo K (2019) PtrARF2.1 is involved in regulation of leaf development and lignin biosynthesis in poplar trees. Int J Mol Sci 20(17):4141

    PubMed  PubMed Central  Google Scholar 

  • Hou J, Xu H, Fan D, Ran L, Li J, Wu S, Luo K, He X (2020) MiR319a-targeted PtoTCP20 regulates secondary growth via interactions with PtoWOX4 and PtoWND6 in Populus tomentosa. New Phytol 228(4):1354–1368

    CAS  PubMed  Google Scholar 

  • Jodder J (2020) miRNA-mediated regulation of auxin signaling pathway during plant development and stress responses. J Biosci 45:91

    CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480-484

    CAS  PubMed  Google Scholar 

  • Li M, Yu B (2021) Recent advances in the regulation of plant miRNA biogenesis. RNA Biol 18(12):2087–2096

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52(1):133–146

    CAS  PubMed  Google Scholar 

  • Liu Y, Yan J, Wang K, Li D, Yang R, Luo H, Zhang W (2021) MiR396-GRF module associates with switchgrass biomass yield and feedstock quality. Plant Biotechnol J 19(8):1523–1536

    CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2T-ΔΔC method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Lu S, Li Q, Wei H, Chang M, Tunlaya-Anukit S, Kim H, Liu J, Song J, Sun Y, Yuan L, Yeh T, Peszlen I, Ralph J, Sederoff R, Chiang VL (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci USA 110(26):10848–10853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luo P, Di D, Wu L, Yang J, Lu Y, Shi W (2022) MicroRNAs are involved in regulating plant development and stress response through fine-tuning of TIR1/AFB-dependent auxin signaling. Int J Mol Sci 23(1):510

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER, Sahinalp SC, Unrau PJ (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res 18(4):571–584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Omidbakhshfard MA, Proost S, Fujikura U, Mueller-Roeber B (2015) Growth-regulating factors (GRFs): a small transcription factor family with important functions in plant biology. Mol Plant 8(7):998–1010

    CAS  PubMed  Google Scholar 

  • Puzey JR, Karger A, Axtell M, Kramer EM (2012) Deep annotation of Populus trichocarpa microRNAs from diverse tissue sets. PLoS ONE 7(3):e33034

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qu G, Peng D, Yu Z, Chen X, Cheng X, Yang Y, Ye T, Lv Q, Ji W, Deng X, Zhou B (2021) Advances in the role of auxin for transcriptional regulation of lignin biosynthesis. Funct Plant Biol 48(8):743–754

    CAS  PubMed  Google Scholar 

  • Quan M, Du Q, Xiao L, Lu W, Wang L, Xie J, Song Y, Xu B, Zhang D (2019) Genetic architecture underlying the lignin biosynthesis pathway involves noncoding RNAs and transcription factors for growth and wood properties in Populus. Plant Biotechnol J 17(1):302–315

    CAS  PubMed  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140

    CAS  PubMed  Google Scholar 

  • Roosjen M, Paque S, Weijers D (2018) Auxin Response Factors: output control in auxin biology. J Exp Bot 69(2):179–188

    CAS  PubMed  Google Scholar 

  • Roush S, Slack FJ (2008) The let-7 family of microRNAs. Trends Cell Biol 18(10):505–516

    CAS  PubMed  Google Scholar 

  • Rubinelli PM, Chuck G, Li X, Meilan R (2013) Constitutive expression of the corngrass1 microRNA in poplar affects plant architecture and stem lignin content and composition. Biomass Bioenerg 54:312–321

    CAS  Google Scholar 

  • Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16(5):258–264

    CAS  PubMed  Google Scholar 

  • Szittya G, Moxon S, Santos DM, Jing R, Fevereiro MPS, Moulton V, Dalmay T (2008) High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genom 9:593

    Google Scholar 

  • Tang F, Wei H, Zhao S, Wang L, Zheng H, Lu M (2016) Identification of microRNAs involved in regeneration of the secondary vascular system in Populus tomentosa Carr. Front Plant Sci 7:724

    PubMed  PubMed Central  Google Scholar 

  • Wang JJ, Guo HS (2015) Cleavage of INDOLE-3-ACETIC ACID INDUCIBLE28 mRNA by microRNA847 upregulates auxin signaling to modulate cell proliferation and lateral organ growth in Arabidopsis. Plant Cell 27(3):574–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Wang H (2015) The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Mol Plant 8(5):677–688

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wang D, Chen Y, Li W, Lu M, Zhou G, Chai G (2021) Vascular cambium: the source of wood formation. Front Plant Sci 12:700928

    PubMed  PubMed Central  Google Scholar 

  • Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149(2):981–993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wojcik AM, Nodine MD, Gaj MD (2017) miR160 and miR166/165 contribute to the LEC2-mediated auxin response involved in the somatic embryogenesis induction in Arabidopsis. Front Plant Sci 8:2024

    PubMed  PubMed Central  Google Scholar 

  • Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38(3):465–475

    CAS  PubMed  Google Scholar 

  • Wu Z, Cao Y, Yang R, Qi T, Hang Y, Lin H, Zhou G, Wang Z, Fu C (2016) Switchgrass SBP-box transcription factors PvSPL1 and 2 function redundantly to initiate side tillers and affect biomass yield of energy crop. Biotechnol Biofuels 9:101

    PubMed  PubMed Central  Google Scholar 

  • Xia R, Xu J, Meyers BC (2017) The emergence, evolution, and diversification of the miR390-TAS3-ARF pathway in land plants. Plant Cell 29(6):1232–1247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu C, Shen Y, He F, Fu X, Yu H, Lu W, Li Y, Li C, Fan D, Wang HC, Luo K (2019) Auxin-mediated Aux/IAA-ARF-HB signaling cascade regulates secondary xylem development in Populus. New Phytol 222(2):752–767

    CAS  PubMed  Google Scholar 

  • Yang G, Li Y, Wu B, Zhang K, Gao L, Zheng C (2019) MicroRNAs transcriptionally regulate promoter activity in Arabidopsis thaliana. J Integr Plant Biol 61(11):1128–1133

    CAS  PubMed  Google Scholar 

  • Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu J-K, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8(6):R96

    PubMed  PubMed Central  Google Scholar 

  • Zhao C, Xia H, Frazier TP, Yao Y, Bi Y, Li A, Li M, Li C, Zhang B, Wang X (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10:3

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was financially supported by National Natural Science Foundation of China (32201585 and 32101549), Natural Science Foundation of Shandong Province (ZR2022QC055), Science & Technology Specific Projects in Agricultural High-tech Industrial Demonstration Area of the Yellow River Delta (2022SZX39) and Taishan Scholar Program of Shandong (tsqn202103092).

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Authors and Affiliations

  1. College of Life Science, Inner Mongolia Agricultural University, Hohhot, 010018, China

    Lihua Yang

  2. College of Resources and Environment, Qingdao Agricultural University, Qingdao, 266109, China

    Tao Ping, Wenjin Lu, Sangfa Song, Qiao Wang & Guohua Chai

  3. Grass and Science Institute of Heilongjiang Academy of Agricultural Sciences, Harbin, 150086, China

    Jianli Wang

  4. Academy of Dongying Efficient Agricultural Technology and Industry on Saline and Alkaline Land in Collaboration with Qingdao Agricultural University, Dongying, 257000, China

    Guohua Chai

  5. Forestry College, Inner Mongolia Agricultural University, Huhhot, 010018, China

    Yue Bai & Yan Chen

  6. College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao, 266109, China

    Yan Chen

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  1. Lihua Yang
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Contributions

LY, WL and SS conducted the experiments. TP, JW and QW contributed the bioinformatic analyses. GC designed the study. YC and YB drafted the manuscript. All authors critically revised the manuscript and approved the final version.

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Correspondence to Yue Bai or Yan Chen.

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13258_2023_1385_MOESM1_ESM.png

Supplementary file1 Supplemental Fig. 1 Phenotype of one-month-old poplar seedlings grown in 1/2 MS with different concentrations of IBA treatment. (PNG 1361 KB)

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Yang, L., Ping, T., Lu, W. et al. Genome-wide identification of auxin-responsive microRNAs in the poplar stem. Genes Genom 45, 1073–1083 (2023). https://doi.org/10.1007/s13258-023-01385-7

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