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Transcriptome-wide identification of microRNAs regulating plant immunity in Gossypium arboreum L.

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Abstract

Crop yields are linked to overall plant health, which is influenced by several regulatory processes responsible for normal gene functions. Any obstruction in gene expression causes abnormal regulatory processes, which ultimately may cause stunted growth and low yields. To cope with these stresses, plants reprogram gene expression at transcription and post-transcriptional levels, improving stress tolerance. MicroRNAs (miRNAs) are endogenous, non-coding, small RNAs that regulate various biological processes and control the expression of active genes by cleavage or translational inhibition of target messenger RNA. In this study, 56 miRNAs belonging to 19 miRNA families targeting resistance genes (R-genes) were found in the sequenced genome of G. arboreum. Seventy-nine potential target disease R-genes were predicted to be regulated by these 19 miRNA families. The result showed that both cis-acting elements of proximal promoters of 19 miRNA genes and the expression level of these miRNAs help to mediate the expression of 79 target R-genes and carry out the regulation of essential cellular processes by messenger RNA cleavage or translational repression of these genes.

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The data used to support the findings of this research are available from the corresponding author upon request.

References

  • Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442

    Article  CAS  PubMed  Google Scholar 

  • Bayless AM, Nishimura MT (2020) Enzymatic functions for toll/interleukin-1 receptor domain proteins in the plant immune system. Front Genet. https://doi.org/10.3389/fgene.2020.00539

    Article  PubMed  PubMed Central  Google Scholar 

  • Biłas R, Szafran K, Hnatuszko-Konka K, Kononowicz AK (2016) Cis-regulatory elements used to control gene expression in plants. Plant Cell Tiss Organ Cult (PCTOC) 127:269–287

    Article  Google Scholar 

  • Butler JE, Kadonaga JT (2001) Enhancer-promoter specificity mediated by DPE or TATA core promoter motifs. Genes Dev 15:2515–2519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaudhry UF, Khalid MN, Aziz S, Amjad I, Khalid A, Noor H, Sajid HB (2022) Genetic studies in different F2 segregating population for yield and fiber quality traits in cotton (Gossypium hirsutum L.). Int J Agric Biosci 11(1):59–69. https://doi.org/10.47278/journal.ijab/2022.009

    Article  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155-159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delteil A, Gobbato E, Cayrol B, Estevan J, Michel-Romiti C, Dievart A, Kroj T, Morel J-B (2016) Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol 16:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78

    Article  CAS  PubMed  Google Scholar 

  • Farooq M, Mansoor S, Guo H, Amin I, Chee PW, Azim MK, Paterson AH (2017) Identification and characterization of miRNA transcriptome in asiatic cotton (Gossypium arboreum) using high throughput sequencing. Front Plant Sci 15(8):969. https://doi.org/10.3389/fpls.2017.00969

    Article  Google Scholar 

  • Gomez-Porras JL, Riano-Pachon DM, Dreyer I, Mayer JE, Mueller-Roeber B (2007) Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC Genom 8:260

    Article  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34:D140-144

    Article  CAS  PubMed  Google Scholar 

  • Hadwiger LA, Chang M-M (2015) Low level DNA damage occurs as PAMPs, chitin and flg22, activates PR genes, and increases pisatin and disease resistance in pea endocarp tissue. New Negat Plant Sci 1:6–15

    Article  Google Scholar 

  • Hassan A, Naseer A, Shahani AAA, Aziz S, Khalid MN, Mushtaq N, Munir MA (2022) Assessment of fiber and yield related traits in mutant population of cotton. Int J Agric Biosci 11(2):95–102

    Google Scholar 

  • Helft L, Thompson M, Bent AF (2016) Directed evolution of FLS2 towards novel flagellin peptide recognition. PLoS ONE 11:e0157155

    Article  PubMed  PubMed Central  Google Scholar 

  • Herger A, Dünser K, Kleine-Vehn J, Ringli C (2019) Leucine-rich repeat extensin proteins and their role in cell wall sensing. Curr Biol 29:R851–R858

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci Int J Exp Plant Bio 217–218:109–119

    Google Scholar 

  • Huang S, Antony G, Li T, Liu B, Obasa K, Yang B, White FF (2016) The broadly effective recessive resistance gene xa5 of rice is a virulence effector-dependent quantitative trait for bacterial blight. Plant J 86:186–194

    Article  CAS  PubMed  Google Scholar 

  • Hwang EE, Wang MB, Bravo JE, Banta LM (2015) Unmasking host and microbial strategies in the Agrobacterium-plant defense tango. Front Plant Sci 6:200

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishige F, Takaichi M, Foster R, Chua N-H, Oeda K (1999) A G-box motif (GCCACGTGCC) tetramer confers high-level constitutive expression in dicot and monocot plants. Plant J 18:443–448

    Article  CAS  Google Scholar 

  • Khan AM, Khan AA, Azhar MT, Amrao L, Cheema HM (2016a) Comparative analysis of resistance gene analogues encoding NBS-LRR domains in cotton. J Sci Food and Agric 96:530–538

    Article  CAS  Google Scholar 

  • Khan IA, Akhtar KP, Akbar F, Hassan I, Amin I, Saeed M, Mansoor S (2016b) Diversity in betasatellites associated with cotton leaf curl disease during source-to-sink movement through a resistant host. Plant Pathol 32:47–52

    Article  Google Scholar 

  • Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochem Biophys Acta 1819:137–148

    CAS  PubMed  Google Scholar 

  • Komiya K, Yamamura M, Rose JA (2010) Quantitative design and experimental validation for a single-molecule DNA nanodevice transformable among three structural states. Nucleic Acids Res 38:4539–4546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kouzai Yusuke, Nakajima Keisuke, Hayafune Masahiro, Ozawa Kenjirou, Kaku Hanae, Shibuya Naoto, Minami Eiichi, Nishizawa Yoko (2014) CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Mole Bio 84(4–5):519–528. https://doi.org/10.1007/s11103-013-0149-6

    Article  CAS  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li F, Fan G, Wang K, Sun F, Yuan Y, Song G, Li Q, Ma Z, Lu C, Zou C, Chen W, Liang X, Shang H, Liu W, Shi C, Xiao G, Gou C, Ye W, Xu X, Zhang X, Wei H, Li Z, Zhang G, Wang J, Liu K, Kohel RJ, Percy RG, Yu JZ, Zhu YX, Wang J, Yu S (2014) Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet 46:567–572

    Article  CAS  PubMed  Google Scholar 

  • Li T, Zhang Q, Jiang X, Li R, Dhar N (2021) Cotton CC-NBS-LRR gene gbcnl130 confers resistance to verticillium wilt across different species. Front Plant Sci 8(12):695691. https://doi.org/10.3389/fpls.2021.695691. (PMID:34567025;PMCID:PMC8456104)

    Article  Google Scholar 

  • Liu Q, Wang F, Axtell MJ (2014) Analysis of complementarity requirements for plant microRNA targeting using a Nicotiana benthamiana quantitative transient assay. Plant Cell 26:741–753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu F, Wang H, Wang S, Jiang W, Shan C, Li B, Yang J, Zhang S, Sun W (2015) Enhancement of innate immune system in monocot rice by transferring the dicotyledonous elongation factor Tu receptor EFR. J Integr Plant Biol 57:641–652

    Article  CAS  PubMed  Google Scholar 

  • Luna E, Bruce TJ, Roberts MR, Flors V, Ton J (2012) Next-generation systemic acquired resistance. Plant Physiol 158:844–853

    Article  CAS  PubMed  Google Scholar 

  • Mao W, Li Z, Xia X, Li Y, Yu J (2012) A combined approach of high-throughput sequencing and degradome analysis reveals tissue specific expression of microRNAs and their targets in cucumber. PLoS ONE 7:e33040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng Y, Chen D, Ma X, Mao C, Cao J, Wu P, Chen M (2010) Mechanisms of microRNA-mediated auxin signaling inferred from the rice mutant osaxr. Plant Signal Behav 5:252–254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muvva C, Tewari L, Aruna K, Ranjit P, Md ZS, Md KA, Veeramachaneni H (2012) In silico identification of miRNAs and their targets from the expressed sequence tags of Raphanus sativus. Bioinformation 8:98–103

    Article  PubMed  PubMed Central  Google Scholar 

  • Nadeem M, Hasnain M, Shahzad N, Ahmad M, Nabi HG, Ullah I, Mahmood N (2023) Expression analysis of fiber related genes in different staple length genotypes in cotton (G. Hirsutum L.). Int J Agric Biosci 12(3):180–187

    Google Scholar 

  • Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP (2015) Rfam 12.0: updates to the RNA families’ database. Nucleic acids res 43:D130-137

    Article  CAS  PubMed  Google Scholar 

  • Neymotin B, Ettore V, Gresham D (2016) Multiple transcript properties related to translation affect mrna degradation rates in Saccharomyces cerevisiae. G3 Genes Genomes Genetics 6(11):3475–3483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang S, Park G, Atamian HS, Han CS, Stajich JE, Kaloshian I, Borkovich KA (2014) MicroRNAs suppress NB domain genes in tomato that confer resistance to Fusarium oxysporum. PLoS Pathology 10:e1004464

    Article  Google Scholar 

  • Park JH, Shin C (2014) MicroRNA-directed cleavage of targets: mechanism and experimental approaches. BMB Rep 47:417–423

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiao Y, Liu L, Xiong Q, Flores C, Wong J, Shi J, Wang X, Liu X, Xiang Q, Jiang S, Zhang F, Wang Y, Judelson HS, Chen X, Ma W (2013) Oomycete pathogens encode RNA silencing suppressors. Nat Genet 45:330–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reese MG (2001) Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem 26:51–56

    Article  CAS  PubMed  Google Scholar 

  • Roy S, Tripathi AM, Yadav A, Mishra P, Nautiyal CS (2016) Identification and expression analyses of miRNAs from two contrasting flower color cultivars of canna by deep sequencing. PLoS ONE 11:e0147499

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanseverino W, Roma G, De Simone M, Faino L, Melito S, Stupka E, Frusciante L, Ercolano MR (2010) PRGdb: a bioinformatics platform for plant resistance gene analysis. Nucleic Acids Res 38:D814-821

    Article  CAS  PubMed  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    Article  CAS  PubMed  PubMed Central  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 11:5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sultana F, Dev W, Zhang Z, Wang Y, Chen J, Wang J, Khan H, Tajo SM, Li Y (2023) The consequences of plant architecture and spatial distribution of light interception on cotton growth and yield. Int J Agric Biosci 12(3):153–158

    Google Scholar 

  • Thain SC, Murtas G, Lynn JR, McGrath RB, Millar AJ (2002) The circadian clock that controls gene expression in Arabidopsis is tissue specific. Plant Physiol 130:102–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trotta A, Suorsa M, Rantala M, Lundin B, Aro EM (2016) Serine and threonine residues of plant STN7 kinase are differentially phosphorylated upon changing light conditions and specifically influence the activity and stability of the kinase. Plant J 87:484–494

    Article  CAS  PubMed  Google Scholar 

  • van Ooijen G, Mayr G, Kasiem MM, Albrecht M, Cornelissen BJ, Takken FL (2008) Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59:1383–1397

    Article  PubMed  Google Scholar 

  • Ve T, Williams SJ, Kobe B (2015) Structure and function of Toll/interleukin-1 receptor/resistance protein (TIR) domains. Apoptosis Int J Program Cell Death 20:250–261

    Article  CAS  Google Scholar 

  • Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T (2008) Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132:875–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Li L, Liu L, Li H, Zhang Y, Yao Y, Ni Z, Gao J (2012) High-throughput sequencing discovery of conserved and novel microRNAs in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Mol Genet and Genomics: MGG 287:555–563

    Article  CAS  PubMed  Google Scholar 

  • Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13:59–69

    Article  CAS  Google Scholar 

  • Wu Y, Wei B, Liu H, Li T, Rayner S (2011) MiRPara: a SVM-based software tool for prediction of most probable microRNA coding regions in genome scale sequences. BMC Bioinf 12:107

    Article  CAS  Google Scholar 

  • Xu MY, Dong Y, Zhang QX, Zhang L, Luo YZ, Sun J, Fan YL, Wang L (2012) Identification of miRNAs and their targets from Brassica napus by high-throughput sequencing and degradome analysis. BMC Genomics 13:421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu M, Gonzalez-Hurtado E, Martinez E (2016) Core promoter-specific gene regulation: TATA box selectivity and Initiator-dependent bi-directionality of serum response factor-activated transcription. Biochem Biophys Acta 1859:553–563

    CAS  PubMed  Google Scholar 

  • Yali W (2022) Polyploidy and its importance in modern plant breeding improvement. Int J Agric Biosci 11(1):53–58

    Google Scholar 

  • Yuan Ning, Rai Krishan Mohan, Balasubramanian Vimal Kumar, Upadhyay Santosh Kumar, Luo Hong, Mendu Venugopal (2018) Genome-wide identification and characterization of LRR-RLKs reveal functional conservation of the SIF subfamily in cotton (Gossypium hirsutum). BMC Plant Bio. https://doi.org/10.1186/s12870-018-1395-1

    Article  Google Scholar 

  • Zhang B, Wang Q (2015) MicroRNA-based biotechnology for plant improvement. J Cell Physiol 230:1–15

    Article  PubMed  Google Scholar 

  • Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35:86–99

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors extend their appreciation to the Researchers Supporting Project number (RSP-2024R369), King Saud University, Riyadh, Saudi Arabia.

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Authors and Affiliations

  1. Institute of Plant Breeding and Biotechnology, MNS University of Agriculture, Multan, Pakistan

    Abdul Manan Khan & Muhammad Abu Bakar Saddique

  2. Department of Plant Breeding and Genetics, The University of Haripur, Haripur, 22620, Pakistan

    Sajid Fiaz

  3. School of Life Sciences, Henan Institute of Science and Technology, Xinxiang, 453003, Henan, China

    Sajid Fiaz

  4. Department of Biochemistry and Biotechnology, The Women University Multan, Multan, 66000, Pakistan

    Saba Zafar

  5. Department of Biochemistry, College of Science, King Saud University, 11451, Riyadh, Saudi Arabia

    Kotb A. Attia & Arif Ahmed Mohammed

  6. Plant Pathology and Biotechnology Laboratory, Agricultural Botany Department, Faculty of Agricultural, EPCRS Excellence Center, Kafrelsheikh University, Kafr El Sheikh, 33516, Egypt

    Yaser M. Hafez

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  1. Abdul Manan Khan
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  2. Muhammad Abu Bakar Saddique
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Contributions

Abdul Manan Khan conceived the study design, Abdul Manan Khan collected data, Muhammad Abu Bakar Saddique and Sajid Fiaz performed the statistical analyses, interpreted the results and drafted the manuscript. Saba Zafar, Kotb A. Attia, Yaser M Hafez and Arif Ahmed Mohammed performed a critical revision of the manuscript. All authors approved the version to be published and agreed to be accountable for all aspects of the work.

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Correspondence to Muhammad Abu Bakar Saddique or Sajid Fiaz.

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Khan, A.M., Saddique, M.A.B., Fiaz, S. et al. Transcriptome-wide identification of microRNAs regulating plant immunity in Gossypium arboreum L.. Genet Resour Crop Evol (2024). https://doi.org/10.1007/s10722-024-02001-7

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