Abstract
microRNAs (miRNAs) are non-coding small RNAs that regulate gene expression at post-transcriptional level. Thousands of miRNAs have been identified in legumes, but studies about miRNAs linked to peanut nodule functionality are scarce. In this work we analyzed transcriptional changes in peanut nodules to identify miRNAs involved in functional processes of these organs. We found 32 miRNAs precursors differentially expressed in nodules compared with roots, and predicted the potential targets of their corresponding mature miRNAs. Among them, 20 belong to 14 conserved miRNAs families and 12 are Arachis hypogaea-specific miRNAs. Expression levels of 3 miRNAs (ahy-miR399, ahy-miR159 and ahy-miR3508) were confirmed experimentally by qPCR. We also demonstrated that the expression of these miRNAs was not affected by inoculation of a biocontrol bacterium or a fungal pathogen. The catalogue of differentially expressed miRNA precursors and the expression of the corresponding mature miRNA potential targets in the nodules of A. hypogaea obtained in this work is a database of strong candidates, including A. hypogaea-specific miRNAs, for the regulation of the nodule functionality. The analysis of their role in this process will certainly lead to the characterization of essential regulators in these particular aeschynomenoid nodules.
References
Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier J and Frugier F 2008 MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J. 54 876–887
Chi X, Yang Q, Chen X, Wang J, Pan L, Chen M, et al. 2011 Identification and characterization of microRNAs from peanut (Arachis hypogaea L.) by high-throughput sequencing. PloS one 6 e27530
Clevenger J, Chu Y, Scheffler B and Ozias-Akins P 2016 A developmental transcriptome map for allotetraploid Arachis hypogaea. Front. Plant Sci. 7 1446
Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, et al. 2004 Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39 487–512
Dai X and Zhao P 2011 psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res. 39 W155–W159
De Luis A, Markmann K, Cognat V, Holt D, Charpentier M, Parniske M, Stougaard J and Voinnet O 2012 Two microRNAs linked to nodule infection and nitrogen-fixing ability in the legume Lotus japonicus. Plant Physiol. 160 2137–2154
El Yahyaoui F, Kuster H, Ben Amor B, Hohnjec N, Puhler A, Becker A, Gouzy J, Vernié T, Gough C, Niebel A, Godiard L and Gamas P 2004 Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol. 136 3159–3176
Figueredo MS, Tonelli ML, Ibáñez F, Morla F, Cerioni G, Tordable M and Fabra A 2017 Induced systemic resistance and symbiotic performance of peanut plants challenged with fungal pathogens and co-inoculated with the biocontrol agent Bacillus sp. CHEP5 and Bradyrhizobium sp. SEMIA6144. Microbiol. Res. 197 65–73
Formey D, Iñiguez LP, Peláez P, Li YF, Sunkar R, Sánchez F, et al. 2015 Genome-wide identification of the Phaseolus vulgaris sRNAome using small RNA and degradome sequencing. BMC Genomics 16 423–440
Formey D, Sallet E, Lelandais-Brière C, Ben C, Bustos-Sanmamed P, Niebel A and Poulain J 2014 The small RNA diversity from Medicago truncatula roots under biotic interactions evidences the environmental plasticity of the miRNAome. Genome Biol. 15 457–478
Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, et al. 2008 High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acid Res. 36 3420–3435
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. 2011 Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat. Biotechnol. 29 644–652
Gupta OP, Sharma P, Gupta RK and Sharma I 2014 MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives. Plant Mol. Biol. 84 1–18
Høgslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah MA, Goffard N, Sanchez DH, Lippold F, et al. 2009 Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS One 4 e6556
Jin D, Meng X, Wang Y, Wang J, Zhao Y and Chen M 2018 Computational investigation of small RNAs in the establishment of root nodules and arbuscular mycorrhiza in leguminous plants. Sci. China Life Sci. 61 706–717
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S and Madden TL 2008 NCBI BLAST: a better web interface. Nucleic Acids Res. 36 W5–W9
Kozomara A and Griffiths-Jones S 2013 miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42 D68–D73
Lelandais-Brière C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J and Crespi M 2009 Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21 780–796
Li B and Dewey CN 2011 RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12 323
Livak KJ and Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25 402–408
Love MI, Huber W, Anders S 2014 Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15 550
Rajendiran A, Vijayakumar S and Pan A 2019 Exploring microRNAs, target mRNAs and their functions in leguminous plant Arachis hypogaea. MicroRNA 8 135–146
Shriram V, Kumar V, Devarumath RM, Khare TS and Wani SH 2016 MicroRNAs as potential target for abiotic stress tolerance in plants. Front. Plant Sci. 7 817–835
Stalker HT 1997 Peanut (Arachis hypogaea L.). Field Crops Res. 53 205–217
Subramanian S, Fu Y, Sunkar R, Barbazuk WB, Zhu JK and Yu O 2008 Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9 160–174
Van Rossum D, Schuumans F, Gillis M, Muyotcha A, Van Verseveld H, Stouthamer A and Boogerd F 1995 Genetic and phenetic analyses of Bradyrhizobium strains nodulating peanut (Arachis hypogaea L.) roots. Appl. Environ. Microbiol. 6 1599–1609
Vincent JM 1970 A manual for the practical study of the root-nodule bacteria. A manual for the practical study of the root-nodule bacteria. IBP Handbook. Oxford: Blackwell Scientific Publications Ltd, pp 73–97
Wang Y, Li K, Chen L, Zou Y, Liu H, Tian Y, Li D, Wang R, et al. 2015 MicroRNA167-directed regulation of the Auxin response factors GmARF8a and GmARF8b is required for soybean nodulation and lateral root development. Plant Physiol. 168 984–999
Wang Y, Li P, Cao X, Wang X, Zhang A and Li X 2009 Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochem. Biophys. Res. Commun. 378 799–803
Yan Z, Hossain MS, Arikit S, Valdés-López O, Zhai J, Wang J and Stacey G 2015 Identification of microRNAs and their mRNA targets during soybean nodule development: functional analysis of the role of miR393j-3p in soybean nodulation. New Phytol. 207 748–759
Zhang T, Hu S, Yan C, Li C, Zhao X, Wan S and Shan S 2017 Mining, identification and function analysis of microRNAs and target genes in peanut (Arachis hypogaea L.). Plant Physiol. Biochem. 111 85–96
Zhao CZ, Xia H, Frazier TP, Yao YY, Bi YP, Li AQ, Li MJ, Li CS, et al. 2010 Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol. 10 3–15
Acknowledgements
MSF and JR hold a scholarship granted by CONICET and ANPCyT, respectively. FI and AF are members of the Research Career from CONICET. DF and GH are members of the National System of Researchers from CONACYT.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by BJ RAO.
Corresponding editor: BJ RAO
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Figueredo, M.S., Formey, D., Rodríguez, J. et al. Identification of miRNAs linked to peanut nodule functional processes. J Biosci 45, 62 (2020). https://doi.org/10.1007/s12038-020-00034-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12038-020-00034-5