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sRNAs involved in the regulation of plant developmental processes are altered during the root-knot nematode interaction for feeding site formation

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Abstract

Plant parasitic root- knot nematodes (RKNs; Meloidogyne spp.) are a significant threat for the agriculture as they infect multiple crops, causing severe economic losses worldwide. Most of the effective chemical nematicides have been or are in the process of being banned on the basis of their harmful effect to the environment and human health. These nematodes penetrate the root, migrate intercellularly and establish in the vascular cylinder. Then, nematode effectors delivered into the plant cells alter the plant development to induce their feeding cells, called giant cells (GCs) that serve to nourish them till life cycle completion. The GCs are embedded into a swelling in the root, called gall, formed by the proliferation and/or hypertrophy of the surrounding tissues. Further studies on the development of the nematode-feeding sites, i.e. to deepen into the molecular bases of the plant-nematode interaction, are required to identify alternative approaches for nematode control. Here, we summarize recent advances specifically in the role of the small RNAs during the compatible interactions between RKNs and Arabidopsis and tomato hosts. Most of the studies describe the deregulation in the galls and/or GCs of gene regulatory modules composed by miRNAs and transcription factors which have already an assigned function during development and/or organogenesis processes in the plant. This may point to a role for these miRNAs as molecular hubs of pathways triggered either by developmental plant cues or by a biotic stress as the nematode infection.

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Fig. 1: Integrated diagram of the major steps in plant miRNA biogenesis and current knowledge on RKN - plant interactions.
Fig. 2: MYB33:GUS is specifically induced in response to nematode GCs development.

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References

  • Aukerman, M. J., & Sakai, H. (2003). Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell, 15(11), 2730–2741. https://doi.org/10.1105/tpc.016238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Axtell, M. J. (2013). Classification and comparison of small RNAs from plants. Annual Review of Plant Biology, 64, 137–159. https://doi.org/10.1146/annurev-arplant-050312-120043.

    Article  CAS  PubMed  Google Scholar 

  • Barcala, M., Garcia, A., Cabrera, J., Casson, S., Lindsey, K., Favery, B., et al. (2010). Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. The Plant Journal, 61(4), 698–712. https://doi.org/10.1111/j.1365-313X.2009.04098.x.

    Article  CAS  PubMed  Google Scholar 

  • Barrero, C., Royo, J., Grijota-Martinez, C., Faye, C., Paul, W., Sanz, S., et al. (2009). The promoter of ZmMRP-1, a maize transfer cell-specific transcriptional activator, is induced at solute exchange surfaces and responds to transport demands. Planta, 229, 235–247. https://doi.org/10.1007/s00425-008-0823-0.

    Article  CAS  PubMed  Google Scholar 

  • Berger, Y., Harpaz-Saad, S., Brand, A., Melnik, H., Sirding, N., Alvarez, J. P., et al. (2009). The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development, 136(5), 823–832.

    Article  CAS  Google Scholar 

  • Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., & Voinnet, O. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science, 320(5880), 1185–1190.

    Article  CAS  Google Scholar 

  • Brown Miyara, S., Ionit, I., Buki, P., & Kolomiets, M. (2015). The Role of Lipid Signalling in Regulating Plant–Nematode Interactions. Advances in Botanical Research, 73, 139–166. https://doi.org/10.1016/bs.abr.2014.12.004.

    Article  CAS  Google Scholar 

  • Buck, A. H., Coakley, G., Simbari, F., McSorley, H. J., Quintana, J. F., Le Bihan, T., et al. (2014). Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nature Communications, 5, 5488.

    Article  CAS  Google Scholar 

  • Cabrera, J., Diaz-Manzano, F. E., Sanchez, M., Rosso, M. N., Melillo, T., Goh, T., et al. (2014). A role for Lateral Organ Boundaries-Domain 16 during the interaction Arabidopsis-Meloidogyne spp. provides a molecular link between lateral root and root-knot nematode feeding site development. New Phytologist, 203(2), 632–645. https://doi.org/10.1111/nph.12826.

    Article  CAS  PubMed  Google Scholar 

  • Cabrera, J., Díaz-Manzano, F. E., Fenoll, C., & Escobar, C. (2015). Developmental Pathways Mediated by Hormones in Nematode Feeding Sites. Advances in Botanical Research, 73, 167–188. https://doi.org/10.1016/bs.abr.2014.12.005.

    Article  CAS  Google Scholar 

  • Cabrera, J., Barcala, M., Garcia, A., Rio-Machin, A., Medina, C., Jaubert-Possamai, S., et al. (2016). Differentially expressed small RNAs in Arabidopsis galls formed by Meloidogyne javanica: a functional role for miR390 and its TAS3-derived tasiRNAs. New Phytologist, 209(4), 1625–1640. https://doi.org/10.1111/nph.13735.

    Article  CAS  PubMed  Google Scholar 

  • Cao, Y., Han, Y., Jin, Q., Lin, Y., & Cai, Y. (2016). Comparative genomic analysis of the GRF genes in Chinese pear (Pyrus bretschneideri Rehd), poplar (Populous), grape (Vitis vinifera), Arabidopsis and rice (Oryza sativa). Frontiers in Plant Science, 7, 1750.

    PubMed  PubMed Central  Google Scholar 

  • Chen, C., Ridzon, D. A., Broomer, A. J., Zhou, Z., Lee, D. H., Nguyen, J. T., et al. (2005). Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Research, 33(20), e179. https://doi.org/10.1093/nar/gni178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Almeida Engler, J., Vieira, P., Rodiuc, N., Grossi de Sa, M. F., & Engler, G. (2015). The Plant Cell Cycle Machinery: Usurped and Modulated by Plant-Parasitic Nematodes. Advances in Botanical Research, 73, 91–118. https://doi.org/10.1016/bs.abr.2014.12.003.

    Article  CAS  Google Scholar 

  • Diaz-Manzano, F. E., Barcala, M., Engler, G., Fenoll, C., de Almeida-Engler, J., & Escobar, C. (2016). A reliable protocol for In situ microRNAs detection in feeding sites induced by root-knot nematodes. Frontiers in Plant Science, 7, 966. https://doi.org/10.3389/fpls.2016.00966.

    Article  PubMed  PubMed Central  Google Scholar 

  • Díaz-Manzano, F. E., Cabrera, J., Ripoll, J.J., del Olmo, I., Andrés, M. F., Silva, A. C., Barcala, M., Sánchez, M., Ruíz-Ferrer, V., de Almeida-Engler, J., Yanofsky, M. F., Piñeiro, M., Jarillo, J. A., Fenoll, C. & Escobar, C. (2018). A role for the gene regulatory module microRNA172/TARGET OF EARLY ACTIVATION TAGGED 1/FLOWERING LOCUS T (miRNA172/TOE1/FT) in the feeding sites induced by Meloidogyne javanica in Arabidopsis thaliana. New Phytologist, 217(2), 813–827.

    Article  Google Scholar 

  • Dowen, R. H., Pelizzola, M., Schmitz, R. J., Lister, R., Dowen, J. M., Nery, J. R., et al. (2012). Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences, 109(32), E2183–E2191.

    Article  CAS  Google Scholar 

  • Dropkin, V. H. (1972). Pathology of Meloidogyne— Galling, Giant Cell Formation, Effects on Host Physiology. EPPO Bulletin, 2(6), 23–32. https://doi.org/10.1111/j.1365-2338.1972.tb02128.x.

    Article  Google Scholar 

  • Escobar, C., Barcala, M., Cabrera, J., & Fenoll, C. (2015). Overview of Root-Knot Nematodes and Giant Cells. Advances in Botanical Research, 73, 1–32. https://doi.org/10.1016/bs.abr.2015.01.001.

    Article  Google Scholar 

  • Franco-Zorrilla, J. M., Valli, A., Todesco, M., Mateos, I., Puga, M. I., Rubio-Somoza, I., et al. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics, 39(8), 1033–1037.

    Article  CAS  Google Scholar 

  • Haag, J. R., & Pikaard, C. S. (2011). Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nature Reviews. Molecular Cell Biology, 12(8), 483.

    Article  CAS  Google Scholar 

  • Han, L., & Luan, Y. S. (2015). Horizontal Transfer of Small RNAs to and from Plants. Frontiers in Plant Science, 6, 1113. https://doi.org/10.3389/fpls.2015.01113.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hewezi, T., Howe, P., Maier, T. R., & Baum, T. J. (2008). Arabidopsis small RNAs and their targets during cyst nematode parasitism. Molecular Plant-Microbe Interactions, 21, 1622–1634.

    Article  CAS  Google Scholar 

  • Hewezi, T., Maier, T. R., Nettleton, D., & Baum, T. J. (2012). The Arabidopsis microRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiology, 159(1), 321–335. https://doi.org/10.1104/pp.112.193649.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hewezi, T., Lane, T., Piya, S., Rambani, A., Rice, J. H., & Staton, M. (2017). Cyst nematode parasitism induces dynamic changes in the root epigenome. Plant Physiology, 174(1), 405–420.

    Article  CAS  Google Scholar 

  • Jain, S., Chittem, K., Brueggeman, R., Osorno, J. M., Richards, J., & Nelson Jr., B. D. (2016). Comparative transcriptome analysis of resistant and susceptible common bean genotypes in response to soybean cyst nematode infection. PLoS One, 11(7), e0159338.

    Article  Google Scholar 

  • Jammes, F., Lecomte, P., Almeida‐Engler, J., Bitton, F., Martin‐Magniette, M-L., Renou, JP., Abad, P., & Favery, B. (2005). Genome‐wide expression profiling of the host response to root‐knot nematode infection in Arabidopsis. The Plant Journal, 44(3) 447–458.

  • Jones-Rhoades, M. W., & Bartel, D. P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell, 14(6), 787–799.

    Article  CAS  Google Scholar 

  • Kaur, P., Shukla, N., Joshi, G., VijayaKumar, C., Jagannath, A., Agarwal, M., et al. (2017). Genome-wide identification and characterization of miRNAome from tomato (Solanum lycopersicum) roots and root-knot nematode (Meloidogyne incognita) during susceptible interaction. PLoS One, 12(4), e0175178. https://doi.org/10.1371/journal.pone.0175178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knip, M., Constantin, M. E., & Thordal-Christensen, H. (2014). Trans-kingdom Cross-Talk: Small RNAs on the Move. PLoS Genetics, 10(9), e1004602. https://doi.org/10.1371/journal.pgen.1004602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumari, C., Dutta, T. K., Banakar, P., & Rao, U. (2016). Comparing the defence-related gene expression changes upon root-knot nematode attack in susceptible versus resistant cultivars of rice. Scientific Reports, 6, 22846.

    Article  CAS  Google Scholar 

  • Kyndt, T., Fernandez, D., & Gheysen, G. (2014). Plant-parasitic nematode infections in rice: molecular and cellular insights. Annual Review of Phytopathology, 52, 135–153.

    Article  CAS  Google Scholar 

  • Lauressergues, D., Couzigou, J. M., San Clemente, H., Martinez, Y., Dunand, C., Bécard, G., & Combier, J. P. (2015). Primary transcripts of microRNAs encode regulatory peptides. Nature, 520(7545), 90–93.

    Article  CAS  Google Scholar 

  • Li, C., & Zhang, B. (2016). MicroRNAs in Control of Plant Development. Journal of Cellular Physiology, 231(2), 303–313. https://doi.org/10.1002/jcp.25125.

    Article  CAS  PubMed  Google Scholar 

  • Liu, B., Liu, X., Liu, Y., Xue, S., Cai, Y., Yang, S., et al. (2016). The infection of cucumber (Cucumis sativus L.) roots by Meloidogyne incognita alters the expression of actin-depolymerizing factor (ADF) genes, particularly in association with giant cell formation. Frontiers in Plant Science, 7, 1393.

  • Ma, X., Tang, Z., Qin, J., & Meng, Y. (2015). The use of high-throughput sequencing methods for plant microRNA research. RNA Biology, 12(7), 709–719. https://doi.org/10.1080/15476286.2015.1053686.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marin, E., Jouannet, V., Herz, A., Lokerse, A. S., Weijers, D., Vaucheret, H., et al. (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. https://doi.org/10.1105/tpc.109.072553.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matzke, M. A., & Mosher, R. A. (2014). RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nature Reviews. Genetics, 15(6), 394–408. https://doi.org/10.1038/nrg3683.

    Article  CAS  PubMed  Google Scholar 

  • Matzke, M. A., Kanno, T., & Matzke, A. J. (2015). RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annual Review of Plant Biology, 66, 243–267.

    Article  CAS  Google Scholar 

  • Medina, C., Rocha, M., Magliano, M., Ratpopoulo, A., Revel, B., Marteu, N., et al. (2017). Characterization of microRNAs from Arabidopsis galls highlights a role for miR159 in the plant response to the root-knot nematode Meloidogyne incognita. New Phytologist, 216(3), 882–896.

    Article  CAS  Google Scholar 

  • Millar, A. A., & 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. https://doi.org/10.1105/tpc.104.027920.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moens, M., Perry, R. N., & Starr, J. L. (2009). Meloidogyne species: a diverse group of novel and important plant parasites. In R. N. Perry, M. Moens, & J. L. Starr (Eds.), Root-knot Nematodes (pp. 1–17). Wallingford: CABI Publishing.

    Google Scholar 

  • Nag, A., King, S., & Jack, T. (2009). miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proceedings of the National Academy of Sciences, 106(52), 22534–22539.

  • Okushima, Y., Fukaki, H., Onoda, M., Theologis, A., & Tasaka, M. (2007). ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell, 19(1), 118–130. https://doi.org/10.1105/tpc.106.047761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olmo, R., Cabrera, J., Moreno-Risueno, M. A., Fukaki, H., Fenoll, C., & Escobar, C. (2017). Molecular transducers from roots are triggered in arabidopsis leaves by root-knot nematodes for successful feeding site formation: a conserved post-embryogenic de novo organogenesis program? Frontiers in Plant Science, 8, 875. https://doi.org/10.3389/fpls.2017.00875.

    Article  PubMed  PubMed Central  Google Scholar 

  • Omidbakhshfard, M. A., Proost, S., Fujikura, U., & Mueller-Roeber, B. (2015). Growth-Regulating Factors (GRFs): a small transcription factor family with important functions in plant biology. Molecular Plant, 8(7), 998–1010. https://doi.org/10.1016/j.molp.2015.01.013.

    Article  CAS  PubMed  Google Scholar 

  • Ori, N., Cohen, A. R., Etzioni, A., Brand, A., Yanai, O., Shleizer, S., et al. (2007). Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nature Genetics, 39(6), 787–791. https://doi.org/10.1038/ng2036.

    Article  CAS  PubMed  Google Scholar 

  • Pan X., Nichols R. L., Li C., & Zhang B. (2018). MicroRNA-target gene responses to root knot nematode (Meloidogyne incognita) infection in cotton (Gossypium hirsutum L.). Genomics, S0888-7543(18), 30117–4. https://doi.org/10.1016/j.ygeno.2018.02.013

  • Petitot, A. S., Kyndt, T., Haidar, R., Dereeper, A., Collin, M., de Almeida Engler, J., et al. (2017). Transcriptomic and histological responses of African rice (Oryza glaberrima) to Meloidogyne graminicola provide new insights into root-knot nematode resistance in monocots. Annals of Botany, 119(5), 885–899.

    Article  CAS  Google Scholar 

  • Portillo, M., Cabrera, J., Lindsey, K., Topping, J., Andres, M. F., Emiliozzi, M., et al. (2013). Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. New Phytologist, 197(4), 1276–1290. https://doi.org/10.1111/nph.12121.

    Article  CAS  PubMed  Google Scholar 

  • Pumplin, N., & Voinnet, O. (2013). RNA silencing suppression by plant pathogens: defence, counterdefence and counter-counter-defence. Nature Reviews Microbiology, 11(11), 745.

  • Ripoll, J. J., Bailey, L. J., Mai, Q. A., Wu, S. L., Hon, C. T., Chapman, E. J., et al. (2015). microRNA regulation of fruit growth. Nature Plants, 1(4), 15036. https://doi.org/10.1038/nplants.2015.36.

    Article  CAS  Google Scholar 

  • Rodriguez, R. E., Schommer, C., & Palatnik, J. F. (2016). Control of cell proliferation by microRNAs in plants. Current Opinion in Plant Biology, 34, 68–76. https://doi.org/10.1016/j.pbi.2016.10.003.

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Ferrer, V., & Voinnet, O. (2009). Roles of plant small RNAs in biotic stress responses. Annual Review of Plant Biology, 60, 485–510.

    Article  CAS  Google Scholar 

  • Schommer, C., Debernardi, J. M., Bresso, E. G., Rodriguez, R. E., & Palatnik, J. F. (2014). Repression of Cell Proliferation by miR319-Regulated TCP4. Molecular Plant, 7(10), 1533–1544. https://doi.org/10.1093/mp/ssu084.

    Article  CAS  PubMed  Google Scholar 

  • Shafiq, S., Li, J., & Sun, Q. (2016). Functions of plants long non-coding RNAs. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1859(1), 155–162.

    Article  CAS  Google Scholar 

  • Siddique, S., & Grundler, F. M. W. (2015). Metabolism in nematode feeding sites. Advances in Botanical Research, 73, 119–138. https://doi.org/10.1016/bs.abr.2015.02.001.

    Article  CAS  Google Scholar 

  • Subramanian, P., Choi, I. C., Mani, V., Park, J., Subramaniyam, S., Choi, K. H., et al. (2016). Stage-wise identification and analysis of miRNA from root-knot nematode meloidogyne incognita. International Journal of Molecular Sciences, 17(10). https://doi.org/10.3390/ijms17101758.

  • Wang, H. L. V., & Chekanova, J. A. (2016). Small RNAs: essential regulators of gene expression and defenses against environmental stresses in plants. Wiley Interdisciplinary Reviews: RNA, 7(3), 356–381.

    Article  CAS  Google Scholar 

  • Wang, Y., Wang, L., Zou, Y., Chen, L., Cai, Z., Zhang, S., et al. (2014). Soybean miR172c targets the repressive AP2 transcription factor NNC1 to activate ENOD40 expression and regulate nodule initiation. Plant Cell, 26(12), 4782–4801. https://doi.org/10.1105/tpc.114.131607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Mao, Z., Yan, J., Cheng, X., Liu, F., Xiao, L., et al. (2015). Identification of MicroRNAs in Meloidogyne incognita Using Deep Sequencing. PLoS One, 10(8), e0133491. https://doi.org/10.1371/journal.pone.0133491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wendte, J. M., & Pikaard, C. S. (2017). The RNAs of RNA-directed DNA methylation. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1860(1), 140–148.

    Article  CAS  Google Scholar 

  • Wesemael, W., Moens, M., & Viaene, N. (2011). Root-knot nematodes (Meloidogyne spp.) in Europe. Nematology, 13(1), 3–16. https://doi.org/10.1163/138855410x526831.

    Article  Google Scholar 

  • Wieczorek, K. (2015). Cell Wall Alterations in Nematode-Infected Roots. Advances in Botanical Research, 73, 61–90. https://doi.org/10.1016/bs.abr.2014.12.002.

    Article  CAS  Google Scholar 

  • Wu, H. J., Wang, Z. M., Wang, M., & Wang, X. J. (2013). Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiology, 161(4), 1875–1884.

    Article  CAS  Google Scholar 

  • Wyss, U., & Grundler, F. M. W. (1992). Feeding behavior of sedentary plant parasitic nematodes. [journal article]. Netherlands Journal of Plant Pathology, 98(2), 165–173. https://doi.org/10.1007/bf01974483.

    Article  Google Scholar 

  • Xu, M., Hu, T., Zhao, J., Park, M. Y., Earley, K. W., Wu, G., et al. (2016). Developmental functions of miR156-regulated Squamosa Promoter Binding Protein-Like (SPL) genes in Arabidopsis thaliana. PLoS Genetics, 12(8), e1006263.

    Article  Google Scholar 

  • Yan, Z., Hossain, M. S., Wang, J., Valdes-Lopez, O., Liang, Y., Libault, M., et al. (2013). miR172 regulates soybean nodulation. Molecular Plant-Microbe Interactions, 26(12), 1371–1377. https://doi.org/10.1094/MPMI-04-13-0111-R.

    Article  CAS  PubMed  Google Scholar 

  • Ye, D. Y., Qi, Y. H., Cao, S. F., Wei, B. Q., & Zhang, H. S. (2017). Histopathology combined with transcriptome analyses reveals the mechanism of resistance to Meloidogyne incognita in Cucumis metuliferus. Journal of Plant Physiology, 212, 115–124.

    Article  CAS  Google Scholar 

  • You, W., Lorkovic, Z. J., Matzke, A. J., & Matzke, M. (2013). Interplay among RNA polymerases II, IV and V in RNA-directed DNA methylation at a low copy transgene locus in Arabidopsis thaliana. Plant Molecular Biology, 82(1–2), 85–96.

    Article  CAS  Google Scholar 

  • Yu, A., Lepère, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., et al. (2013). Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proceedings of the National Academy of Sciences, 110(6), 2389–2394.

    Article  CAS  Google Scholar 

  • Zhang, Y., Wang, Y., Xie, F., Li, C., Zhang, B., Nichols, R. L., et al. (2016). Identification and characterization of microRNAs in the plant parasitic root-knot nematode Meloidogyne incognita using deep sequencing. Functional & Integrative Genomics, 16(2), 127–142. https://doi.org/10.1007/s10142-015-0472-x.

    Article  CAS  Google Scholar 

  • Zhao, W., Li, Z., Fan, J., Hu, C., Yang, R., Qi, X., et al. (2015). Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. Journal of Experimental Botany, 66(15), 4653–4667. https://doi.org/10.1093/jxb/erv238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng, B., Wang, Z., Li, S., Yu, B., Liu, J. Y., & Chen, X. (2009). Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes & Development, 23(24), 2850–2860.

    Article  CAS  Google Scholar 

  • Zhou, G., Zhou, Y., & Chen, X. (2017). New insight into inter-kingdom communication: horizontal transfer of mobile small RNAs. Frontiers in Microbiology, 8, 768.

    Article  Google Scholar 

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Acknowledgements

Work supported by the Spanish Government (grants AGL2013-48787; AGL2016-75287-R to CE, CSD2007-057 and PCIN-2013-053 to CF) and by the Castilla-La Mancha Government (PEII-2014-020-P to CF). JC is supported by a Cytema-Santander contract from Universidad de Castilla- La Mancha. We apologize to all colleagues whose work could not be cited due to the size limitations of this manuscript.

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Correspondence to Carolina Escobar.

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Cabrera, J., Ruiz-Ferrer, V., Fenoll, C. et al. sRNAs involved in the regulation of plant developmental processes are altered during the root-knot nematode interaction for feeding site formation. Eur J Plant Pathol 152, 945–955 (2018). https://doi.org/10.1007/s10658-018-1451-6

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