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In plants, small RNA (sRNA)\u2010mediated gene silencing (sRNA\u2010MGS) plays pivotal roles in growth, development, and pathogen attack. Here, we explored the role of core components of <jats:italic>Arabidopsis thaliana<\/jats:italic> sRNA\u2010MGS pathways during its interaction with <jats:italic>Trichoderma<\/jats:italic>. Upon interaction with <jats:italic>Trichoderma<\/jats:italic>, sRNA\u2010MGS\u2010related genes paralleled the expression of Arabidopsis defense\u2010related genes, linked to salicylic acid (SA) and jasmonic acid (JA) pathways. SA\u2010 and JA\u2010related genes were primed by <jats:italic>Trichoderma<\/jats:italic> in leaves after the application of the well\u2010known pathogen\u2010associated molecular patterns flg22 and chitin, respectively. Defense\u2010related genes were primed in roots as well, but to different extents and behaviors. Phenotypical characterization of mutants in <jats:italic>AGO<\/jats:italic> genes and components of the RNA\u2010dependent DNA methylation (RdDM) pathway revealed that different sets of sRNA\u2010MGS\u2010related genes are essential for (i) the induction of systemic acquired resistance against <jats:italic>Botrytis cinerea<\/jats:italic>, (ii) the activation of the expression of plant defense\u2010related genes, and (iii)\u2009root colonization by <jats:italic>Trichoderma<\/jats:italic>. Additionally, plant growth induced by <jats:italic>Trichoderma<\/jats:italic> depends on functional RdDM. Profiling of DNA methylation and histone N\u2010tail modification patterns at the Arabidopsis <jats:italic>Nitrile\u2010Specifier Protein\u20104<\/jats:italic> (<jats:italic>NSP4<\/jats:italic>) locus, which is responsive to <jats:italic>Trichoderma<\/jats:italic>, showed altered epigenetic modifications in RdDM mutants. Furthermore, NSP4 is required for the induction of systemic acquired resistance against <jats:italic>Botrytis<\/jats:italic> and avoidance of enhanced root colonization by <jats:italic>Trichoderma<\/jats:italic>. Together, our results indicate that RdDM is essential in Arabidopsis to establish a beneficial relationship with <jats:italic>Trichoderma<\/jats:italic>. We propose that DNA methylation and histone modifications are required for plant priming by the beneficial fungus against <jats:italic>B. cinerea<\/jats:italic>.<\/jats:p>","DOI":"10.1111\/tpj.15599","type":"journal-article","created":{"date-parts":[[2021,11,22]],"date-time":"2021-11-22T15:48:46Z","timestamp":1637596126000},"page":"873-890","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":38,"title":["The small RNA\u2010mediated gene silencing machinery is required in Arabidopsis for stimulation of growth, systemic disease resistance, and suppression of the nitrile\u2010specifier gene <i>NSP4<\/i> by <i>Trichoderma atroviride<\/i>"],"prefix":"10.1111","volume":"109","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1042-5630","authenticated-orcid":false,"given":"Oscar Guillermo","family":"Rebolledo\u2010Prudencio","sequence":"first","affiliation":[{"name":"Divisi\u00f3n de Biolog\u00eda Molecular IPICYT Camino a la presa San Jos\u00e9 No. 2055, Colonia Lomas 4\u00aa Secci\u00f3n San Luis Potos\u00ed S.L.P. 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