Argonaute7 (AGO7) optimizes arbuscular mycorrhizal fungal associations and enhances competitive growth inNicotiana attenuata

Abstract

Summary Plants interact with arbuscular mycorrhizal fungi (AMF) and in doing so, change transcript levels of many miRNAs and their targets. However, the identity of an Argonaute (AGO) that modulates this interaction remains unknown, including in Nicotiana attenuata. We examined how the silencing of NaAGO1/2/4/7/and 10 by RNAi influenced plant‐competitive ability under low‐P conditions when they interact with AMF. Furthermore, the roles of seven miRNAs, predicted to regulate signaling and phosphate homeostasis, were evaluated by transient overexpression. Only NaAGO7 silencing by RNAi (irAGO7) significantly reduced the competitive ability under P‐limited conditions, without changes in leaf or root development, or juvenile‐to‐adult phase transitions. In plants growing competitively in the glasshouse, irAGO7 roots were over‐colonized with AMF, but they accumulated significantly less phosphate and the expression of their AMF‐specific transporters was deregulated. Furthermore, the AMF‐induced miRNA levels were inversely regulated with the abundance of their target transcripts. miRNA overexpression consistently decreased plant fitness, with four of seven‐tested miRNAs reducing mycorrhization rates, and two increasing mycorrhization rates. Overexpression of Na‐miR473 and Na‐miRNA‐PN59 downregulated targets in GA, ethylene, and fatty acid metabolism pathways. We infer that AGO7 optimizes competitive ability and colonization by regulating miRNA levels and signaling pathways during a plant's interaction with AMF.

A journey into the world of small RNAs in the arbuscular mycorrhizal symbiosis

“…In this case, a specific member (AGO7) of the AGO family was shown to contribute to the AM-induced sRNA modulation that allowed to control of root colonization levels through the actions of various phytohormone signaling pathways (gibberellins, ethylene and auxin) and phosphate and fatty acid metabolism (Pradhan et al, 2023). Moreover, the downregulation of N. attenuata AGO7 by RNAi led to an increased mycorrhization level (Pradhan et al, 2023). Interestingly, enhanced root nodulation was described in a M. truncatula AGO7 The downregulation (blue color) of miR393 by AM symbiosis releases its suppressive effect on members of the auxin signaling pathway, thereby promoting arbuscule development (Etemadi et al, 2014).…”

“…Similar results were obtained in the host plant Nicotiana attenuata (Pandey et al ., 2018). In this case, a specific member (AGO7) of the AGO family was shown to contribute to the AM‐induced sRNA modulation that allowed to control of root colonization levels through the actions of various phytohormone signaling pathways (gibberellins, ethylene and auxin) and phosphate and fatty acid metabolism (Pradhan et al ., 2023). Moreover, the downregulation of N. attenuata AGO7 by RNAi led to an increased mycorrhization level (Pradhan et al ., 2023).…”

“…To have a full view of the sRNA‐mediated plant gene regulation network occurring in the AM symbiosis, integrated analyses of the different populations of RNA, covering the sRNAs and their targets and including the so far little characterized tiny and circular RNAs, should be performed (Zeng et al ., 2023). The role of specific members from the DCL and/or AGO family in the AM symbiosis also deserves further investigation (Huang et al ., 2019; Pradhan & Requena, 2022; Pradhan et al ., 2023).…”