Conserved and Diverse Transcriptional Reprogramming Triggered by the Establishment of Symbioses in Tomato Roots Forming Arum-Type and Paris-Type Arbuscular Mycorrhizae

Abstract

Arbuscular mycorrhizal (AM) fungi allocate mineral nutrients to their host plants, and the hosts supply carbohydrates and lipids to the fungal symbionts in return. The morphotypes of intraradical hyphae are primarily determined on the plant side into Arum- and Paris-type AMs. As an exception, Solanum lycopersicum (tomato) forms both types of AMs depending on the fungal species. Previously, we have shown the existence of diverse regulatory mechanisms in Arum- and Paris-type AM symbioses in response to gibberellin (GA) among different host species. However, due to the design of the study, it remained possible that the use of different plant species influenced the results. Here, we used tomato plants to compare the transcriptional responses during Arum- and Paris-type AM symbioses in a single plant species. The tomato plants inoculated with Rhizophagus irregularis or Gigaspora margarita exhibited Arum- and Paris-type AMs, respectively, and demonstrated similar colonization rates and shoot biomass. Comparative transcriptomics showed shared expression patterns of AM-related genes in tomato roots upon each fungal infection. On the contrary, the defense response and GA biosynthetic process was transcriptionally upregulated during Paris-type AM symbiosis. Thus, both shared and different transcriptional reprogramming function in establishing Arum- and Paris-type AM symbioses in tomato plants.

The RNAome landscape of tomato during arbuscular mycorrhizal symbiosis reveals an evolving RNA layer symbiotic regulatory network

“…The representative enriched pathways include transmembrane transport, regulation of protein kinase activity, fatty acid biosynthesis, fatty acid metabolic process, brassinosteroid homeostasis, response to peptide hormone, and ammonium transmembrane transport ( Figure 2 C). These pathways are highly consistent with those reported by previous studies on AMS using tomato and other angiosperms as host plants ( Sugimura and Saito, 2017 ; Tominaga et al., 2021 , 2022 ; Vasan et al., 2021 ).

Figure 2 Identification of the upregulated tomato protein-coding genes between AIR and ANR samples.

…”

“…Among the upregulated genes (defined as AMS-induced genes hereafter), 28 were orthologous to those known to be involved in AMS, including PT4 , RAM1 , RAD1 , FatM , and STR , along with some additional AMS-associated genes, demonstrating the AIRs were well colonized by AMF ( Supplemental Figure 2 and Supplemental Table 2 ). Using data from three previously reported tomato AMS-associated transcriptome studies ( Sugimura and Saito, 2017 ; Ho-Plagaro et al., 2019 ; Tominaga et al., 2022 ), a comparative analysis with AMS-induced genes was performed. The results showed that a set of 280 AMS-induced genes was identified in all four data sets; 193 and 703 genes were shared by three and two studies, respectively ( Figure 2 A).…”

“…The Micro Tom tomato was used as a model to uncover the RNAome reconfiguration induced by AMS to elucidate the RNA layer regulation of AMS. Although a reference genome for tomato is available ( Tomato Genome, 2012 ), and several previous studies have reported on tomato transcriptomics during AMS ( Sugimura and Saito, 2017 ; Ho-Plagaro et al., 2019 ; Tominaga et al., 2022 ), a global model on the role of non-coding RNA function during tomato AMS is still lacking. The results from this in-depth, combinatorial RNA-seq study of AIR and ANR samples presented here not only significantly improved the annotation of the tomato genome, but also provided a more comprehensive understanding of AMS-induced protein-coding genes ( Supplemental Figures 2 and 3 ).…”

“…Clean reads from this study and public databases ( Sugimura and Saito, 2017 ; Ho-Plagaro et al., 2019 ; Tominaga et al., 2022 ) were aligned to the S. lycopersicum reference genome using Hisat2 v2.1.0 ( Kim et al., 2019 ). The obtained transcripts were assembled by using StringTie v1.2.3 with the parameters ‘-p 8 -j 5 -a 20 -f 0.8’ ( Pertea et al., 2015 ).…”

Analysis of the molecular and biochemical mechanisms involved in the symbiotic relationship between Arbuscular mycorrhiza fungi and Manihot esculenta Crantz

“…STs are key signaling molecules used by plants to attract AMF through interactions with other phytohormones ( Lanfranco et al., 2018 ; Faizan et al., 2020 ). GAs specific roles in AMF colonization and AM symbiosis are still unclear and confusing ( Takeda et al., 2015 ; Tominaga et al., 2020 ; Tominaga et al., 2021 ; Tominaga et al., 2022 ). According to these studies, GA may promote or alter AMF penetration and proliferation in plants’ roots depending on the type of fungi.…”