Conservation and Diversity in Gibberellin-Mediated Transcriptional Responses Among Host Plants Forming Distinct Arbuscular Mycorrhizal Morphotypes

Abstract

Morphotypes of arbuscular mycorrhizal (AM) symbiosis, Arum, Paris, and Intermediate types, are mainly determined by host plant lineages. It was reported that the phytohormone gibberellin (GA) inhibits the establishment of Arum-type AM symbiosis in legume plants. In contrast, we previously reported that GA promotes the establishment of Paris-type AM symbiosis in Eustoma grandiflorum, while suppressing Arum-type AM symbiosis in a legume model plant, Lotus japonicus. This raises a hitherto unexplored possibility that GA-mediated transcriptional reprogramming during AM symbiosis is different among plant lineages as the AM morphotypes are distinct. Here, our comparative transcriptomics revealed that several symbiosis-related genes were commonly upregulated upon AM fungal colonization in L. japonicus (Arum-type), Daucus carota (Intermediate-type), and E. grandiflorum (Paris-type). Despite of the similarities, the fungal colonization levels and the expression of symbiosis-related genes were suppressed in L. japonicus and D. carota but were promoted in E. grandiflorum in the presence of GA. Moreover, exogenous GA inhibited the expression of genes involved in biosynthetic process of the pre-symbiotic signal component, strigolactone, which resulted in the reduction of its endogenous accumulation in L. japonicus and E. grandiflorum. Additionally, differential regulation of genes involved in sugar metabolism suggested that disaccharides metabolized in AM roots would be different between L. japonicus and D. carota/E. grandiflorum. Therefore, this study uncovered the conserved transcriptional responses during mycorrhization regardless of the distinct AM morphotype. Meanwhile, we also found diverse responses to GA among phylogenetically distant AM host 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.

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

“…AM morphotypes are known to change depending mainly on host traits. In previous studies, we used several host species and one AM fungal species to compare the molecular mechanisms underlying AM symbioses forming different morphotypes [ 31 , 32 ]. In this study, we focused on the transcriptional responses occurring in a single host species, tomato, associating with two AM fungi, namely, R. irregularis and G. margarita .…”

“…To elucidate these enigmas, we have recently compared the regulatory mechanisms underlying Arum - and Paris -type AM symbioses using several phylogenetically distant host species [ 31 , 32 ]. Interestingly, the phytohormone gibberellin (GA) promotes the establishment of Paris -type AM symbiosis in Eustoma grandiflorum and Primula malacoides [ 31 ], whereas GA suppresses Arum -type AM symbiosis in legume plants and rice [ 33 , 34 , 35 , 36 ].…”

“…Interestingly, the phytohormone gibberellin (GA) promotes the establishment of Paris -type AM symbiosis in Eustoma grandiflorum and Primula malacoides [ 31 ], whereas GA suppresses Arum -type AM symbiosis in legume plants and rice [ 33 , 34 , 35 , 36 ]. Notably, one of our previous studies demonstrated that AM fungal colonization transcriptionally promotes conserved symbiotic genes such as STR and RAM1 among three host plants forming distinct AM morphotypes [ 32 ]. This previous study also showed that GA treatment alters the transcriptional responses of the symbiotic genes among the examined host plants.…”

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.…”