DLK2 regulates arbuscule hyphal branching during arbuscular mycorrhizal symbiosis

Ho-Plágaro, Tania; Morcillo, Rafael J. L.; Tamayo-Navarrete, María I.; Huertas, Raúl; Molinero‐Rosales, Nuria; López‐Ráez, Juan Antonio; Macho, Alberto P.; García‐Garrido, José Manuel

doi:10.1111/nph.16938

Cited by 28 publications

(30 citation statements)

References 71 publications

(107 reference statements)

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“…Of the SL signaling-related genes, DLK2 was significantly induced in the examined host plants upon AM fungal colonization compared with NC control ( Figure 4 ). Similarly, DLK2 induction was reported in other host plants, O. sativa and Solanum lycopersicum ( Choi et al, 2020 ; Ho-Plagaro et al, 2021 ). Moreover, compared with the +AMF control, GA treatment significantly reduced DLK2 expression in L. japonicus but further increased in E. grandiflorum ( Figures 4A,C ; Tominaga et al, 2020b ).…”

Section: Resultssupporting

confidence: 73%

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

et al. 2021

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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.

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Section: Resultssupporting

confidence: 73%

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

et al. 2021

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“…Furthermore, KAI2‐dependent signalling may have a role in regulating the lifespan of AM symbiosis, at least on the level of individual arbuscules. Recently, an AM‐inducible DLK2 homologue was shown to constrain mycorrhizal colonisation and control the life cycle of arbuscules in tomato (Ho‐Plágaro et al., 2021). In Brachypodium, all three DLK2 homologues were induced by AM colonisation, as were DLK2a (Os05g51240) and DLK2b (Os01g41240) in rice (Kobae et al., 2018).…”

Section: Discussionmentioning

confidence: 99%

KARRIKIN INSENSITIVE2 regulates leaf development, root system architecture and arbuscular‐mycorrhizal symbiosis in Brachypodium distachyon

et al. 2022

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SUMMARY KARRIKIN INSENSITIVE2 (KAI2) is an α/β‐hydrolase required for plant responses to karrikins, which are abiotic butenolides that can influence seed germination and seedling growth. Although represented by four angiosperm species, loss‐of‐function kai2 mutants are phenotypically inconsistent and incompletely characterised, resulting in uncertainties about the core functions of KAI2 in plant development. Here we characterised the developmental functions of KAI2 in the grass Brachypodium distachyon using molecular, physiological and biochemical approaches. Bdkai2 mutants exhibit increased internode elongation and reduced leaf chlorophyll levels, but only a modest increase in water loss from detached leaves. Bdkai2 shows increased numbers of lateral roots and reduced root hair growth, and fails to support normal root colonisation by arbuscular‐mycorrhizal (AM) fungi. The karrikins KAR1 and KAR2, and the strigolactone (SL) analogue rac‐GR24, each elicit overlapping but distinct changes to the shoot transcriptome via BdKAI2. Finally, we show that BdKAI2 exhibits a clear ligand preference for desmethyl butenolides and weak responses to methyl‐substituted SL analogues such as GR24. Our findings suggest that KAI2 has multiple roles in shoot development, root system development and transcriptional regulation in grasses. Although KAI2‐dependent AM symbiosis is likely conserved within monocots, the magnitude of the effect of KAI2 on water relations may vary across angiosperms.

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“…Moreover, the expression of SlDLK2 was also upregulated by the two AM fungi ( Figure 5 b, Table S4 ). Recent work has elucidated the involvement of SlDLK2 in the negative regulation of arbuscule branching [ 43 ]. In addition to AM-upregulated SlVpy expression, the mechanisms underlying arbuscule formation would be shared in Arum - and Paris -type AMs.…”

Section: Discussionmentioning

confidence: 99%

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

Tominaga

Yao

Saito

et al. 2022

Plants

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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.

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DLK2 regulates arbuscule hyphal branching during arbuscular mycorrhizal symbiosis

Cited by 28 publications

References 71 publications

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

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

KARRIKIN INSENSITIVE2 regulates leaf development, root system architecture and arbuscular‐mycorrhizal symbiosis in Brachypodium distachyon

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

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