Zaxinone synthase controls arbuscular mycorrhizal colonization level in rice

Abstract

The Oryza sativa (rice) carotenoid cleavage dioxygenase OsZAS was described to produce zaxinone, a plant growth-promoting apocarotenoid. A zas mutant line showed reduced arbuscular mycorrhizal (AM) colonization, but the mechanisms underlying this behavior are unknown. Here, we investigated how OsZAS and exogenous zaxinone treatment regulate mycorrhization. Micromolar exogenous supply of zaxinone rescued root growth but not the mycorrhizal defects of the zas mutant, and even reduced mycorrhization in wildtype and zas genotypes. The zas line did not display the increase in the level of strigolactones (SLs) that was observed in wild-type plants at 7 days post-inoculation with AM fungus. Moreover, exogenous treatment with the synthetic SL analog GR24 rescued the zas mutant mycorrhizal phenotype, indicating that the lower AM colonization rate of zas is caused by a deficiency in SLs at the early stages of the interaction, and indicating that during this phase OsZAS activity is required to induce SL production, possibly mediated by the Dwarf14-Like (D14L) signaling pathway. OsZAS is expressed in arbuscule-containing cells, and OsPT11prom::OsZAS transgenic lines, where OsZAS expression is driven by the OsPT11 promoter active in arbusculated cells, exhibit increased mycorrhization compared with the wild type. Overall, our results show that the genetic manipulation of OsZAS activity in planta leads to a different effect on AM symbiosis from that of exogenous zaxinone treatment, and demonstrate that OsZAS influences the extent of AM colonization, acting as a component of a regulatory network that involves SLs.

ZAXINONE SYNTHASE 2 regulates growth and arbuscular mycorrhizal symbiosis in rice

“…A similar phenotype was also observed in the Oszas mutant ( Wang et al, 2019 ). We recently demonstrated that the lower AM colonization rate of the Oszas mutant is due to SL deficiency at the early stage of the AM interaction ( Votta et al, 2022 ): during this phase OsZAS activity is required to induce SL production possibly through the Dwarf14-Like (D14L) signaling pathway which was shown to regulate AM colonization in rice ( Gutjahr et al, 2015 ). We can hypothesize that also OsZAS2 acts as a component of a regulatory network that involves SL and D14L pathways.…”

Carotenoid metabolism: New insights and synthetic approaches

“…Apocarotenoids exert a series of further biological activities, such as regulating of growth, biotic and abiotic stress response, retrograde signaling, photo acclimation, and include pigments and volatiles that play a role in plant-animal communication ( Wang et al., 2019 ; Jia et al., 2019 ; Moreno et al., 2020 ; Moreno et al., 2021a ). For instance, it has been recently shown that the apocarotenoid zaxinone is involved in the modulation of plant growth and in regulating SLs level and arbuscular-mycorrhizal (AM) colonization in rice ( Figure 1 ), and SL and ABA levels in Arabidopsis ( Wang et al., 2019 ; Ablazov et al., 2020 ; Votta et al., 2022 ). Moreover, the volatile apocarotenoid β-ionone, usually released by leaves, contributes to the scent of flowers in many plants and plays an interesting role as a herbivore repellent in plant-insect interaction ( Figure 1 ) ( Ômura et al., 2000 ; Gruber et al., 2009 ; Moreno et al., 2021a ).…”

Metabolomics of plant root exudates: From sample preparation to data analysis

“…In addition, the carotenoid-derived plant hormones strigolactones (SLs) are important rhizosphere signals in the communication with arbuscular mycorrhizal (AM) fungi ( Fiorilli et al., 2019 ; Ito et al., 2022 ), while the AM symbiosis is also regulated by several carotenoid-derived signaling molecules, such as zaxinone and blumenols ( Wang et al., 2018 ; Wang et al., 2020 ; Wang et al., 2021 ). Notably, the biosynthesis and/or exudation of these specialized metabolites are highly correlated to nutrition deficiency, especially phosphate and nitrogen, suggesting the beneficial functions of plant-microbe interactions ( Fiorilli et al., 2019 ; Wang et al., 2020 ; Ablazov et al., 2022 ; Votta et al., 2022 ). However, SLs are also used by root parasitic plants, such as Striga that causes up-to 10 billion yield losses in Africa ( Jamil et al., 2022 ), to localize a suitable host and coordinate their germination with its presence ( Wang et al., 2022 ).…”