The negative regulator SMAX1 controls mycorrhizal symbiosis and strigolactone biosynthesis in rice

Abstract

Most plants associate with beneficial arbuscular mycorrhizal (AM) fungi that facilitate soil nutrient acquisition. Prior to contact, partner recognition triggers reciprocal genetic remodelling to enable colonisation. The plant Dwarf14-Like (D14L) receptor conditions pre-symbiotic perception of AM fungi, and also detects the smoke constituent karrikin. D14L-dependent signalling mechanisms, underpinning AM symbiosis are unknown. Here, we present the identification of a negative regulator from rice, which operates downstream of the D14L receptor, corresponding to the homologue of the Arabidopsis thaliana Suppressor of MAX2-1 (AtSMAX1) that functions in karrikin signalling. We demonstrate that rice SMAX1 is a suppressor of AM symbiosis, negatively regulating fungal colonisation and transcription of crucial signalling components and conserved symbiosis genes. Similarly, rice SMAX1 negatively controls strigolactone biosynthesis, demonstrating an unexpected crosstalk between the strigolactone and karrikin signalling pathways. We conclude that removal of SMAX1, resulting from D14L signalling activation, de-represses essential symbiotic programmes and increases strigolactone hormone production.

Karrikin Signaling Acts Parallel to and Additively with Strigolactone Signaling to Regulate Rice Mesocotyl Elongation in Darkness

“…D53 has been revealed to act downstream of D14 and D3 and regulate the shoot branching of rice (Jiang et al, 2013;Zhou et al, 2013). By contrast, OsSMAX1 acts downstream of D14L and D3 to regulate root colonization by AM fungi and the elongation of the mesocotyl in rice (Choi et al, 2020). In this study, we show that OsSMAX1 acts downstream of D14L and D3 and parallel to D14-D3-D53 in regulation the elongation of the mesocotyl.…”

“…However, the genes involved in CSSP downstream of OsCERK1 were found to be upregulated in Ossmax1 (Choi et al, 2020). It seems that the karrikin signaling pathway plays an essential role in coordinating with CSSP and SL signaling during AM symbiosis.…”

“…Notably, the expression of a MAX1 homolog in rice (Os01g0700900), which is referred to as both LOC_Os01g50520 and LOC01g50530 (Cardoso et al, 2014, Zhang et al, 2014, was downregulated in the d14, d14l, d14 d14l and d3 mutants as well as in D53m-OE and OsSMAX1m-OE transgenic seedlings but was upregulated in the Ossmax1, Ossmax1 d14, and Ossmax1 d3 seedlings ( Figure 7E). Therefore, OsSMAX1 negatively regulates SL biosynthesis, suggesting an alternative mechanism of the cross-talk between the SL pathway and KL pathway (Choi et al, 2020).…”

“…To reveal how karrikin signaling mediates the communication between plants and AM fungi requires intensive further investigation. The signaling paradigm of karrikin strongly suggests that several unidentified chemicals play roles in AM symbiosis (Choi et al, 2020). The recent discovery of zaxinone synthase (ZAS) (Wang et al, 2019) and β-cyclocitral (Dickinson et al, 2019) and their roles in rice root development and stress adaptation indicated that apocarotenoid-derived small molecules might be candidates for the KL molecule that regulates mesocotyl development and/or symbiosis between plant and AM fungi.…”

Phytohormone production by the arbuscular mycorrhizal fungus Rhizophagus irregularis

“…Lipochitooligosaccharides (LCOs) and chitooligosaccharides (COs) are released by germinating spores of AM fungi and stimulate the initiation of the symbiosis via the activation of the common symbiosis signalling pathway and the activation of lateral root formation [16][17][18]; and a plant exporter of N-acetylglucosamine has been shown to be required for the first steps of the interaction [19]. Finally, additional, yet unidentified, signals of plant or fungal origin may act prior to root colonization [20][21][22][23].…”