An Ancestral Function of Strigolactones as Symbiotic Rhizosphere Signals

Abstract

In flowering plants, carotenoid-derived strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), a previously unidentified SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating that it is ancestral in land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders M. paleacea cells BSB-responsive. These results suggest that BSB is not perceived by M. paleacea cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.

Masks Start to Drop: Suppressor of MAX2 1-Like Proteins Reveal Their Many Faces

“…Despite the presence of the SL biosynthesis enzymes D27, CAROTENOID CLEAVAGE DIOXYGENASE (CCD) 7, CCD8, and MAX1 in most nonseed plants, the canonical SL receptor D14 is only found in seed plants ( Bythell-Douglas et al, 2017 ; Walker et al, 2019 ), leading to the assumption that SLs first acted as symbiotic signals in the rhizosphere, rather than as plant development-regulating phytohormones ( Kodama et al, 2021 ). Interestingly, most nonvascular land plants possess additional KAI2-like receptors, whereas in the moss P. patens , they appear to have evolved independently from D14 to act as SL receptors ( Bythell-Douglas et al, 2017 ; Lopez-Obando et al, 2021 ).…”

Plant–microbe interactions that have impacted plant terrestrializations

“…To determine whether the chemical dialog between plants and Glomeromycota is conserved across embryophytes, knock-out mutants for the two CCD8 paralogs observed in M. paleacea were generated by CRISPR/Cas9 and their symbiotic abilities scored. These ccd8 double mutants were found defective in AM symbiosis formation, a defect rescued by the exogenous application of synthetic strigolactones, in a similar manner as the angiosperm mutants ( Kodama et al, 2021 ).…”

“…Mutants in the strigolactone-biosynthesis gene called the carotenoid cleavage dioxygenase 8 ( CCD8 ) are affected in AM symbiosis establishment in both monocots and dicots ( Gomez-Roldan et al, 2008 ; Kobae et al, 2018 ). Strigolactones are also produced by bryophytes that are able to host AM fungi, including M. paleacea ( Delaux et al, 2012 ; Kodama et al, 2021 ), while non-AM hosts seem to have lost this ability ( Kodama et al, 2021 ). To determine whether the chemical dialog between plants and Glomeromycota is conserved across embryophytes, knock-out mutants for the two CCD8 paralogs observed in M. paleacea were generated by CRISPR/Cas9 and their symbiotic abilities scored.…”

Ancestral sequence reconstruction of the CYP711 family reveals functional divergence in strigolactone biosynthetic enzymes associated with gene duplication events in monocot grasses

“…The conversion of CL to CLA is a well‐conserved activity reported for all active CYP711As characterized so far. Although it has been speculated that CL was not the native substrate for the P450s ancestral to the CYP711 family (Wu et al ., 2021), it is the substrate for MpaCYP711A, which catalyzes the synthesis of bryosymbiol, an SL discovered in the early land plant M. paleacea (Kodama et al ., 2021) (Fig. 1).…”

“…The results presented here indicate that CYP711As probably played a fundamental role in the structural diversification of SLs before the development of angiosperms, a conclusion that is supported by the observations that CYP711As are responsible for 4DO synthesis in spikemoss ( Selaginella moellendorfii ) (Yoneyama et al ., 2018a) and the synthesis of bryosymbiol in the bryophyte M. paleacea (Kodama et al ., 2021). Notably all ancestors characterized here generated multiple hydroxylation products from GR24 (Fig.…”