Strigolactones (SLs) are a class of plant hormones which regulate shoot branching and function as host recognition signals for symbionts and parasites in the rhizosphere. However, steps in SL biosynthesis after carlactone (CL) formation remain elusive. This study elucidated the common and diverse functions of MAX1 homologs which catalyze CL oxidation. We have reported previously that ArabidopsisMAX1 converts CL to carlactonoic acid (CLA), whereas a rice MAX1 homolog has been shown to catalyze the conversion of CL to 4-deoxyorobanchol (4DO). To determine which reaction is conserved in the plant kingdom, we investigated the enzymatic function of MAX1 homologs in Arabidopsis, rice, maize, tomato, poplar and Selaginella moellendorffii. The conversion of CL to CLA was found to be a common reaction catalyzed by MAX1 homologs, and MAX1s can be classified into three types: A1-type, converting CL to CLA; A2-type, converting CL to 4DO via CLA; and A3-type, converting CL to CLA and 4DO to orobanchol. CLA was detected in root exudates from poplar and Selaginella, but not ubiquitously in other plants examined in this study, suggesting its role as a species-specific signal in the rhizosphere. This study provides new insights into the roles of MAX1 in endogenous and rhizosphere signaling.
Summary
Root parasitic plants such as Striga, Orobanche, and Phelipanche spp. cause serious damage to crop production world‐wide. Deletion of the Low Germination Stimulant 1 (LGS1) gene gives a Striga‐resistance trait in sorghum (Sorghum bicolor). The LGS1 gene encodes a sulfotransferase‐like protein, but its function has not been elucidated.
Since the profile of strigolactones (SLs) that induce seed germination in root parasitic plants is altered in the lgs1 mutant, LGS1 is thought to be an SL biosynthetic enzyme. In order to clarify the enzymatic function of LGS1, we looked for candidate SL substrates that accumulate in the lgs1 mutants and performed in vivo and in vitro metabolism experiments.
We found the SL precursor 18‐hydroxycarlactonoic acid (18‐OH‐CLA) is a substrate for LGS1. CYP711A cytochrome P450 enzymes (SbMAX1 proteins) in sorghum produce 18‐OH‐CLA. When LGS1 and SbMAX1 coding sequences were co‐expressed in Nicotiana benthamiana with the upstream SL biosynthesis genes from sorghum, the canonical SLs 5‐deoxystrigol and 4‐deoxyorobanchol were produced.
This finding showed that LGS1 in sorghum uses a sulfo group to catalyze leaving of a hydroxyl group and cyclization of 18‐OH‐CLA. A similar SL biosynthetic pathway has not been found in other plant species.
Strigolactones (SLs) are a plant hormone inhibiting shoot branching/tillering and a rhizospheric, chemical signal that triggers seed germination of the noxious root parasitic plant
Striga
and mediates symbiosis with beneficial arbuscular mycorrhizal fungi. Identifying specific roles of canonical and noncanonical SLs, the two SL subfamilies, is important for developing
Striga
-resistant cereals and for engineering plant architecture. Here, we report that rice mutants lacking canonical SLs do not show the shoot phenotypes known for SL-deficient plants, exhibiting only a delay in establishing arbuscular mycorrhizal symbiosis, but release exudates with a significantly decreased
Striga
seed–germinating activity. Blocking the biosynthesis of canonical SLs by TIS108, a specific enzyme inhibitor, significantly lowered
Striga
infestation without affecting rice growth. These results indicate that canonical SLs are not the determinant of shoot architecture and pave the way for increasing crop resistance by gene editing or chemical treatment.
The plant hormones strigolactones (SLs) regulate shoot branching and mediate the communication with symbiotic mycorrhizal fungi, but also with noxious root parasitic weeds, such as Striga spp. SLs derive from carlactone (CL) and are divided structurally into canonical and non-canonical SLs. However, the questions about particular biological functions of the two groups and the identification of the SL that inhibits shoot branching are still unanswered, hampering targeted modification of SL pattern towards improving plant architecture and resistance against Striga. Here, we reported that 4-deoxyorobanchol (4DO) and orobanchol, the two canonical SLs in rice, do not have major role in determining rice shoot architecture. CRISPR/Cas9 mediated Osmax1-900 mutants, lacking these two SLs, do not show the high tillering and dwarf phenotype typical for SL-deficient plants. However, the absence of 4DO and orobanchol in root exudates significantly decreased their capability in inducing Striga seed germination, while caused only a delay in root colonization by mycorrhizal fungi. To confirm the genetic evidence, we used the SL-biosynthesis inhibitor TIS108. Our results showed that TIS108 is a MAX1-specific inhibitor that lowers 4DO and orobanchol synthesis, conferring a resistance to Striga without a severe impact on rice architecture. Hence, our work uncovers the specific function of canonical SLs as rhizospheric signals and paves the way for establishing chemical and genetic based approaches for combating the root parasitic weeds, by targeted depletion of their release.
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.
In flowering plants, 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), an SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating its origin in the common ancestor of 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.
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