Abstract
Main conclusion
CYP722C from cotton, a homolog of the enzyme involved in orobanchol synthesis in cowpea and tomato, catalyzes the conversion of carlactonoic acid to 5-deoxystrigol.
Abstract
Strigolactones (SLs) are important phytohormones with roles in the regulation of plant growth and development. These compounds also function as signaling molecules in the rhizosphere by interacting with beneficial arbuscular mycorrhizal fungi and harmful root parasitic plants. Canonical SLs, such as 5-deoxystrigol (5DS), consist of a tricyclic lactone ring (ABC-ring) connected to a methylbutenolide (D-ring). Although it is known that 5DS biosynthesis begins with carlactonoic acid (CLA) derived from β-carotene, the enzyme that catalyzes the conversion of CLA remains elusive. Recently, we identified cytochrome P450 (CYP) CYP722C as the enzyme that catalyzes direct conversion of CLA to orobanchol in cowpea and tomato (Wakabayashi et al., Sci Adv 5:eaax9067, 2019). Orobanchol has a different C-ring configuration from that of 5DS. The present study aimed to characterize the homologous gene, designated GaCYP722C, from cotton (Gossypium arboreum) to examine whether this gene is involved in 5DS biosynthesis. Expression of GaCYP722C was upregulated under phosphate starvation, which is an SL-producing condition. Recombinant GaCYP722C was expressed in a baculovirus-insect cell expression system and was found to catalyze the conversion of CLA to 5DS but not to 4-deoxyorobanchol. These results strongly suggest that GaCYP722C from cotton is a 5DS synthase and that CYP722C is the crucial CYP subfamily involved in the generation of canonical SLs, irrespective of the different C-ring configurations.
This is a preview of subscription content, log in via an institution to check access.
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Abbreviations
- CCD7:
-
CAROTENOID CLEAVAGE DIOXYGENASE 7
- CCD8:
-
CAROTENOID CLEAVAGE DIOXYGENASE 8
- CLA:
-
Carlactonoic acid
- D27:
-
DWARF 27
- 4DO:
-
4-Deoxyorobanchol
- 5DS:
-
5-Deoxystrigol
- MAX1:
-
MORE AXIALLY GROWTH 1
- SLs:
-
Strigolactones
References
Abe S, Sado A, Tanaka K et al (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci USA 111:18084–18089. https://doi.org/10.1073/pnas.1410801111
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827. https://doi.org/10.1038/nature03608
Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186. https://doi.org/10.1146/annurev-arplant-043014-114759
Alder A, Jamil M, Marzorati M et al (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351. https://doi.org/10.1126/science.1218094
Cardoso C, Zhang Y, Jamil M et al (2014) Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci USA 111:2379–2384. https://doi.org/10.1073/pnas.1317360111
Cook CE, Whichard LP, Turner B et al (1966) Germination of witchweed (Striga lutea Lour.): Isolation and properties of a potent stimulant. Science 154:1189–1190. https://doi.org/10.1126/science.154.3753.1189
Gomez-Roldan V, Fermas S, Brewer PB et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194. https://doi.org/10.1038/nature07271
Iseki M, Shida K, Kuwabara K et al (2018) Evidence for species-dependent biosynthetic pathways for converting carlactone to strigolactones in plants. J Exp Bot 69:2305–2318. https://doi.org/10.1093/jxb/erx428
Madeira F, Park Y, Lee J et al (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47:W636–W641. https://doi.org/10.1093/nar/gkz268
Mizutani M, Ohta D (1998) Two isoforms of NADPH:cytochrome P450 reductase in Arabidopsis thaliana. Gene structure, heterologous expression in insect cells, and differential regulation. Plant Physiol 116:357–367. https://doi.org/10.1104/PP.116.1.357
Mori N, Nomura T, Akiyama K (2020a) Identification of two oxygenase genes involved in the respective biosynthetic pathways of canonical and non-canonical strigolactones in Lotus japonicus. Planta 251:40. https://doi.org/10.1007/s00425-019-03332-x
Mori N, Sado A, Xie X et al (2020b) Chemical identification of 18-hydroxycarlactonoic acid as an LjMAX1 product and in planta conversion of its methyl ester to canonical and non-canonical strigolactones in Lotus japonicus. Phytochemistry 174:112349. https://doi.org/10.1016/j.phytochem.2020.112349
Nelson D, Werck-Reichhart D (2011) A P450-centric view of plant evolution. Plant J 66:194–211. https://doi.org/10.1111/j.1365-313X.2011.04529.x
Saito S, Hirai N, Matsumoto C et al (2004) Arabidopsis CYP707As encode (+)-abscisic acid 8’-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol 134:1439–1449. https://doi.org/10.1104/pp.103.037614.1
Seto Y, Sado A, Asami K et al (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci USA 111:1640–1645. https://doi.org/10.1073/pnas.1314805111
Umehara M, Hanada A, Yoshida S et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200. https://doi.org/10.1038/nature07272
Wakabayashi T, Hamana M, Mori A et al (2019) Direct conversion of carlactonoic acid to orobanchol by cytochrome P450 CYP722C in strigolactone biosynthesis. Sci Adv 5:9067. https://doi.org/10.1126/sciadv.aax9067
Wang Y, Bouwmeester HJ (2018) Structural diversity in the strigolactones. J Exp Bot 69:2219–2230. https://doi.org/10.1093/jxb/ery091
Yoneyama K, Mori N, Sato T et al (2018a) Conversion of carlactone to carlactonoic acid is a conserved function of MAX1 homologs in strigolactone biosynthesis. New Phytol 218:1522–1533. https://doi.org/10.1111/nph.15055
Yoneyama K, Xie X, Yoneyama K et al (2018b) Which are the major players, canonical or non-canonical strigolactones? J Exp Bot 69:2231–2239. https://doi.org/10.1093/jxb/ery090
Zhang Y, Cheng X, Wang Y et al (2018) The tomato MAX1 homolog, SlMAX1, is involved in the biosynthesis of tomato strigolactones from carlactone. New Phytol 219:297–309. https://doi.org/10.1111/nph.15131
Zhang Y, van Dijk ADJ, Scaffidi A et al (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10:1028–1033. https://doi.org/10.1038/nchembio.1660
Zhu T, Liang C, Meng Z et al (2017) CottonFGD: an integrated functional genomics database for cotton. BMC Plant Biol 17:101. https://doi.org/10.1186/s12870-017-1039-x
Acknowledgements
This work was supported, in part, by JST/JICA SATREPS (JPMJSA1607 to YS) and JSPS KAKENHI (25292065 and 19H02897 to YS).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Fig. S1
Sequence comparison of the transcript of the cloned GaCYP722C with Ga12G2447.1 from the Cotton Functional Genomics database. Supplementary Fig. S2 Alignment of amino acid sequences of CYP722C from cotton, tomato, cowpea and L. japonicus. Sequences were aligned using CLUSTAL Omega program. (DOCX 1034 kb)
Rights and permissions
About this article
Cite this article
Wakabayashi, T., Shida, K., Kitano, Y. et al. CYP722C from Gossypium arboreum catalyzes the conversion of carlactonoic acid to 5-deoxystrigol. Planta 251, 97 (2020). https://doi.org/10.1007/s00425-020-03390-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-020-03390-6