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 wild-type 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.

Department of Life Sciences and Systems Biology University of Turin Turin 10125 Italy

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany The Czech Academy of Sciences Olomouc 78371 Czech Republic

National Research Council Institute for Sustainable Plant Protection Turin 10135 Italy

The BioActives Lab Center for Desert Agriculture King Abdullah University of Science and Technology Thuwal 23955 Saudi Arabia

Zobrazit více v PubMed

Ablazov, A. , Mi, J. , Jamil, M. , Jia, K.P. , Wang, J.Y. , Feng, Q. et al. (2020) The apocarotenoid zaxinone is a positive regulator of strigolactone and abscisic acid biosynthesis in arabidopsis roots. Frontiers in Plant Science, 11, 578. 10.3389/fpls.2020.00578 PubMed DOI PMC

Akiyama, K. , Matsuzaki, K. & Hayashi, H. (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 435, 824–827. PubMed

Balestrini, R. , Estanyol, M.J. , Puigdoménech, P. & Bonfante, P. (1997) Hydroxyproline‐rich glycoprotein mRNA accumulation in maize root cells colonized by an arbuscular mycorrhizal fungus as revealed by in situ hybridization. Protoplasma, 198, 36–42.

Balestrini, R. , Gómez‐Ariza, J. , Lanfranco, L. & Bonfante, P. (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Molecular Plant‐Microbe Interactions, 20, 1055–1062. PubMed

Besserer, A. , Bécard, G. , Jauneau, A. , Roux, C. & Séjalon‐Delmas, N. (2008) GR24, a synthetic analogue of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiology, 148, 402–413. PubMed PMC

Besserer, A. , Puech‐Pagès, V. , Kiefer, P. , Gomez‐Roldan, V. , Jauneau, A. , Roy, S. et al. (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology, 4, e226. PubMed PMC

Butt, H. , Jamil, M. , Wang, J.Y. , Al‐Babili, S. & Mahfouz, M. (2018) Engineering plant architecture via CRISPR/Cas9‐mediated alteration of strigolactone biosynthesis. BMC Plant Biology, 18, 174. PubMed PMC

Carotenuto, G. , Chabaud, M. , Miyata, K. , Capozzi, M. , Takeda, N. , Kaku, H. , et al. (2017) The rice LysM receptor-like kinasesOsCERK1 is required for the perception of short-chain chitin oligomers in arbuscularmycorrhizal signaling. New Phytologist, 214, 1440–1446. PubMed

Charpentier, M. , Sun, J. , Wen, J. , Mysore, K.S. & Oldroyd, G.E.D. (2014) Abscisic acid promotion of arbuscular mycorrhizal colonization requires a component of the PROTEIN PHOSPHATASE 2A complex. Plant Physiology, 166, 2077–2090. PubMed PMC

Chen, M. , Arato, M. , Borghi, L. , Nouri, E. & Reinhardt, D. (2018) Beneficial services of arbuscular mycorrhizal fungi – from ecology to application. Frontiers in Plant Science, 9, 1270. PubMed PMC

Choi, J. , Lee, T. , Cho, J. , Servante, E.K. , Pucker, B. , Summers, W. et al. (2020) The negative regulator SMAX1 controls mycorrhizal symbiosis and strigolactone biosynthesis in rice. Nature Communications, 11, 2114. PubMed PMC

Crosino, A. , Moscato, E. , Blangetti, M. , Carotenuto, G. , Spina, F. , Bordignon, S. et al. (2021) Extraction of short chain chitooligosaccharides from fungal biomass and their use as promoters of arbuscular mycorrhizal symbiosis. Scientific Reports, 11, 3798. PubMed PMC

Das, D. , Paries, M. , Hobecker, K. , Gigl, H. , Dawid, C. , Lam, H.M. et al. (2021) Phosphate starvation response enables arbuscular mycorrhiza symbiosis. bioRxiv preprint 10.1101/2021.11.05.467437 PubMed DOI PMC

Felemban, A. , Braguy, J. , Zurbriggen, M.D. & Al‐Babili, S. (2019) Apocarotenoids Involved in Plant Development and Stress Response. Frontiers in Plant Science, 10, 1168. 10.3389/fpls.2019.01168 PubMed DOI PMC

Fiorilli, V. , Vallino, M. , Biselli, C. , Faccio, A. , Bagnaresi, P. & Bonfante, P. (2015) Host and non‐host roots in rice: cellular and molecular approaches reveal differential responses to arbuscular mycorrhizal fungi. Frontiers in Plant Science, 6, 636. PubMed PMC

Fiorilli, V. , Wang, J.Y. , Bonfante, P. , Lanfranco, L. & Al‐Babili, S. (2019) Apocarotenoids: old and new mediators of the arbuscular mycorrhizal symbiosis. Frontiers in Plant Science, 10, 1186. PubMed PMC

Floss, D.S. , Levy, J.G. , Levesque‐Tremblay, V. , Pumplin, N. & Harrison, M.J. (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proceeding of the National Academy of Science U S A, 110, E5025–E5034. PubMed PMC

Genre, A. , Chabaud, M. , Balzergue, C. , Puech‐Pagès, V. , Novero, M. , Rey, T. et al. (2013) Short‐chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist, 198, 190–202. PubMed

Genre, A. , Lanfranco, L. , Perotto, S. & Bonfante, P. (2020) Unique and common traits in mycorrhizal symbioses. Nature Review Microbiology, 18, 649–660. PubMed

Giovannetti, M. , Mari, A. , Novero, M. & Bonfante, P. (2015) Early Lotus japonicus root transcriptomic responses to symbiotic and pathogenic fungal exudates. Frontiers in Plant Science, 6, 480. PubMed PMC

Giuliano, G. , Al‐Babili, S. & von Lintig, J. (2003) Carotenoid oxygenases: cleave it or leave it. Trends in Plant Science, 8, 145–149. PubMed

Güimil, S. , Chang, H.S. , Zhu, T. , Sesma, A. , Osbourn, A. , Roux, C. et al. (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proceeding of the National Academy of Science U S A, 102, 8066–8070. PubMed PMC

Gutjahr, C. , Gobbato, E. , Choi, J. , Riemann, M. , Johnston, M.G. , Summers, W. et al. (2015) Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science, 350, 1521–1524. PubMed

Gutjahr, C. & Parniske, M. (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell and Developmental Biology, 29, 593–617. PubMed

Hammer, Ø. , Harper, D.A.T. & Ryan, P.D. (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 9.

Harrison, M.J. , Dewbre, G.R. & Liu, J. (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. The Plant Cell, 14, 2413–2429. PubMed PMC

Herrera‐Medina, M.J. , Steinkellner, S. , Vierheilig, H. , Ocampo Bote, J.A. & García Garrido, J.M. (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytologist, 175, 554–564. PubMed

Hill, E.M. , Robinson, L.A. , Abdul‐Sada, A. , Vanbergen, A.J. , Hodge, A. & Hartley, S.E. (2018) Arbuscular mycorrhizal fungi and plant chemical defence: effects of colonisation on aboveground and belowground metabolomes. Journal of Chemical Ecology., 44, 198–208. PubMed PMC

Hou, X. , Rivers, J. , León, P. , McQuinn, R.P. & Pogson, B.J. (2016) Synthesis and function of apocarotenoid signals in plants. Trends in Plant Science, 21, 792–803. PubMed

Kobae, Y. , Kameoka, H. , Sugimura, Y. , Saito, K. , Ohtomo, R. , Fujiwara, T. et al. (2018) Strigolactone biosynthesis genes of rice are required for the punctual entry of arbuscular mycorrhizal fungi into the roots. Plant Cell Physiology, 59, 544–553. PubMed

Lanfranco, L. , Fiorilli, V. & Gutjahr, C. (2018) Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis. New Phytologist, 220, 1031–1046. PubMed

Lanfranco, L. , Fiorilli, V. , Venice, F. & Bonfante, P. (2018) Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. Jornal of Experimental Botany, 69, 2175–2188. PubMed

Liao, D. , Wang, S. , Cui, M. , Liu, J. , Chen, A. & Xu, G. (2018) Phytohormones regulate the development of arbuscular mycorrhizal symbiosis. International Journal of Molecular Sciences, 19, 3146. PubMed PMC

López‐Ráez, J.A. , Fernández, I. , García, J.M. , Berrio, E. , Bonfante, P. , Walter, M.H. et al. (2015) Differential spatio‐temporal expression of carotenoid cleavage dioxygenases regulates apocarotenoid fluxes during AM symbiosis. Plant Science, 230, 59–69. PubMed

Ma, Y. , Cao, J. , He, J. , Chen, Q. , Li, X. & Yang, Y. (2018) Molecular mechanism for the regulation of ABA homeostasis during plant development and stress responses. International Journal of Molecular Sciences, 19, 3643. PubMed PMC

MacLean, A.M. , Bravo, A. & Harrison, M.J. (2017) Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. The Plant Cell, 29, 2319–2335. PubMed PMC

Martín‐Rodríguez, J.A. , Huertas, R. , Ho‐Plágaro, T. , Ocampo, J.A. , Turečková, V. , Tarkowská, D. et al. (2016) Gibberellin–abscisic acid balances during arbuscular mycorrhiza formation in tomato. Frontiers of Plant Science, 7, 1273. PubMed PMC

Martín‐Rodríguez, J.A. , León‐Morcillo, R. , Vierheilig, H. , Ocampo, J.A. , Ludwig‐Müller, J. & García‐Garrido, J.M. (2011) Ethylene‐dependent/ethylene‐independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytologist, 190, 193–205. PubMed

Moise, A. , Vonlintig, J. & Palczewski, K. (2005) Related enzymes solve evolutionarily recurrent problems in the metabolism of carotenoids. Trends in Plant Science, 10, 178–186. PubMed

Moreno, J.C. , Mi, J. , Alagoz, Y. & Al‐Babili, S. (2021) Plant apocarotenoids: from retrograde signaling to interspecific communication. The Plant Journal, 105, 351–375. PubMed PMC

Müller, L.M. & Harrison, M.J. (2019) Phytohormones, miRNAs, and peptide signals integrate plant phosphorus status with arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology, 50, 132–139. PubMed

Paszkowski, U. , Kroken, S. , Roux, C. & Briggs, S.P. (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proceeding of the National Academy of Science U S A, 99, 13324–13329. PubMed PMC

Peleg, Z. & Blumwald, E. (2011) Hormone balance and abiotic stress tolerance in crop plants. Current Opinion in Plant Biology, 14, 290–295. PubMed

Pozo, M.J. , López‐Ráez, J.A. , Azcón‐Aguilar, C. & García‐Garrido, J.M. (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytologist, 205, 1431–1436. PubMed

Rademacher, W. (2000) Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 501–531. PubMed

Rich, M.K. , Nouri, E. , Courty, P.E. & Reinhardt, D. (2017) Diet of arbuscular mycorrhizal fungi: bread and butter? Trends in Plant Science, 22, 652–660. PubMed

Rillig, M. , Aguilar‐Trigueros, C.A. , Camenzind, T. , Cavagnaro, T.R. , Degrune, F. , Hohmann, P. et al. (2019) Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytologist, 222, 1171–1175. PubMed

Rizza, A. & Jones, A.M. (2019) The makings of a gradient: spatiotemporal distribution of gibberellins in plant development. Current Opinion in Plant Biology, 47, 9–15. PubMed PMC

Shi, J. , Zhao, B. , Zheng, S. , Zhang, X. , Wang, X. , Dong, W. et al. (2021) A phosphate starvation response‐centered network regulates mycorrhizal symbiosis. Cell 28, 184(22), 5527‐5540.e18. PubMed

Šimura, J. , Antoniadi, I. , Široká, J. , Tarkowská, D. , Strnad, M. , Ljung, K. et al. (2018) Plant hormonomics: multiple phytohormone profiling by targeted metabolomics. Plant Physiology, 177, 476–489. PubMed PMC

Spatafora, J.W. , Chang, Y. , Benny, G.L. , Lazarus, K. , Smith, M.E. , Berbee, M.L. et al. (2016) A phylum‐level phylogenetic classification of zygomycete fungi based on genome‐scale data. Mycologia, 108, 1028–1046. PubMed PMC

Ton, J. , Flors, V. & Mauch‐Mani, B. (2009) The multifaceted role of ABA in disease resistance. Trends in Plant Science, 14, 310–317. PubMed

Trouvelot, A. , Kough, J. & Gianinazzi‐Pearson, V. (1986) Evaluation of VA infection levels in root systems. Research for estimation methods having a functional significance. In: Gianinazzi‐Pearson, V. & Gianinazzi, S. (Eds.) Physiological and Genetical Aspects of Mycorrhizae. France: INRAPress, pp. 217–221.

Vallino, M. , Fiorilli, V. & Bonfante, P. (2014) Rice flooding negatively impacts root branching and arbuscular mycorrhizal colonization, but not fungal viability. Plant Cell Environment, 37, 557–572. PubMed

Volpe, V. , Giovannetti, M. , Sun, X.G. , Fiorilli, V. & Bonfante, P. (2016) The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non mycorrhizal roots: Characterization of AM‐induced Pi transporters. Plant Cell Environment, 39, 660–671. PubMed

Volpe, V. , Carotenuto, G. , Berzero, C. , Cagnina, L. , Puech-Pagès, V. & Genre, A. (2020) Short chainchito-oligosaccharides promote arbuscular mycorrhizal colonization in Medicagotruncatula. Carbohydrate Polymers, 229. 115505 PubMed

Walter, M.H. , Floß, D.S. , Hans, J. , Fester, T. & Strack, D. (2007) Apocarotenoid biosynthesis in arbuscular mycorrhizal roots: contributions from methylerythritol phosphate pathway isogenes and tools for its manipulation. Phytochemistry, 68, 130–138. PubMed

Wang, J.Y. , Haider, I. , Jamil, M. , Fiorilli, V. , Saito, Y. , Mi, J. et al. (2019) The apocarotenoid metabolite zaxinone regulates growth and strigolactone biosynthesis in rice. Nature Communications, 10, 810. PubMed PMC

Wang, J.Y. , Jamil, M. , Lin, P.Y. , Ota, T. , Fiorilli, V. , Novero, M. et al. (2020) Efficient mimics for elucidating zaxinone biology and promoting agricultural applications. Molecular Plant, 13, 1654–1661. PubMed PMC

Wang, J.Y. , Lin, P.Y. & Al‐Babili, S. (2021) On the biosynthesis and evolution of apocarotenoid plant growth regulators. Seminars in Cell and Devlopmental Biology, 109, 3–11. PubMed

Wang, M. , Schäfer, M. , Li, D. , Halitschke, R. , Dong, C. , McGale, E. et al. (2018) Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi. eLife, 7, e37093. PubMed PMC

Yang, S.Y. , Grønlund, M. , Jakobsen, I. , Grotemeyer, M.S. , Rentsch, D. , Miyao, A. et al. (2012) Non redundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. The Plant Cell, 24, 4236–4251. PubMed PMC

The SlDLK2 receptor, involved in the control of arbuscular mycorrhizal symbiosis, regulates hormonal balance in roots