Zaxinone synthase controls arbuscular mycorrhizal colonization level in rice.

Valentina Fiorilli, Luisa Lanfranco, Cristina Votta, Imran Haider, Jian You Wang, Raffaella Balestrini, Ivan Petřík, Danuše Tarkowská, Ondřej Novák, Akmaral Serikbayeva, Paola Bonfante, Salim Al-Babili

Journal: The Plant journal : for cell and molecular biology 2022;111(6):1688-1700

PMID: 35877598

Abstract

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.

© 2022 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Address: Department of Life Sciences and Systems Biology, University of Turin, Turin, 10125, Italy.; The BioActives Lab, Center for Desert Agriculture (CDA), Biological and Environment Science and Engineering (BESE), King Abdullah University of Science and Technology, Thuwal, 23955, Saudi Arabia.; National Research Council, Institute for Sustainable Plant Protection, Turin, 10135, Italy.; Laboratory of Growth Regulators, Faculty of Science, Palacký University and Institute of Experimental Botany, The Czech Academy of Sciences, Olomouc, 78371, Czech Republic.
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