KARRIKIN INSENSITIVE2 regulates leaf development, root system architecture and arbuscular-mycorrhizal symbiosis in Brachypodium distachyon

Authors: MENG, YONGJIE - University Of Western Australia; VARSHNEY, KARTIKYE - Technical University Of Munich; INCZE, NORBERT - Technical University Of Munich; BADICS, ESZLER - Eotvos Lorand University; KAMRAN, MUHAMMAD - University Of Western Australia; DAVIES, SABRINA - University Of Western Australia; OPPERMANN, LARISSA - University Of Western Australia; MAGNE, KEVIN - Inrae; DALMAIS, MARION - Inrae; BENDAHMANE, ABDEL - Inrae; SIBOUT, RICHARD - Agro Paris Tech; VOGEL, JOHN - US Department Of Energy; L Chingcuanco, Debbie; BOND, CHARLES - University Of Western Australia; SOOS, VILMOS - Eotvos Lorand University; GUTJAHR, CAROLINE - Technical University Of Munich; WATERS, MARK - University Of Western Australia

Submitted to: The Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/20/2021
Publication Date: 12/25/2021
Citation: Meng, Y., Varshney, K., Incze, N., Badics, E., Kamran, M., Davies, S., Oppermann, L.M., Magne, K., Dalmais, M., Bendahmane, A., Sibout, R., Vogel, J., Chingcuanco, D.L., Bond, C.S., Soos, V., Gutjahr, C., Waters, M. 2021. KARRIKIN INSENSITIVE2 regulates leaf development, root system architecture and arbuscular-mycorrhizal symbiosis in Brachypodium distachyon. The Plant Journal. 109(6):1559-1574. https://doi.org/10.1111/tpj.15651.
DOI: https://doi.org/10.1111/tpj.15651

Interpretive Summary: The symbiotic relationship between plants and arbuscular-mycorrhizal (AM) fungi results in plant acquisition of inorganic phosphates and nitrogen processed by fungi from mineral-poor soils in exchange for photosynthesis derived organic carbon. Chemical signals recognized by both partners are required for the establishment of successful symbiosis. One of these plant signals are the karrikins, butanolide compounds that stimulate seed germination from burn vegetation and hyphae branching of AM fungi promoting a symbiotic interaction. This paper dissected the function of KARRAKIN INSENSITIVE2 genes (kai2) in Brachypodium using phenotypic, transgenic, and transcriptomic analysis. Results suggest that KAI2-dependent signals condition the root into a permissive state for fungal colonization and may play a role in regulating the life span of AM symbiosis. Understanding the molecular mechanism of karrikin action will provide insights in developing strategies to improve crop nutrient acquisition especially when grown in marginal lands.

Technical Abstract: KARRIKIN INSENSITIVE2 (KAI2) is an a/ß-hydrolase required for plant responses to karrikins, which are abiotic butenolides that can influence seed germination and seedling growth. Although represented by four angiosperm species, loss-of-function kai2 mutants are phenotypically inconsistent and incompletely characterised, resulting in uncertainties about the core functions of KAI2 in plant development. Here we characterised the developmental functions of KAI2 in the grass Brachypodium distachyon using molecular, physiological and biochemical approaches. Bdkai2 mutants exhibit increased internode elongation and reduced leaf chlorophyll levels, but only a modest increase in water loss from detached leaves. Bdkai2 shows increased numbers of lateral roots and reduced root hair growth, and fails to support normal root colonisation by arbuscular-mycorrhizal (AM) fungi. The karrikins KAR1 and KAR2, and the strigolactone (SL) analogue rac-GR24, each elicit overlapping but distinct changes to the shoot transcriptome via BdKAI2. Finally, we show that BdKAI2 exhibits a clear ligand preference for desmethyl butenolides and weak responses to methyl-substituted SL analogues such as GR24. Our findings suggest that KAI2 has multiple roles in shoot development, root system development and transcriptional regulation in grasses. Although KAI2-dependent AM symbiosis is likely conserved within monocots, the magnitude of the effect of KAI2 on water relations may vary across angiosperms.