Light‐dependent activation of HY5 promotes mycorrhizal symbiosis in tomato by systemically regulating strigolactone biosynthesis

• Published in: The New phytologist Vol. 233; no. 4; pp. 1900 - 1914
• Main Authors: Ge, Shibei, He, Liqun, Jin, Lijuan, Xia, Xiaojian, Li, Lan, Ahammed, Golam Jalal, Qi, Zhenyu, Yu, Jingquan, Zhou, Yanhong
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.02.2022
• Subjects: Accumulation; Agrochemicals; arbuscular mycorrhizal fungi (AMFs); Arbuscular mycorrhizas; Biosynthesis; Carotenoids; Chemical fertilizers; Chromatin; chromatin immunoprecipitation; Colonization; Dioxygenase; Electrophoretic mobility; Fertilizers; Fungi; gel electrophoresis; Genes; Heterocyclic Compounds, 3-Ring; Immunoprecipitation; Lactones - metabolism; Light; Light quality; light signaling; Lycopersicon esculentum - genetics; Mineral nutrients; Mycorrhizae - physiology; Nutrient utilization; Phosphates; phosphorus uptake; phytochrome; Phytochrome B; Plant roots; Plant Roots - metabolism; Pollution; Proteins; red light; Roots; Signal transduction; Signal transmission; Signaling; strigolactone; strigolactones; Symbiosis; systemic signaling; tomato (Solanum lycopersicum); Tomatoes; Transcription; Uptake; vesicular arbuscular mycorrhizae; tomato (Solanum lycopersicum); arbuscular mycorrhizal fungi (AMFs); light signaling; phosphorus uptake; strigolactone; systemic signaling
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.17883

Summary Light quality affects mutualisms between plant roots and arbuscular mycorrhizal fungi (AMFs), which modify nutrient acquisition in plants. However, the mechanisms by which light systemically modulates root colonization by AMFs and phosphate uptake in roots remain unclear. We used a range of approaches, including grafting techniques, protein immunoblot analysis, electrophoretic mobility shift assay, chromatin immunoprecipitation, and dual‐luciferase assays, to unveil the molecular basis of light signal transmission from shoot to root that mediates arbuscule development and phosphate uptake in tomato. The results show that shoot phytochrome B (phyB) triggers shoot‐derived mobile ELONGATED HYPOCOTYL5 (HY5) protein accumulation in roots, and HY5 further positively regulates transcription of strigolactone (SL) synthetic genes, thus forming a shoot phyB‐dependent systemic signaling pathway that regulates the synthesis and accumulation of SLs in roots. Further experiments with carotenoid cleavage dioxygenase 7 mutants and supplementary red light confirm that SLs are indispensable in the red‐light‐regulated mycorrhizal symbiosis in roots. Our results reveal a phyB–HY5–SLs systemic signaling cascade that facilitates mycorrhizal symbiosis and phosphate utilization in plants. The findings provide new prospects for the potential application of AMFs and light manipulation to effectively improve nutrient utilization and minimize the use of chemical fertilizers and associated pollution.