Carotenoid biosynthesis drives root plasticity through aerenchyma and iron plaque formation in rice

nature plants Article https://doi.org/10.1038/s41477-025-02170-y Carotenoid biosynthesis drives root plasticity through aerenchyma and iron plaque formation in rice Received: 17 February 2025 Accepted: 13 November 2025 Published online: 2 January 2026 Jeevan Kumar Shrestha 1,2,3, Chih-Yu Lin1, Jian You Wang 1,4,5, I-Chien Tang1, Chun-Hao Hu1, Munkhtsetseg Tsednee 1, Yasha Zhang6, Muhammad Jamil 4,5, Lamis Berqdar 4, Ikram Blilou5,6, Salim Al-Babili 4,5,6, Chang-Sheng Wang7 & Kuo-Chen Yeh 1,2,8 Check for updates Rice roots develop aerenchyma, which transports oxygen from shoots to roots, facilitating adaptation to waterlogged conditions. This oxygen oxidizes ferrous ions into ferric compounds, forming iron plaque that mitigates iron toxicity. However, the molecular mechanisms linking aerenchyma and iron plaque formation remain poorly understood. Here we identified a rice mutant (AZ1302) defective in both aerenchyma and iron plaque formation, with the causal mutation mapped to the PHYTOENE SYNTHASE 2 (OsPSY2) gene. CRISPR–Cas9-induced psy2 mutants exhibited reduced levels of carotenoid-derived hormones, strigolactones and abscisic acid, in roots. In psy2 mutants, exogenous application of strigolactones rescued aerenchyma formation, while abscisic acid restored iron plaque deposition, providing evidence for distinct hormonal regulatory functions in the two processes. These findings revise the current understanding by dissociating the roles of aerenchyma and iron plaque formation, establishing a role for OsPSY2 in integrating hormonal signalling to drive root plasticity and offering new insights into plant adaptation under environmental stress. Rice (Oryza sativa L.) is a staple cereal crop that sustains over half of the global population, and its growth and productivity are highly sensitive to environmental fluctuations. The ability of rice roots to modify their architecture in response to stress, known as root plasticity, is essential for adapting to challenges such as nutrient imbalances1 and water availability extremes2. Rice roots adapt to environmental stress through vital mechanisms such as the formation of aerenchyma and the deposition of iron plaque. Deciphering the molecular mechanisms of aerenchyma and iron plaque formation could offer new strategies to enhance stress resilience and improve rice resilience in challenging agroecological conditions. Most plants struggle to survive under waterlogged conditions due to oxygen deprivation and mineral toxicity. However, rice has evolved specialized root adaptations that allow it to thrive in waterlogged environments. One key adaptation is the formation of aerenchyma, a channel-like structure in the roots that facilitates oxygen transfer Present address: Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan. 2Molecular and Biological Agricultural Sciences Program, Taiwan International Graduate Program, Academia Sinica and National Chung Hsing University, Taipei, Taiwan. 3Graduate Institute of Biotechnology, National Chung Hsing University, Taichung, Taiwan. 4BioActives Lab, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia. 5 Centre of Excellence for Sustainable Food Security, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia. 6Plant Science Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia. 7 Department of Agronomy, National Chung Hsing University, Taichung, Taiwan. 8Biotechnology Center, National Chung Hsing University, Taichung, Taiwan. e-mail: 1 Nature Plants | Volume 12 | January 2026 | 179–190 179 Article from the shoots to the roots, enabling tolerance of anoxic conditions3. Another critical adaptation is the oxidation of ferrous ions (Fe2+) at the root surface, thereby causing the formation of reddish-brown ferric compounds known as iron plaque. This iron plaque not only protects rice from iron toxicity by sequestering excess Fe2+ on the root surface4 but also plays a role in regulating nutrient availability5 and interactions with soil microbes6. These observations suggest a functional relationship between aerenchyma formation and iron plaque deposition, as aerenchyma enhances oxygen transport to the roots, which is essential for the oxidative processes leading to iron plaque formation7. Despite its importance, the specific role of aerenchyma in facilitating iron plaque formation remains speculative and poorly understood. Aerenchyma formation is a constitutive feature of rice roots but can be enhanced by various environmental and physiological factors, including waterlogging8, hypoxia or ethylene9, and auxin signalling10. Ethylene activates respiratory burst oxidase homologue isoform H, which produces reactive oxygen species in the cortical cells11. When reactive oxygen species levels exceed the scavenging capacity of metallothioneins, programmed cell death occurs in cortical cells, leading to the creation of air spaces that form the aerenchyma12. The oxygen transported via aerenchyma to the root surface plays a pivotal role in oxidizing Fe2+ to Fe3+, driving the formation of iron plaque. However, despite extensive research on aerenchyma formation, its direct involvement in iron plaque deposition remains untested. For this purpose, we investigate a mutagenized population of the indica cultivar IR64 and identify PHYTOENE SYNTHASE 2 (OsPSY2) as a key regulator of aerenchyma and iron plaque formation in rice roots through genetic mapping of a mutant impaired in these traits. We demonstrate that OsPSY2 modulates the biosynthesis of strigolactones (SLs) and abscisic acid (ABA), which positively regulate aerenchyma formation and iron plaque deposition, respectively. Our results highlight the distinct regulation of these two traits, providing crucial insights into how rice adapts to waterlogged conditions and mitigates iron toxicity. Results A locus on chromosome 12 governs aerenchyma and iron plaque Iron plaque formation on rice roots was observed under lowland cultivation conditions but was markedly reduced in upland conditions (Fig. 1a). To elucidate the genetic mechanism controlling iron plaque formation, we screened mutants from a sodium azide (NaN3) induced mutagenized population of the IR64 cultivar in excess iron conditions. On the basis of visual observations, the mutants ‘413’, ‘419’, ‘654’ and AZ1302 exhibited reduced iron plaque formation specifically in adventitious roots. In contrast, iron plaque was not clearly detectable in the seminal roots of either wild-type or mutant plants (Fig. 1b,c and Extended Data Fig. 1a,b). Among these mutants, AZ1302 displayed additional impairments in radial oxygen loss (ROL) (Fig. 1d) and aerenchyma formation (Fig. 1e and Extended Data Fig. 1c), warranting detailed genetic investigation. Comparative phenotypic analysis between IR64, which retains normal aerenchyma formation, ROL and iron plaque for (...truncated)