Control of Adventitious Root Architecture in Rice by Darkness, Light, and Gravity

Abstract

ORCID IDs: 0000-0002-3607-6133 (C.L.); 0000-0002-7370-643X (M.S.).Rice (Oryza sativa) is a semiaquatic plant that is well adapted to partial flooding. Rice stems develop adventitious root (AR) primordia at each node that slowly mature but emerge only when the plant gets flooded, leading to the formation of a whole new secondary root system upon flooding. AR growth is induced by ethylene that accumulates in submerged plant tissues due to its lowered diffusion rate in water. Here, we report that the architecture of the secondary root system in flooded rice plants is controlled not only by altered gas diffusion but also by gravity and light. While ethylene promotes the emergence and growth of ARs, gravity and light determine their gravitropic setpoint angle (i.e. the deviation of growth direction relative to vertical). ARs grow upward at about 120°in the dark and downward at 54°in the light. The upward growth direction is conserved in indica and japonica rice varieties, suggestive of a conserved trait in rice. Experiments with a klinostat and with inverted stem orientation revealed that gravity promotes upward growth by about 10°. Red, far-red, and blue light lead to negative phototropism in a dose-dependent manner, with blue light being most effective, indicating that phytochrome and blue light signaling control AR system architecture. The cpt1 (coleoptile phototropism1) mutant, which lacks one of the phototropin-interacting CPT proteins, shows reduced sensitivity to blue light. Hence, the gravitropic setpoint angle of rice ARs is controlled by genetic and environmental factors that likely balance the need for oxygen supply (upward growth) with avoidance of root desiccation (downward growth).

Hypoxia and the group VII ethylene response transcription factor HRE2 promote adventitious root elongation inArabidopsis

“…Adventitious root growth in rice is a well‐known adaptive trait for survival under prolonged flooding that is primarily regulated by ethylene (Lorbiecke & Sauter ; Lin & Sauter ). However, apart from favouring ethylene accumulation, flooding causes O 2 deprivation that also acts as a submergence signal.…”

“…Letters in (C, D) indicate statistically different values (Kruskal-Wallis test, n C2H4 = 20-31, n MCP = 20-28, P < 0.05). regulated by ethylene (Lorbiecke & Sauter 1999;Lin & Sauter 2018). However, apart from favouring ethylene accumulation, flooding causes O 2 deprivation that also acts as a submergence signal.…”

“…Future work may clarify if the sensitivity to ethylene changes under hypoxia. In contrast to Arabidopsis, ethylene has a promotive effect on AR emergence and growth in several flood-tolerant species including rice (Lorbiecke & Sauter 1999;Lin & Sauter 2018). The contrasting regulation of ARs by ethylene may reflect different adaptive strategies in flooding-tolerant rice compared to moderately tolerant A. thaliana (Vashisht et al 2011).…”

Tolerant mechanisms to O2 deficiency under submergence conditions in plants

“…This is because they do not form subsequent ARs when exposed to long-term severe anaerobic stress associated with high ethylene accumulation. In contrast to Arabidopsis, ethylene has promotive effects on the AR emergence and growth in several wetland species including rice (Lin and Sauter 2018). The contrasting regulation of ethylene on ARs may reflect the different adaptive strategies between the flood-tolerant and intolerant species (Fig.…”

The Dynamic Plant: Capture, Transformation, and Management of Energy

“…These roots need to be near to the air-water interface to be well aerated. Remarkably, the young adventitious roots of partially submerged rice display strong upward growth due to a change in gravitational setpoint in the dark, but not in R, FR, or blue light (Lin and Sauter, 2018).…”