Abstract

In plants, the root system plays many important roles, including anchorage, water, and mineral uptake, and responding to environmental signals. The mechanisms underlying root system development are complex and involve many phytohormones of which auxin is the most important one. However, the role of plant stress hormone Jasmonic acid in root development remained elusive. Here, we report that Jasmonic acid promotes crown root development in rice by regulating OsGER4, a Germin-like protein. This gene was discovered by a Genome-Wide Association Study while observing the increase of crown root under Jasmonic acid-stimulated stress. OsGER4 was confirmed to be a hormone-responsive gene involved in various stress responses and its expression coincided with the auxin distribution pattern for lateral root initiation and crown root emergence. Further studies revealed that OsGER4 is targeted in plasmodesmata, suggesting how OsGER4 could be involved in regulating plasmodesmata permeability to regulate the auxin flow as a part of stress responses that results in changes in root development. Overall, the study provides significant novel insights on auxin homeostasis via uncharted roots through plasmodesmata with the involvement of OsGER4 during root formation in rice under perturbation conditions. Root developmental plasticity is critical for plants to adapt to changing soil environment, where nutrients and abiotic stress factors are distributed heterogeneously. How plant roots sense and avoid heterogeneous abiotic stress in soil remains unclear. Here, we show that, in response to asymmetric stress of heavy metals (Cd, Cu or Pb) and salt (NaCl), rice roots rapidly proliferate lateral root branching in the stress-free area, thereby remodeling root architecture to avoid localized stress. Imaging and quantitative analyses of reactive oxygen species (ROS) show that asymmetric stress induces ROS burst in the tips of the exposed roots, simultaneously triggering rapid systemic ROS signaling to the unexposed roots, which is prerequisite to stress-induced lateral root branching. We identify two respiratory burst oxidase homologs, OsRBOHA and OsRBOHI, as key players for ROS generation and systemic signaling in response to asymmetric stress. Auxin signaling and cell wall remodeling act downstream of the systemic ROS signaling to promote lateral root development. Our study reveals a RBOH-ROS-auxin signaling cascade that enables rice roots to avoid localized stress of heavy metals and salt and provides new insight into root system plasticity in heterogenous soil.

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