Die for living better: Plants modify root system architecture through inducing PCD in root meristem under severe water stress

Plant root development is highly plastic in order to cope with various environmental stresses; many questions on the mechanisms underlying developmental plasticity of root system remain unanswered. Recently, we showed that autophagic PCD occurs in the region of root apical meristem in response to severe water deficit. We provided evidence that reactive oxygen species (ROS) accumulation may trigger the cell death process of the meristematic cells in the stressed root tips. Analysis of BAX inhibitor-1 (AtBI1) expression and the phenotypic response of atbi1-1 mutant under the severe water stress revealed that AtBI1 and the endoplasmic reticulum (ER) stress response pathway modulate water stress-induced PCD. As a result, the thick and short lateral roots with increased tolerance to the stress are induced. We propose that under severe drought condition, plants activate PCD program in the root apical root meristem, so that apical root dominance is removed. In this way, they can remodel their root system architecture to adapt the stress environment.Key words: Arabidopsis, adaptation, PCD, root system architecture, water stressPlant shoot apical dominance is well known. The axillary buds are inhibited by the growing shoot apical meristem, and they would not grow until the shoot apical meristems are decapitated.¹ The same phenomenon has been found in the roots of dicot plants. Primary roots exhibit apical dominance over lateral roots and are able to penetrate deeply into the soil. Lateral root primordia were rapidly activated when primary root tips of lettuce (Lactuca sativa) were removed.² It is apparent that apical meristem activity in shoots and roots determines lateral organs and the shapes of above ground and root system architecture under normal conditions. Many plants have active meristematic activity in their shoot and root tips through their whole life resulting in indeterminate development of their shoots and primary roots, whereas others generate branches at certain developmental stages when the meristematic activity and apical dominance become low.It has long been known that plants modify their root morphology, orientation and increase root biomass to maximize water and nutrient absorption.^3,4 However, how the root morphology and architecture are changed in response to water shortage and what the underlying mechanisms are largely unknown. Previously, it has been reported that plants, due to their sessile nature, have developed a very important adaptive mechanism, namely hydrotropism to avoid the damage caused by water shortage. Plant roots can sense the moisture gradient and grow toward to water or moisture when they are grown at conditions with non-uniform water distribution.⁵ Recently, we found another key mechanism through which plants can remove root apical dominance and remodel their root system architecture, thus to minimize the damage caused by a uniform severe water shortage condition.⁶Firstly, we found that growth rates of the Arabidopsis plants germinated on normal conditions were reduced when the concentrations of PEG in the growth media was increased, and primary roots of the stressed plants completely ceased growth when the PEG concentrations reached 40% (w/v) in the agar medium, a severe water stress. The results showed that growth cessation of the stressed plants was caused by PCD of the cells in the region of root apical meristems, and the cells underwent autophagic cell death upon the most severe water deficit. Secondly, we demonstrated that AtBI-1, a marker gene which plays a critical role in protecting the cells from ER stress-induced PCD in plants, mediates water stress-induced PCD of the root meristem. Further observation of ROS accumulation in the root tips upon to the severe water stress suggests that the high level of the ROS may disrupt the ER homeostasis and ROS may act as a signal to trigger the PCD. Importantly, we found that the occurrence of PCD of the meristematic cells of the stressed plants promoted the development of lateral roots. These short and tublized lateral roots grew slowly under severe water stress, but they could immediately become normal lateral roots and resume their elongation and after rehydration. Plant growth is subsequently restored to complete their entire life cycle. However, the lateral roots induced by decapitating primary root tips under normal conditions did not continue elongation like the stress induced lateral roots, and they cannot restore their growth after rehydration.Based on these results, we propose that plants can sense the severity of water stress, initiate autophagic PCD of meristematic cells in Arabidopsis root tips through ER stress signaling pathway and stimulate lateral root development (Fig. 1). Death of meristematic cells results in the loss of mitotic cell division activity in meristem and eventual root meristem function. The outcome of PCD caused-loss of root meristem activity is same as the surgical removal of apical root tips. In both cases, lateral root primordia are activated and lateral root emergence is promoted. However, the main difference between water stress induced-loss of root meristem function and surgical decapitation of root tips is that the former induces lateral roots with enhanced stress tolerance plays key roles in post-stress recovery, whereas the latter promotes development of lateral roots do not alter stress response. This implicates that stress-induced loss of meristem function and subsequent occurrence of specified lateral roots are adaptive mechanisms for plants to cope with the severe water stress. In other words, plants induce cell death of root meristem for living better.Open in a separate windowFigure 1A simplified model depicting the role of PCD in root meristem in plastic development of root system architecture in response to water stress.It is known that auxin distribution and maxima play key roles in lateral root initiation and emergence.^7–10 Alteration in auxin polar transport has been proposed as the main reason of decapitation induced lateral root development.¹¹ It is conceivable that auxin is also involved in stress induced-lateral root formation and development, but it is clear that interplay between stress signaling cascades and developmental signalings occurs after perception of the stress signals by plant cells resulting in root system development remodeling. These findings provide novel insights into mechanisms of plants to adapt to the uniform severe water stress at organ, cellular and molecular levels. However, the research of plastic development of root system in response to water stress is still in its infancy. Combinatorial strategies for the investigation of stress induced-PCD of root meristematic cells and subsequent lateral root development will help to uncover the molecular mechanisms underlying this positive response of plants in response to severe water stress. In particular, further study of auxin redistribution under water stress and interaction between auxin and stress hormone signalings in remodeling root system architecture will further our understanding of how developmental plasticity of plant root system is regulated. The results will facilitate the improvement of drought tolerance in crops.