Physiologically mediated self/non-self discrimination in roots

Abstract

Recent evidence suggests that self͞non-self discrimination exists among roots; its mechanisms, however, are still unclear. We compared the growth of Buchloe dactyloides cuttings that were grown in the presence of neighbors that belonged to the same physiological individual, were separated from each other for variable periods, or originated from adjacent or remote tillers on the same clone. The results demonstrate that B. dactyloides plants are able to differentiate between self and non-self neighbors and develop fewer and shorter roots in the presence of other roots of the same individual. Furthermore, once cuttings that originate from the very same node are separated, they become progressively alienated from each other and eventually relate to each other as genetically alien plants. The results suggest that the observed self͞non-self discrimination is mediated by physiological coordination among roots that developed on the same plant rather than allogenetic recognition. The observed physiological coordination is based on an as yet unknown mechanism and has important ecological implications, because it allows the avoidance of competition with self and the allocation of greater resources to alternative functions.Buchloe dactyloides ͉ competition ͉ development ͉ phenotypic plasticity ͉ physiological coordination V irtually all multicellular organisms possess recognition systems that allow them to distinguish self from non-self with precision (1-4). For example, self͞non-self recognition systems enable the prevention of inbreeding by self-pollination in plants (4-5) as well as the cooperation between kin in various clonal marine invertebrates (6-8). Because competition entails allocation of limiting resources to nonreproductive functions (9-11), natural selection is expected to favor mechanisms that minimize wasteful competition among parts of the same individual (12), clonemates, and kin (13).Recent evidence suggests that roots are able to alter their growth according to the presence or absence of specific neighbors (14) and to segregate spatially in ''territories'' (15). The evidence also suggests the existence of two different types of self͞non-self discrimination among roots. (24,31), it is usually not studied in the context of self͞non-self interactions. However, the results of previous studies suggest the involvement of physiological coordination in self͞non-self root discrimination (18,20,21). The prevention of contact inhibition between roots of the same A. dumosa plant (18) as well as the avoidance of self competition between roots of F. chiloensis (20) was found to be at least partially based on physiological coordination between roots that develop on the same plant. In an earlier study, P. sativum plants were grown so that they had two roots and two shoots that could be either longitudinally separated into two genetically identical but physiologically distinct individuals or left intact. Root growth was significantly greater in the presence and the direction of roots that belonged to different plants,...

Plant synapses: actin-based domains for cell-to-cell communication

“…Furthermore, plant synapses might represent the crucial structures that determine the integrity of individual plants by allowing their cells and organs to define and detect 'self ' and recognize 'nonself ' [13,49]. Last but not least, the plant synapse concept would explain why plants are able to use non-genetic 'public' information [50] transmitted between species boundaries [12,50] for their trial-and-error-navigated and experience-based behaviour [11,12].…”

“…Last but not least, the plant synapse concept would explain why plants are able to use non-genetic 'public' information [50] transmitted between species boundaries [12,50] for their trial-and-error-navigated and experience-based behaviour [11,12]. Synapses might provide the information platform that confers the integrity and self-consciousness [13,49] to multicellular organisms. All this suggests that plants are much more similar to animals than one would have been willing to believe a few years ago.…”

“…The plant synapse concept can also help to explain the latest enigma of plant biology -the ability of whole roots to discriminate between 'self '-and 'non-self ' neighbours and to adapt their growth and physiology accordingly [13]. Fertile soil is densely packed with root biomass and every root is competing for space and for the limited resources of oxygen, water and mineral nutrients.…”

“…It is a mystery what processes and mechanisms are behind the ability of plant roots to identify 'self' from 'non-self '. A recent breakthrough study discovered that root cuttings from genetically identical plants start to perceive each other as 'non-self ' after a short time of separation from the parent body, which suggests that unknown non-genetic processes determine the ability of 'self' and 'non-self ' recognition in plants [13]. The concept of the plant synapse might provide a useful framework for explaining this enigma of plant biology because synapses are fundamentally important for 'self and non-self ' discrimination at both cellular (immunological synapses) and organismal (neuronal synapses) levels [49].…”

“…Plant action potentials trigger a transient rise in cytoplasmic calcium levels [9], and the rapid transmission of oxidative and nitrosative stress signals between root and shoot apices of Arabidopsis appear to be relevant for the spread of systemic signals in the establishment of plant immunity [10]. Recent advances in plant physiology and ecology have revealed that plants might indeed be considered as intelligent organisms [11] showing a complex social life mediated preferentially via their root systems [8,12,13]. Plants receive, store and process large amounts of information about their environment, including information from neighbouring plants and other organisms.…”