This essay develops a conceptual framework for a theory of plant organisms. This framework has to consider the specificities of the plant lifestyle: the lack of contiguous borders, a centrifugal architecture based on continuous addition of modular elements, the lack of developmental hierarchy, a strong autonomy of individual cells, the absence of cell-lineage or predefined developmental programmes, and, most importantly, the lack of physical body contiguity (defined as continuous interface between internal and external space). The challenges posed by these constraints are met by an organisation that is highly modular. This “LEGO principle” of plant organisation becomes manifest on the level of architecture (as so called telomes, modules comprising vascular tissue accompanied by ground tissue that can differentiate into vasculature), cellular organisation (as innate polarity of individual cells), and genetics (as modular genetic programmes that can be rearranged in time to yield a great variety of combinations). The assembly of these versatile modules is controlled through robust self-organisation driven by autocatalytic loops linked to lateral inhibition. The origin of this selforganisation can be traced back to photosynthetic prokaryotes as outlined for heterocyst differentiation of cyanobacteria. Lateral inhibition can use actual chemical agents, but in many cases it is based on mutual competition for a limiting patterning signal. This inhibition by competition is demonstrated for phyllotaxis (the pattern by which leaves are laid down in the shoot apex), and vascular differentiation, phenomena that are both regulated by the plant hormone auxin. To address the dynamic formation of plant organisms, we have established cell lines derived from the ground tissue of tobacco as experimental system. These cells produce, upon addition of auxin, pluricellular files with distinct axis and polarity partially recapitulating the developmental programme of their progenitor tissue. The individual cell divisions within a file are synchronised through weak coupling based on a directional flow of auxin and thus constitute a simple minimal organism that can be used to get insight into the process of self-organisation. Using this system we have identified an oscillatory circuit as central element of self organisation. This self-refering circuit connects auxin-dependent remodeling of the actin cytoskeleton with actin-dependent remodeling of auxin flux. We can manipulate this oscillator, and consequently, the temporal pattern of cell divisions, by genetic engineering of actin structure, but also by optical engineering of auxin gradients within a file. The essay concludes with the working hypothesis that the contiguity of plant organisms is manifest in time (“rhythm”) rather than in space (“body”). Plant organisms are manifest as resonance between highly autonomous oscillators (telomes, cells, genetic programmes) achieved by weak coupling. The resonance proceeds on the background of a strong noise of the individual oscillations. This strong noise represents a system property of plant organisms which can be explained and deduced from the diffuse organisation of plant sensing. A plant „organism” should therefore be understood as process – as entrainment of the initially dissonant individual rhythms. As soon as synchrony between the individual oscillators is established, a plant “organism” will vanish behind the resonating individual cells. This culminates in a paradox: the organismic flow of plant organisms is directed to self-abolition.
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