Aspects of plant intelligence: an answer to Firn

In a recent 'Invited Review', I stated the case for plant intelligence, provided definitions and outlined some of the consequences, illustrating them with examples. A short critique of this concept by Firn is given in the preceding 'Viewpoint' and rebuttals of the criticisms it contains are presented in the present article. The importance of plant intelligence as an emergent property resulting from interactions and communication of the component tissues is re-stated. The contentions made by Firn that plants are collectives of physically joined organs but acting in relative isolation of each other is subject to critical analysis and found to be contradicted by much established literature. Viewing plants as expressing intelligent behaviour should lead to better understanding of their ecological success and indicate experiments to test the basic concept.     

Plant intelligence: Why,why not or where?

The concept of plant intelligence, as proposed by Anthony Trewavas, has raised considerable discussion. However, plant intelligence remains loosely defined; often it is either perceived as practically synonymous to Darwinian fitness, or reduced to a mere decorative metaphor. A more strict view can be taken, emphasizing necessary prerequisites such as memory and learning, which requires clarifying the definition of memory itself. To qualify as memories, traces of past events have to be not only stored, but also actively accessed. We propose a criterion for eliminating false candidates of possible plant intelligence phenomena in this stricter sense: an “intelligent” behavior must involve a component that can be approximated by a plausible algorithmic model involving recourse to stored information about past states of the individual or its environment. Re-evaluation of previously presented examples of plant intelligence shows that only some of them pass our test.

“You were hurt?” Kumiko said, looking at the scar.Sally looked down. “Yeah.”“Why didn''t you have it removed?”“Sometimes it''s good to remember.”“Being hurt?”“Being stupid.”—(W. Gibson: Mona Lisa Overdrive)

Key words: intelligence, memory, learning, plant development, mathematical models, plant neurobiology, definition of terms     

Green plants as intelligent organisms

Intelligent behaviour, even in humans, is an aspect of complex adaptive behaviour that provides a capacity for problem solving. This article assesses whether plants have a capacity to solve problems and, therefore, could be classified as intelligent organisms. The complex molecular network that is found in every plant cell and underpins plant behaviour is described. The problems that many plants face and that need solution are briefly outlined, and some of the kinds of behaviour used to solve these problems are discussed. A simple way of comparing plant intelligence between two genotypes is illustrated and some of the objections raised against the idea of plant intelligence are considered but discarded. It is concluded that plants exhibit the simple forms of behaviour that neuroscientists describe as basic intelligence.     

A new paradigma on the plant evolution: from a natural evolution to an artificial evolution?

After evidencing the great importance of plants for animals and humans in consequence of the photosynthesis, several considerations on plant evolution are made. One of the peculiar characteristics of the plant is the sessile property, due especially to the cell wall. This factor, principally, strengthened by the photosynthetic process, determined the particular developmental pattern of the plant, which is characterized by the continuous formation of new organs. The plant immobility, although negative for its survival, has been, in great part, overcome by the acquisition of the capacity of adaptation (plasticity) to the environmental stresses and changes, and the establishment of more adapted genotypes. This capacity to react to the external signals induced Trewavas to speak of "plant intelligence". The plant movement incapacity and the evolution of the sexual reproduction system were strongly correlated. In this context, the evolution of the flower in the Angiosperms has been particularly important to allow the male gamete to fertilize the immobile female gamete. Moreover, the formation of fruit and seed greatly improved the dispersal and conservation of the progeny in the environment. With the flower, mechanisms to favour the outcrossing among different individuals appeared, which are essential to increase the genetic variability and, then, the plant evolution itself. Although the Angiosperms seem highly evolved, the plant evolution is not surely finished, because many reported morpho-physiological processes may be still considered susceptible of further improvement. In the last years the relationships among humans, plants and environment are becoming closer and closer. This is due to the use of the DNA recombinant techniques with the aim to modify artificially plant characters. Therefore, the risk of a plant evolution strongly directed towards practical or commercial objectives, or "an artificial evolution", may be hypothesized.     

Is the extent of the proliferation of component cell lineages critical during organ morphogenesis?

Shoot meristems of higher plants are composed of several clonally distinct cell lineages. Periclinal chimeras have been used to determine the fate of derivatives of these lineages in mature leaves and other organs of the plant. Fates of individual meristem cells are not rigidly fixed and the distribution of tissue derived from each meristem lineage in different regions of an organ is variable. The amount of proliferation from an individual lineage can be altered without affecting the overall morphology of organs. Mechanisms exist by which cells from several lineages coordinate their relative amounts of proliferation. The conclusion from these studies is that cell proliferation and organ morphogenesis are developmental events that can be uncoupled.     

Cell Differentiation and Organ Initiation at the Shoot Apical Meristem

Plants continuously generate organs at the flanks of their shoot apical meristems (SAMs). The patterns in which these organs are initiated, also called patterns of phyllotaxis, are highly stereotypic and characteristic for a particular species or developmental stage. This stable, predictable behaviour of the meristem has led to the idea that organ initiation must be based on simple and robust mechanisms. This conclusion is less evident, however, if we consider the very dynamic behaviour of the individual cells. How dynamic cellular events are coordinated and how they are linked to the regular patterns of organ initiation is a major issue in plant developmental biology.     

植物表皮毛研究进展

表皮毛是大多数植物地上部分表皮组织所延伸出来的一种特化的毛状结构附属物。表皮毛在植物表皮层和环境间构筑了一道天然的物理屏障, 不但对植物的生长发育具有重要意义, 而且还具有非常高的应用价值和经济价值。近几年, 研究者从不同植物中不断克隆出新的表皮毛发育相关基因, 在揭示植物调控表皮毛生长发育的分子机制方面取得很大进展。该文综述了植物表皮毛的最新研究进展, 并展望了植物表皮毛的研究方向及应用开发价值。     

The tomato ethylene receptor gene family: Form and function

Phytohormones are essential for integrating many aspects of plant development and responses to the environment. Regulation of hormonally controlled events occurs at multiple levels: synthesis, catabolism and perception (Trewavas 1983, Bradford and Trewavas 1994). At the level of perception, sensitivity to hormones can be regulated both spatially and temporally during the life cycle. An example of spatial regulation is the differential response to a hormone that occurs during organ abscission. Temporally, sensitivity of an organ to a hormone may change during maturation, as occurs during fruit ripening. In this review, we will focus on the initial event in recognition of one hormone, ethylene. The ethylene receptor was the first plant hormone receptor to be unambiguously identified. Over the last few years, great progress has been made in elucidating the genes involved in ethylene action. Nonetheless, the mechanisms of signal transduction remain to be established. Here, we will address the status of the tomato receptor gene family and the evidence that regulation of receptor gene expression can influence the response of the plant to the hormone.     

Immunity of a leguminous plant infected by nodular bacteria <Emphasis Type="Italic">Rhizobium</Emphasis> spp. F.: Review

Recent studies of the immune system of leguminous plants infected with nodular bacteria (rhizobia) are summarized. The possibility of blocking the invasion of rhizobia into plant organs not affected by the primary infection is discussed. The concept of local and systemic resistance of the leguminous plant to rhizobial infection is introduced. The Nod factors of rhizobia are considered, as well as the plant receptors that interact with these factors upon the formation of symbiosis of the plant and bacteria. The role of bacterial surface exopolysaccharides in the suppression of the protective system of the plants is discussed. The innate immunity of leguminous plant cells is assumed to affect the formation and functioning of the symbiosis of the plant and the bacteria.     

Increase of homologous recombination frequency in vascular tissue of Arabidopsis plants exposed to salt stress

Here we analyzed the influence of salt stress on plant genome stability. Homologous recombination events were detected in transgenic Arabidopsis plants that carried in their genome a beta-glucuronidase recombination marker. Recombination events were scored as blue sectors using a stereo microscope. Exposure to 50 mM salt resulted in a 3.0-fold increase in recombination frequency. To analyze the organ and tissue specificity of recombination events, we examined cross-sections of leaves, stems and roots. We found that nearly 30% of recombination events in plants grown under normal conditions and nearly 50% of events in plants grown on salt were undetected by the conventional method. Most of the recombination events represented a cluster/group of cells (12 on average), although events with single cells were also detected. Recombination events were very frequent in leaf mesophyll cells. On average, individual recombination events located on leaves contained more cells than events located on roots or stems. Analysis of recombination events in cross-sectioned tissue of salt-treated plants revealed a shift in the distribution of recombination events towards the vascular tissue. We discuss the significance of the finding for plant stress physiology.     

Endocrine Organs of a Parasitic Male Deep-Sea Angler-Fish,Edriolychnus schmidti

The parasitic male deep-sea angler-fish Edriolychnus schmidti Regan 1925, which was described by Regan and Trewavas 1932, was reinvestigated with respect to the endocrine organs. Although the original microscopical sections are not in a good condition, it could be concluded that those organs which are involved in regulation of various internal environmental factors, as well as those involved in adaption to external factors, appear poorly developed or reduced. Mechanisms regulating reproductive activities seem to be well developed; a pronounced tuberis region is seen in the otherwise reduced brain and the peculiar pituitary gland appears to contain secretory active cells.     

Plants that differ in height investment can coexist if they are distributing non-uniformly within an area

In nature, there is a large variability in the intrinsic height of plants living within an area. The question arises whether these height differences affect the plants’ ability to coexist and thus is an adaptive trait.Using a biologically mechanistic model, we explored the possibilities for coexistence of plant types that differ in their pattern of allocation between stem (i.e. height growth) and other organs. We simulated the competition for light between growing individual plants. The study was game theoretical in the sense that each individual plant at any time affected the light availability for all plants in a locality, making conditions variable throughout the growing season and between seasons when the composition of competing plants changed.It was found that plant types that differed in their allocation to height growth could coexist over the course of years when these plants distributed their seeds non-uniformly in space, creating local differences in plant density. At each different density, one type with a specific investment in height performed better (i.e. achieved a greater seed production) than the rest of the types, thus preventing the exclusion of that type over the years. The resulting model community was self-assembling; local densities and competitive pressures originated as traits from the model plants themselves and were not the result of imposed external factors acting upon the model community.This mechanistic modelling approach shows that a condition as simple as a non-uniform distribution of seeds can generate the conditions for plants of various height growth strategies to live together over multiple generations. This study suggests that differences in plant height can be an emerging property of dispersing populations.     

基因组学技术大发展助力园艺植物研究取得新进展

园艺植物包括花卉、蔬菜、果树、部分瓜类(如西瓜(Citrullus lanatus)和甜瓜(Cucumis melo))和茶树(Camellia sinensis),在植物分类上涉及大量物种。园艺植物的基因组学和遗传学研究具有重要的理论价值和经济意义。基因组测序技术及相关生物信息学工具的发展为园艺植物基因组和分子生物学研究注入了新的活力。睡莲是一种重要的花卉植物,除了具有观赏价值,其进化地位也非常特殊,属于一种早期被子植物类群。最近,蓝星睡莲(N.colorata)的高质量基因组图谱绘制完成。通过系统分析和比较睡莲基因组与其它被子植物的基因组,研究者阐明了睡莲的进化位置及相关进化事件。所获得的高质量基因组序列将有助于园艺植物研究者开展深入的分子遗传学研究,鉴定到控制和调控花器官、花色花香及品质等众多性状的功能基因,从而推动基础研究的快速发展和加快新品种创制。     

Intrachromosomal homologous recombination in whole plants.

A system to assay intrachromosomal homologous recombination during the complete life-cycle of a whole higher eukaryote was set up. Arabidopsis thaliana plants were transformed with a recombination substrate carrying a non-selectable and quantitatively detectable marker gene. The recombination substrates contain two overlapping, non-functional deletion mutants of a chimeric beta-glucuronidase (uidA) gene. Upon recombination, as proven by Southern blot analysis, a functional gene is restored and its product can be detected by histochemical staining. Therefore, cells in which recombination events occurred, and their progeny, can be precisely localized in the whole plant. Recombination was observed in all plant organs examined, from the seed stage until the flowering stage of somatic plant development. Meristematic recombination events revealed cell lineage patterns. Overall recombination frequencies typically were in the range 10(-6)-10(-7) events/genome. Recombination frequencies were found to differ in different organs of particular transgenic lines.     

Das Leitgewebe gibt den Takt an

Hierarchy in the plant clock shop Higher plants use an endogenous timekeeper, the circadian clock, to adjust to the periodic changes in light and darkness in their environment. It has long been assumed that plant cellular clocks act as stand‐alone systems. Recent evidence points to widespread coupling among clocks in different organs and different cells. Moreover, a hierarchy has been observed between clocks in leaves and roots and even between clocks in individual cell types of the leaf, with the clock in the vasculature being dominant over the clock in mesophyll cells. Thus, the plant circadian system may also show a hierarchical organization reminiscent of the clock system in mammals.     

Growth substance sensitivity: The need for clearer ideas, precise terms and purposeful experiments

The idea that growth substance-responsive cells might not have a fixed capacity to respond to a growth substance is not new, but it is an idea which has received much greater consideration in the last few years, largely as a result of a series of articles by Trewavas (1981a,b, 1982, 1983). Despite the fact that no thorough attempt has been made to explore this concept experimentally, it seems to have been accepted as a valid and useful one, even by some of Trewavas's critics (Cleland 1983). However, the term "change in growth substance sensitivity" can be shown to have several meanings, each with a very different underlying physiological mechanism. If the concept is to be developed into a productive model of the way in which plant growth and development are regulated under certain circumstances, it will be necessary to be more precise. New terms are proposed to describe some of the factors which could contribute to changes in the sensitivity of a cell to a growth substance. It is argued that much more purposeful experiments will be needed in order to establish whether changes in sensitivity do accompany some developmental processes and to probe the exact nature of these changes.     

Noninvasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode

Auxin (also known as indole-3-acetic acid, IAA) represents an ancient signaling molecule of plants that also exerts bioactive actions on yeast and animal cells. Importantly, IAA emerges as a new anticancer agent due to the ability of oxidatively activated IAA to selectively kill tumor cells. IAA acts as a pheromone-like molecule in brown algae, whereas the hormone concept of IAA dominates current plant biology. However, recent advances also favor the morphogen- and transmitter-like nature of IAA in plants, making this small molecule one of the most unique molecules in the eukaryotic superkingdom. Here, we introduce new technology for the continuous measuring of IAA fluxes in living cells, tissues, and whole organs that is based on a carbon nanotube-modified and self-referencing microelectrode specific for IAA. This technique not only will advance our knowledge of how IAA regulates plant development but will also be applicable in medicine for its potential use in cancer therapy.     

Imaging calcium dynamics in living plants using semi-synthetic recombinant aequorins

The genetic transformation of the higher plant Nicotiana plumbaginifolia to express the protein apoaequorin has recently been used as a method to measure cytosolic free calcium ([Ca2+]i) changes within intact living plants (Knight, M. R., A. K. Campbell, S. M. Smith, and A. J. Trewavas. 1991. Nature (Lond.). 352:524-526; Knight, M. R., S. M. Smith, and A. J. Trewavas. 1992. Proc. Natl. Acad. Sci. USA. 89:4967-4971). After treatment with the luminophore coelenterazine the calcium-activated photoprotein aequorin is formed within the cytosol of the cells of the transformed plants. Aequorin emits blue light in a dose-dependent manner upon binding free calcium (Ca2+). Thus the quantification of light emission from coelenterazine-treated transgenic plant cells provides a direct measurement of [Ca2+]i. In this paper, by using a highly sensitive photon-counting camera connected to a light microscope, we have for the first time imaged changes in [Ca2+]i in response to cold-shock, touch and wounding in different tissues of transgenic Nicotiana plants. Using this approach we have been able to observe tissue-specific [Ca2+]i responses. We also demonstrate how this method can be tailored by the use of different coelenterazine analogues which endow the resultant aequorin (termed semi-synthetic recombinant aeqorin) with different properties. By using h-coelenterazine, which renders the recombinant aequorin reporter more sensitive to Ca2+, we have been able to image relatively small changes in [Ca2+]i in response to touch and wounding: changes not detectable when standard coelenterazine is used. Reconstitution of recombinant aequorin with another coelenterazine analogue (e-coelenterazine) produces a semi-synthetic recombinant aequorin with a bimodal spectrum of luminescence emission. The ratio of luminescence at two wavelengths (421 and 477 nm) provides a simpler method for quantification of [Ca2+]i in vivo than was previously available. This approach has the benefit that no information is needed on the amount of expression, reconstitution or consumption of aequorin which is normally required for calibration with aequorin.