Basic versus applied research: Julius Sachs (1832–1897) and the experimental physiology of plants

The German biologist Julius Sachs was the first to introduce controlled, accurate, quantitative experimentation into the botanical sciences, and is regarded as the founder of modern plant physiology. His seminal monograph Experimental-Physiologie der Pflanzen (Experimental Physiology of Plants) was published 150 y ago (1865), when Sachs was employed as a lecturer at the Agricultural Academy in Poppelsdorf/Bonn (now part of the University). This book marks the beginning of a new era of basic and applied plant science. In this contribution, I summarize the achievements of Sachs and outline his lasting legacy. In addition, I show that Sachs was one of the first biologists who integrated bacteria, which he considered to be descendants of fungi, into the botanical sciences and discussed their interaction with land plants (degradation of wood etc.). This “plant-microbe-view” of green organisms was extended and elaborated by the laboratory botanist Wilhelm Pfeffer (1845–1920), so that the term “Sachs-Pfeffer-Principle of Experimental Plant Research” appears to be appropriate to characterize this novel way of performing scientific studies on green, photoautotrophic organisms (embryophytes, algae, cyanobacteria).     

Julius Sachs (1832–1897) and the Unity of Life

In 1865, the German botanist Julius Sachs published a seminal monograph entitled Experimental-Physiologie der Pflanzen (Experimental Physiology of Plants) and hence became the founder of a new scientific discipline that originated 150 y ago. Here, we outline the significance of the achievements of Sachs. In addition, we document, with reference to his Vorlesungen über Pflanzen-Physiologie (Lectures on the Physiology of Plants, 1882), that Sachs was one of the first experimentalists who proposed the functional unity of all organisms alive today (humans, animals, plants and other “vegetable” organisms, such as algae, cyanophyceae, fungi, myxomycetes, and bacteria).     

Towards a postmodern synthesis of evolutionary biology

In 2009, we are celebrating the 200th anniversary of Charles Darwin and the 150th jubilee of his masterpiece, the Origin of Species. Darwin constructed the first coherent and compelling narrative of biological evolution and thus founded evolutionary biology—and modern biology in general, remembering the famous dictum of Dobzhansky. It is, however, counter-productive, and ultimately, a disservice to Darwin’s legacy, to define modern evolutionary biology as neo-Darwinism. The current picture of evolution, informed by results of comparative genomics and systems biology, is by far more complex than that presented in the Origin of Species, so that Darwinian principles, including natural selection, are incorporated into the evolving new synthesis as important but certainly not all-embracing tenets. This expansion of evolutionary biology does not denigrate Darwin in the least but rather emphasizes the fertility of his ideas.     

Systems biology of eukaryotic superorganisms and the holobiont concept

The founders of modern biology (Jean Lamarck, Charles Darwin, August Weismann etc.) were organismic life scientists who attempted to understand the morphology and evolution of living beings as a whole (i.e., the phenotype). However, with the emergence of the study of animal and plant physiology in the nineteenth century, this “holistic view” of the living world changed and was ultimately replaced by a reductionistic perspective. Here, I summarize the history of systems biology, i.e., the modern approach to understand living beings as integrative organisms, from genotype to phenotype. It is documented that the physiologists Claude Bernard and Julius Sachs, who studied humans and plants, respectively, were early pioneers of this discipline, which was formally founded 50 years ago. In 1968, two influential monographs, authored by Ludwig von Bertalanffy and Mihajlo D. Mesarovi?, were published, wherein a “systems theory of biology” was outlined. Definitions of systems biology are presented with reference to metabolic or cell signaling networks, analyzed via genomics, proteomics, and other methods, combined with computer simulations/mathematical modeling. Then, key insights of this discipline with respect to epiphytic microbes (Methylobacterium sp.) and simple bacteria (Mycoplasma sp.) are described. The principles of homeostasis, molecular systems energetics, gnotobiology, and holobionts (i.e., complexities of host–microbiota interactions) are outlined, and the significance of systems biology for evolutionary theories is addressed. Based on the microbe—Homo sapiens—symbiosis, it is concluded that human biology and health should be interpreted in light of a view of the biomedical sciences that is based on the holobiont concept.     

Seed Physiology: Its History from antiquity to the beginning of the 20th century

Seed physiology, especially seed germination, has intrigued the human mind since antiquity, partly out of curiosity, partly because of practical reasons. Theophrastus could be called the father of seed physiology since he already described many of the facts and problems which up to this day are being investigated by seed physiologists. Most of the other ancient authors writing about natural history or agriculture (Columella, Varro, Pliny the elder, Virgil) added little to Theophrastus’ all encompassing knowledge of seed physiology. The 1700 years from the first century A.D. to the end of the 18th century were a “black out” (Johansen, 1951) of seed physiology. At the beginning of the 19th century people like Schleiden, Amici, Brown and Hofmeister first understood structure and function of ovule, embryo sac and pollen tube whereas fertilization and double fertilization were only detected at the end of the 19th century by Strasburger, Nawaschin and Guignard. The physiology and biochemistry of seed maturation were first investigated by Sachs and Pfeffer, two great masters of modern plant physiology. In modern times our detailed knowledge of the effect of external factors on seed germination is due to the many authors working at the end of the 19th and the beginning of the 20th centuries. Our knowledge of the impact of temperature on germination derives mainly from the investigations of Sachs, De Vries and Haberlandt, and of light from those of Caspary, Cieslar, Heinricher and Kinzel. The action spectrum of light was first investigated by Cieslar, and Flint and McAllister whereas the most important discovery of the effect of light on germination (and on many other physiological phenomena), the R-FR photoreversible system, was made by Borthwick et al. leading later to the discovery of the phytochrome. The first germination inhibiting and stimulating substances were found by Siegmund and Lehman. The long history of seed physiology should make today’s seed physiologists conscious of the fact that they stand on the “shoulders of giants.”     

The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

Williams' evolutionary theory of senescence based on antagonistic pleiotropy has become a landmark in evolutionary biology, and more recently in biogerontology and evolutionary medicine. In his original article, Williams launched a set of nine “testable deductions” from his theory. Although some of these predictions have been repeatedly discussed, most have been overlooked and no systematic evaluation of the whole set of Williams' original predictions has been performed. For the sixtieth anniversary of the publication of the Williams' article, we provide an updated evaluation of all these predictions. We present the pros and cons of each prediction based on recent accumulation of both theoretical and empirical studies performed in the laboratory and in the wild. From our viewpoint, six predictions are mostly supported by our current knowledge at least under some conditions (although Williams' theory cannot thoroughly explain why for some of them). Three predictions, all involving the timing of senescence, are not supported. Our critical review of Williams' predictions highlights the importance of William's contribution and clearly demonstrates that, 60 years after its publication, his article does not show any sign of senescence.     

Besprechungen

Book Reviewed in this article: Osche, G. (1966): Die Welt der Parasiten. Frisch, Karl v. (1965): Tanzsprache und Orientierung der Bienen. Reichenbach-Klinke, H. H. (1963): Krankheiten der Reptilien. Reichenbach-Klinke, H. , und E. Elkan (1965): The principal diseases of lower vertebrates. Griffin, D. R. (1964): Bird migration, the biology and physics of orientation behavior. Kaestner, A. (1965): Lehrbuch der Speziellen Zoologie. Kühn, A. (1965): Vorlesungen über Entwicklungsphysiologie. Lorenz, K. (1966): Stammes- und kulturgeschichtliche Ritenbildung. Hafez, E. S. (1962): The Behaviour of domestic animals. Hassenstein, B. (1965): Biologische Kybernetik. Bally, G. (1966): Vom Spielraum der Freiheit. Strohmeyer, C. (1959): Schweinekomödie.     

Human physiology in space

The universality of gravity (1 g ) in our daily lives makes it difficult to appreciate its importance in morphology and physiology. Bone and muscle support systems were created, cellular pumps developed, neurons organised and receptors and transducers of gravitational force to biologically relevant signals evolved under 1g gravity. Spaceflight provides the only microgravity environment where systematic experimentation can expand our basic understanding of gravitational physiology and perhaps provide new insights into normal physiology and disease processes. These include the surprising extent of our body's dependence on perceptual information, and understanding the effect and importance of forces generated within the body's weightbearing structures such as muscle and bones. Beyond this exciting prospect is the importance of this work towards opening the solar system for human exploration. Although both appear promising, we are only just beginning to taste what lies ahead.     

Evolution and mechanisms of plant tolerance to flooding stress

Background

In recognition of the 200th anniversary of Charles Darwin''s birth, this short article on flooding stress acknowledges not only Darwin''s great contribution to the concept of evolution but also to the study of plant physiology. In modern biology, Darwin-inspired reductionist physiology continues to shed light on mechanisms that confer competitive advantage in many varied and challenging environments, including those where flooding is prevalent.

Scope

Mild flooding is experienced by most land plants but as its severity increases, fewer species are able to grow and survive. At the extreme, a highly exclusive aquatic lifestyle appears to have evolved numerous times over the past 120 million years. Although only 1–2% of angiosperms are aquatics, some of their adaptive characteristics are also seen in those adopting an amphibious lifestyle where flooding is less frequent. Lowland rice, the staple cereal for much of tropical Asia falls into this category. But, even amongst dry-land dwellers, or certain of their sub-populations, modest tolerance to occasional flooding is to be found, for example in wheat. The collection of papers summarized in this article describes advances to the understanding of mechanisms that explain flooding tolerance in aquatic, amphibious and dry-land plants. Work to develop more tolerant crops or manage flood-prone environments more effectively is also included. The experimental approaches range from molecular analyses, through biochemistry and metabolomics to whole-plant physiology, plant breeding and ecology.Key words: Abiotic stress, adaptation, anoxia, Charles Darwin, environmental stress, evolution, flooding, hypoxia, rice, submergence, wetlands     

[PSI+] turns 50

abstract

The year 2015 sees the fiftieth anniversary of the publication of a research paper that underpins much of our understanding of fungal prion biology, namely “ψ, a cytoplasmic suppressor of super-suppressor in yeast” by Brian Cox. Here we show how our understanding of the molecular nature of the [PSI⁺] determinant evolved from an ‘occult’ determinant to a transmissible amyloid form of a translation termination factor. We also consider the impact studies on [PSI] have had – and continue to have - on prion research. To demonstrate this, leading investigators in the yeast prion field who have made extensive use of the [PSI⁺] trait in their research, provide their own commentaries on the discovery and significance of [PSI].     

Über Calcium-Phosphor-Bilanzen an Kaninchen bei Fütterung mit Luzerne und Rotklee

Abstract

Lehrbuch der Physiologie der Haustiere, Reviewed by E. Wiesner

M. F. Tommé und A. V. Modjanov: Ersatzstoffe des Futterproteins (Zameniteli Kormovogo proteina), Verlag Landwirtschaftlicher Literatur, Zeitschriften und Plakate, Moskau 1963, 351 Seiten, russisch. Reviewed by S. Poppe

Lehrbuch der physiologischen Chemie. Reviewed by H. Bergner

Voisin, A.: Weidetetanle, 234 Seiten, 22 Abbildungen, Ganzleinen. Bayerischer Landwirtschaftsverlag München, Basel, Wien, 1963. 34.— DM. Reviewed by E. Kolb     

Discovery of the extracytoplasmic function σ factors

This special issue of Molecular Microbiology marks the 25^th anniversary of the discovery of the extracytoplasmic function (ECF) σ factors, proteins that subsequently emerged as the largest group of alternative σ factors and one of the three major pillars of signal transduction in bacteria, alongside one‐ and two‐component systems. A single bacterial genome can encode > 100 ECF σ factors, and combined with their cognate anti‐σ factors, they represent a modular design that primarily functions in transmembrane signal transduction. Here, we first describe the immediate events that led to the 1994 publication in the Proceeding of the National Academy of Sciences USA, and then set them in the broader context of key events in the history of σ biology research.     

The reproductive biology of two poorly known relatives of the fig (Ficus) and insights into the evolution of the fig syconium

We conducted the first detailed investigation of the floral architecture and reproductive biology of two species from the genus Dorstenia, which are poorly known relatives of Ficus (Moraceae). Our aims were to extend and refine knowledge of the understudied genus Dorstenia and to explore possible insights into the evolution of the fig syconium. We characterised four key stages of floral development using light microscopy, scanning electron microscopy and histological staining. Reproductive biology was found to be complex and species‐specific. Both study species are monoecious and produce an inflorescence of minute male and female flowers. Protogyny, associated with a spatial separation of male and female flowers and asynchronous stamen development, was species‐specific, as was seed set. Our results reveal novel insights into the complex reproductive biology of an under‐studied genus in the family Moraceae. We propose that exploring the reproductive biology of Dorstenia and other poorly known Ficus relatives will provide insights into the evolution of the fig syconium – the unique reproductive structure of this economically and ecologically important genus.     

Developmental phenotypic plasticity: Where ecology and evolution meet molecular biology

The plastic response of phenotypic traits to environmental change is a common research focus in several disciplines - from ecology and evolutionary biology to physiology and molecular genetics. The use of model systems such as the flowering plant Arabidopsis thaliana has facilitated a dialogue between developmental biologists asking how plasticity is controlled (proximate causes) and organismal biologists asking why plasticity exists (ultimate causes). Researchers studying ultimate causes and consequences are increasingly compelled to reject simplistic, ‘black box’ models, while those studying proximate causes and mechanisms are increasingly obliged to subject their interpretations to ecological ‘reality checks.’ We review the successful multidisciplinary efforts to understand the phytochrome-mediated shade-avoidance and light-seeking responses of flowering plants as a pertinent example of convergence between evolutionary and molecular biology. In this example, the two-way exchange between reductionist and holist camps has been essential to rapid and sustained progress. This should serve as a model for future collaborative efforts towards understanding the responses of organisms to their constantly changing environments.     

Model plant systems in salinity and drought stress proteomics studies: a perspective on Arabidopsis and Sorghum

More than a decade after the sequencing of its genome, Arabidopsis still stands as the epitome of a model system in plant biology. Arabidopsis proteomics has also taught us great lessons on different aspects of plant growth, development and physiology. Without doubt our understanding of basic principles of plant biology would not have been this advanced if it were not for knowledge gained using Arabidopsis as a model system. However, with the projections of global climate change and rapid population growth, it is high time we evaluate the applicability of this model system in studies aimed at understanding abiotic stress tolerance and adaptation, with a particular emphasis on maintaining yield under hot and dry environmental conditions. Because of the innate nature of sorghum's tolerance to drought and moderate tolerance to salinity stresses, we believe sorghum is the next logical model system in such studies amongst cereals. In this acute view, we highlight the importance of Arabidopsis as a model system, briefly discuss its potential limitations in drought and salt stress studies, and present our views on the potential usefulness of sorghum as a model system for cereals in drought and salinity stress proteomic studies.     

Decoding and recoding plant development

The development of multicellular organisms has been studied for centuries, yet many critical events and mechanisms of regulation remain challenging to observe directly. Early research focused on detailed observational and comparative studies. Molecular biology has generated insights into regulatory mechanisms, but only for a limited number of species. Now, synthetic biology is bringing these two approaches together, and by adding the possibility of sculpting novel morphologies, opening another path to understanding biology. Here, we review a variety of recently invented techniques that use CRISPR/Cas9 and phage integrases to trace the differentiation of cells over various timescales, as well as to decode the molecular states of cells in high spatiotemporal resolution. Most of these tools have been implemented in animals. The time is ripe for plant biologists to adopt and expand these approaches. Here, we describe how these tools could be used to monitor development in diverse plant species, as well as how they could guide efforts to recode programs of interest.

One-sentence summary: Recent advances in tracking cell lineage and molecular states could inspire new strategies to understand and engineer plant development.     

Seedling development in buckwheat and the discovery of the photomorphogenic shade‐avoidance response

Numerous botanists of the early 19th century investigated the effect of sunlight on plant development, but no clear picture developed. One hundred and fifty years ago, Julius Sachs (1863) systematically analysed the light–plant relationships, using developing garden nasturtium (Tropaeolum majus) and seedlings of buckwheat (Fagopyron esculentum) as experimental material. From these studies, Sachs elucidated the phenomenon of photomorphogenesis (plant development under the influence of daylight) and the associated ‘shade‐avoidance response’. We have reproduced the classical buckwheat experiments of Sachs (1863) and document the original shade‐avoidance syndrome with reference to hypocotyl elongation and cotyledon development in darkness (skotomorphogenesis), white light and shade induced by a canopy of green leaves. In subsequent publications, Sachs elaborated his concepts of 1863 and postulated the occurrence of ‘flower‐inducing substances’. In addition, he argued that the shade‐avoidance response in cereals, such as wheat and maize, is responsible for lodging in crowded plant communities. We discuss these processes with respect to the red‐ to far‐red light/phytochrome B relationships. Finally, we summarise the phytochrome B–phytohormone (auxin, brassinosteroids) connection within the cells of shaded Arabidopsis plants, and present a simple model to illustrate the shade‐avoidance syndrome. In addition, we address the relationship between plant density and health of the corresponding population, a topic that was raised for the first time by Sachs (1863) in his seminal paper and elaborated in his textbooks.     

Secret life of plants: From memory to intelligence

Plants are able to perform photosynthesis and cannot escape from environmental stresses, so they therefore developed sophisticated, highly responsive and dynamic physiology. Others'' and our results indicate that plants solve their optimal light acclimation and immune defenses, photosynthesis and transpiration by a computational algorithm of the cellular automation. Our recent results however suggest that plants are capable of processing information encrypted in light intensity and in its energy. With the help of nonphotochemical quenching and photoelectrophysiological signaling (PEPS) plants are able to perform biological quantum computation and memorize light training in order to optimize their Darwinian fitness. Animals have their network of neuron synapses, electrophysiological circuits and memory, but plants have their network of chloroplasts connected by stromules, PEPS circuits transduced by bundle sheath cells and cellular light memory. It is suggested that plants could be intelligent organisms with much higher organism organization levels than it was thought before.Key words: excess excitation energy, cellular automation, cellular light memory, Darwinian fitness, nonphotochemical quenching, photoelectrophysiological signaling, SAA, SAR