Julius Sachs (1868): The father of plant physiology.

The year 2018 marks the 150th anniversary of the first publication of Julius von Sachs' (1832-1897) Lehrbuch der Botanik (Textbook of Botany), which provided a comprehensive summary of what was then known about the plant sciences. Three years earlier, in 1865, Sachs produced the equally impressive Handbuch der Experimental-Physiologie der Pflanzen (Handbook of Experimental Plant Physiology), which summarized the state of knowledge in all aspects of the discipline known today as plant physiology. Both of these books provided numerous insights based on Sachs' seminal experiments. By virtue of a reliance on detailed empirical observation and the rigorous application of chemical and physical principles, it is fair to say that the publication of these two monumental works marked the beginning of what can be called "modern-day" plant science. Moreover, Sachs' Lehrbuch der Botanik prefigured the ascendance of plant molecular biology and the systems biology of photoautotrophic organisms. Regrettably, many of the insights of this great scientist have been forgotten by the generations who followed. It is only fitting, therefore, that the anniversary of the publication of the Lehrbuch der Botanik and the career of "the father of plant physiology" should be honored and reviewed, particularly because Sachs established the physiology of green organisms as an integral branch of botany and incorporated a Darwinian perspective into plant biology. Here we highlight key insights, with particular emphasis on Sachs' detailed discussion of sexual reproduction at the cellular level and his endorsement of Darwinian evolution.

Phototropic solar tracking in sunflower plants: an integrative perspective.

BACKGROUND: One of the best-known plant movements, phototropic solar tracking in sunflower (Helianthus annuus), has not yet been fully characterized. Two questions are still a matter of debate. (1) Is the adaptive significance solely an optimization of photosynthesis via the exposure of the leaves to the sun? (2) Is shade avoidance involved in this process? In this study, these concepts are discussed from a historical perspective and novel insights are provided. SCOPE AND METHODS: Results from the primary literature on heliotropic growth movements led to the conclusion that these responses cease before anthesis, so that the flowering heads point to the East. Based on observations on 10-week-old plants, the diurnal East-West oscillations of the upper fifth of the growing stem and leaves in relation to the position of the sun (inclusive of nocturnal re-orientation) were documented, and photon fluence rates on the leaf surfaces on clear, cloudy and rainy days were determined. In addition, the light-response curve of net CO2 assimilation was determined on the upper leaves of the same batch of plants, and evidence for the occurrence of shade-avoidance responses in growing sunflower plants is summarized. CONCLUSIONS: Only elongating, vegetative sunflower shoots and the upper leaves perform phototropic solar tracking. Photon fluence response and CO2 assimilation measurements cast doubt on the 'photosynthesis-optimization hypothesis' as the sole explanation for the evolution of these plant movements. We suggest that the shade-avoidance response, which maximizes light-driven CO2 assimilation, plays a major role in solar tracking populations of competing sunflower plants, and an integrative scheme of these growth movements is provided.

Did meiosis evolve before sex and the evolution of eukaryotic life cycles?

Biologists have long theorized about the evolution of life cycles, meiosis, and sexual reproduction. We revisit these topics and propose that the fundamental difference between life cycles is where and when multicellularity is expressed. We develop a scenario to explain the evolutionary transition from the life cycle of a unicellular organism to one in which multicellularity is expressed in either the haploid or diploid phase, or both. We propose further that meiosis might have evolved as a mechanism to correct for spontaneous whole-genome duplication (auto-polyploidy) and thus before the evolution of sexual reproduction sensu stricto (i.e. the formation of a diploid zygote via the fusion of haploid gametes) in the major eukaryotic clades. In addition, we propose, as others have, that sexual reproduction, which predominates in all eukaryotic clades, has many different advantages among which is that it produces variability among offspring and thus reduces sibling competition.

Blue light-induced proteomic changes in etiolated Arabidopsis seedlings.

Plants adapt to environmental light conditions by photoreceptor-mediated physiological responses, but the mechanism by which photoreceptors perceive and transduce the signals is still unresolved. Here, we used 2D difference gel electrophoresis (2D DIGE) and mass spectrometry to characterize early molecular events induced by short blue light exposures in etiolated Arabidopsis seedlings. We observed the phosphorylation of phototropin 1 (phot1) and accumulation of weak chloroplast movement under blue light 1 (WEB1) in the membrane fraction after blue light irradiation. Over 50 spots could be observed for the two rows of phot1 spots in the 2-DE gels, and eight novel phosphorylated Ser/Thr sites were identified in the N-terminus and Hinge 1 regions of phot1 in vivo. Blue light caused ubiquitination of phot1, and K526 of phot1 was identified as a putative ubiquitination site. Our study indicates that post-translational modification of phot1 is more complex than previously reported.

Amphimixis and the individual in evolving populations: does Weismann's Doctrine apply to all, most or a few organisms?

The German biologist August Weismann (1834-1914) proposed that amphimixis (sexual reproduction) creates variability for natural selection to act upon, and hence he became one of the founders of the Neo-Darwinian theory of biological evolution. He is perhaps best known for what is called "Weismann's Doctrine" or "Weismann's Barrier" (i.e. the irreversible separation of somatic and germ cell functionalities early during ontogeny in multicellular organisms). This concept provided an unassailable argument against "soft inheritance" sensu Lamarck and informed subsequent theorists that the only "individual" in the context of evolution is the mature, reproductive organism. Herein, we review representative model organisms whose embryology conforms to Weismann's Doctrine (e.g. flies and mammals) and those that do not (e.g. freshwater hydroids and plants) based on this survey and the Five Kingdoms of Life scheme; we point out that most species (notably bacteria, fungi, protists and plants) are "non-Weismannian" in ways that make a canonical definition of the "individual" problematic if not impossible. We also review critical life history functional traits that allow us to create a matrix of all theoretically conceivable life cycles (for eukaryotic algae, embryophytes, fungi and animals), which permits us to establish where this scheme Weismann's Doctrine holds true and where it does not. In addition, we argue that bacteria, the dominant organisms of the biosphere, exist in super-cellular biofilms but rarely as single (planktonic) microbes. Our analysis attempts to show that competition among genomic variants in cell lineages played a critical part in the evolution of multicellularity and life cycle diversity. This feature was largely ignored during the formulation of the synthetic theory of biological evolution and its subsequent elaborations.

Antonie van Leeuwenhoek (1632-1723): Master of Fleas and Father of Microbiology.

The Dutch scientist and entrepreneur Antonie van Leeuwenhoek (1632-1723) was the first to discover and describe microorganisms (protists, bacteria), living beings he characterized as "animalcules" (little animals) [...].

Mendel-200: Pea as a model system to analyze hormone-mediated stem elongation.

In a recent Review Article on Gregor Mendel's (1822-1884) work with pea (Pisum sativum)-plants, it was proposed that this crop species should be re-vitalized as a model organism for the study of cell- and organ growth. Here, we describe the effect of exogenous gibberellic acid (GA3) on the growth of the second internode in 4-day-old light-grown pea seedlings (Pisum sativum, large var. "Senator"). lnjection of glucose into the internode caused a growth-promoting effect similar to that of the hormone GA3. Imbibition of dry pea seeds in GA3, or water as control, resulted in a drastic enhancement in organ development in this tall variety. Similar results were reported for dwarf peas. These "classical" experimental protocols are suitable to study the elusive effect of gibberellins (which act in coordination with auxin) on the regulation of plant development at the biochemical and molecular levels.

Root phototropism: from dogma to the mechanism of blue light perception.

In roots, the "hidden half" of all land plants, gravity is an important signal that determines the direction of growth in the soil. Hence, positive gravitropism has been studied in detail. However, since the 19th century, the response of roots toward unilateral light has also been analyzed. Based on studies on white mustard (Sinapis alba) seedlings, botanists have concluded that all roots are negatively phototropic. This "Sinapis-dogma" was refuted in a seminal study on root phototropism published a century ago, where it was shown that less then half of the 166 plant species investigated behave like S. alba, whereas 53% displayed no phototropic response at all. Here we summarize the history of research on root phototropism, discuss this phenomenon with reference to unpublished data on garden cress (Lepidium sativum) seedlings, and describe the effects of blue light on the negative bending response in Thale cress (Arabidopsis thaliana). The ecological significance of root phototropism is discussed and the relationships between gravi- and phototropism are outlined, with respect to the starch-statolith-theory of gravity perception. Finally, we present an integrative model of gravi- and blue light perception in the root tip of Arabidopsis seedlings. This hypothesis is based on our current view of the starch-statolith-concept and light sensing via the cytoplasmic red/blue light photoreceptor phytochrome A and the plasma membrane-associated blue light receptor phototropin-1. Open questions and possible research agendas for the future are summarized.

Brassinosteroid action in flowering plants: a Darwinian perspective.

The year 2012 marks the 150th anniversary of the publication of Charles Darwin's first botanical book, on the fertilization of orchids (1862), wherein he described pollen grains and outlined his evolutionary principles with respect to plant research. Five decades later, the growth-promoting effect of extracts of Orchid pollen on coleoptile elongation was documented. These studies led to the discovery of a new class of phytohormones, the brassinosteroids (BRs) that were isolated from rapeseed (Brassica napus) pollen. These growth-promoting steroids, which regulate height, fertility, and seed-filling in crop plants such as rice (Oryza sativa), also induce stress- and disease resistance in green algae and angiosperms. The origin and current status of BR-research is described here, with reference to BR-action and -signal transduction, and it is shown that modern high-yield rice varieties with erect leaves are deficient in endogenous BRs. Since brassinosteroids induce pathogen resistance in rice plants and hence can suppress rice blast- and bacterial blight-diseases, genetic manipulation of BR-biosynthesis or -perception may be a means to increase crop production. Basic research on BR activity in plants, such as Arabidopsis and rice, has the potential to increase crop yields further as part of a 21th century 'green biotech-revolution' that can be traced back to Darwin's classical breeding experiments. It is concluded that 'Nothing in brassinosteroid research makes sense except in the light of Darwinian evolution' and the value of basic science is highlighted, with reference to the genetic engineering of better food crops that may become resistant to a variety of plant diseases.

Forever young: stem cell and plant regeneration one century after Haberlandt 1921.

Plants are characterized by a post-embryonic mode of organ development, which results in a need for these photoautotrophic organisms to regenerate lost parts in the course of their life cycle. This capacity depends on the presence of "pluripotent stem cells," which are part of the meristems within the plant body. One hundred years ago, the botanist Gottlieb Haberlandt (1854-1945) published experiments showing wounding-induced callus formation, which led ultimately to plant regeneration in tissue culture and thence to the techniques of "plant biotechnology," with practical applications for mankind. Here, we recount Haberlandt's discovery within the context of his long research life and his most influential book Physiologische Pflanzenanatomie. In the second part, we describe and analyze a plant tissue-culture regeneration system using sterile, dark-grown sunflower (Helianthus annuus) seedlings as experimental material. We document that excised hook segments, which contain a "stem cell niche," can regenerate entire miniature H. annuus-plantlets that, raised in a light/dark regime, develop flowers. Finally, we discuss molecular data relevant to plant regeneration with reference to phytohormones and conclude that, one century after Haberlandt, 1921, the exact biochemical/genetic mechanisms responsible for the capability of stem cells to remain "forever young" are, although already complex, really just beginning to become known.

On the historical roots of creationism and intelligent design: German Allmacht and Darwinian evolution in context.

As detailed in a Letter published in Science in 2017, the adherents of creationism and intelligent design are still active in promoting their biblical-literalist views of the origin and evolution of life on Earth. In this contribution, we take a look at this ideological phenomenon in the USA and analyze the philosophical roots of this ongoing movement. Specifically, we discuss Vernon Kellogg's book entitled Headquarters Nights (1917) with reference to the German 'Allmacht' (English-omnipotence) and Darwinian evolution to demonstrate how this publication bolstered the development of active anti-evolutionism in the USA among American fundamentalist Christians, inclusive of the Intelligent Design (ID)-agenda. The current activities of creationist associations in the USA and Germany are summarized, with reference to a new pro-ID-group established in Austria in 2019 that is sponsored by the Discovery Institute in Seattle, Washington (USA).

The evolution of the land plant life cycle.

The extant land plants are unique among the monophyletic clade of photosynthetic eukaryotes, which consists of the green algae (chlorophytes), the charophycean algae (charophytes), numerous groups of unicellular algae (prasinophytes) and the embryophytes, by possessing, firstly, a sexual life cycle characterized by an alternation between a haploid, gametophytic and a diploid, sporophytic multicellular generation; secondly, the formation of egg cells within multicellular structures called archegonia; and, thirdly, the retention of the zygote and diploid sporophyte embryo within the archegonium. We review the developmental, paleobotanical and molecular evidence indicating that: the embryophytes descended from a charophyte-like ancestor; this common ancestor had a life cycle with only a haploid multicellular generation; and the most ancient (c. 410 Myr old) land plants (e.g. Cooksonia, Rhynia and Zosterophyllum) had a dimorphic life cycle (i.e. their haploid and diploid generations were morphologically different). On the basis of these findings, we suggest that the multicellular reproductive structures of extant charophytes and embryophytes are developmentally homologous, and that those of the embryophytes evolved by virtue of the co-option and re-deployment of ancient algal homeodomain gene networks.

Auxin action in developing maize coleoptiles: challenges and open questions.

The year 2020 marks the 150th anniversary of the elucidation of the process of plant organ growth at the cellular level by Julius Sachs (1870). In this Addendum to a Review Article in Molecular Plant, we describe this fundamental discovery and argue that the etiolated grass coleoptile still represents the system of choice for the experimental analysis of auxin (indole-3-acetic acid, IAA)-action. With reference to the phenomenon of 'tissue tension', we discuss the acid-growth hypotheses of IAA-induced wall loosening and the process of vacuolar expansion, respectively. IAA-mediated elongation appears to be independent of wall acidification, and may be regulated via the secretion of glycoproteins into the outer epidermal wall, whereby turgor (and tissue) pressure provides the 'driving force' for growth. As predicted by the "acid growth-hypothesis", the fungal phytotoxin Fusicoccin (Fc) induces organ elongation via the rapid secretion of protons. We conclude that "cell elongation" can only be understood at the level of the entire organ that displays biomechanical features not established by single cells. This systems-level approach can be traced back to the work of Sachs (1870).

Ernst Haeckel, ancient forests, and the Anthropocene.

In this Addendum to an article in  Nature commemorating the 100th anniversary of Ernst Haeckel's death (9 August 1919), we recall the largely forgotten fact that Haeckel (1868) was an early proponent of the concept of an "Anthropozoic Age", a 19th-century anticipation of the "Anthropocene". Haeckel in particular highlighted man's extensive remodeling of the planet in ancient forests. Earlier influences on Haeckel included Alexander von Humboldt (1769-1859) and dozens of similar writers in the 19th century Romantic era, including the Italian geologist and priest Antonio Stoppani (1824-1891), and the American diplomat and environmentalist George P. Marsh (1801-1882). Starting in the 1840s, Marsh described in extraordinary detail the destructive influence of mankind on natural ecosystems, again with particular emphasis on the destruction of forests. Marsh, like Haeckel after him, was a pioneer in describing the far-reaching human re-modeling of the planet that they and their colleagues presciently labeled the "Anthropozoic Age".

The Warburg-effects: basic metabolic processes with reference to cancer development and global photosynthesis.

One century ago (1920), Otto Warburg (1883-1970) discovered that in liquid cultures of unicellular green algae (Chlorella sp.) molecular oxygen (O2) exerts an inhibitory effect on photosynthesis. Decades later, O2 dependent suppression of photosynthetic carbon dioxide (CO2) assimilation (the "green" Warbur geffect) was confirmed on the leaves of seed plants. Here, we summarize the history of this discovery and elucidate the consequences of the photorespiratory pathway in land plants with reference to unpublished CO2 exchange data measured on the leaves of sunflower (Helianthus annuus) plants. In addition, we discuss the inefficiency of the key enzyme Rubisco and analyze data concerning the productivity of C3 vs. C4 crop species (sunflower vs. maize, Zea mays). Warburg's discovery inaugurated a research agenda in the biochemistry of photosynthetic CO2 assimilation that continues to the present. In addition, we briefly discuss Warburg's model of metabolic processes in cancer, net primary production (global photosynthesis) with respect to climate change, trees and other land plants as CO2 removers, and potential climate mitigators in the Anthropocene.

Charles Darwin's Origin of Species, directional selection, and the evolutionary sciences today.

The book On the Origin of Species, published in November 1859, is an "abstract" without references, compiled by Charles Darwin from a much longer manuscript entitled "Natural Selection." Here, I summarize the five theories that can be extracted from Darwin's monograph, explain the true meaning of the phrase "struggle for life" (i.e., competition and cooperation), and outline Darwin's original concept of natural selection in populations of animals and plants. Since neither Darwin nor Alfred R. Wallace distinguished between stabilizing and directional natural selection, the popular argument that "selection only eliminates but is not creative" is still alive today. However, I document that August Weismann (Die Bedeutung der sexuellen Fortpflanzung für die Selektions-Theorie. Gustav Fischer-Verlag, Jena, 1886) and Ivan Schmalhausen (Factors of evolution. The theory of stabilizing selection. The Blackiston Company, Philadelphia, 1949) provided precise definitions for directional (dynamic) selection in nature and illustrate this "Weismann-Schmalhausen principle" with respect to the evolutionary development of novel phenotypes. Then, the modern (synthetic) theory of biological evolution that is based on the work of Theodosius Dobzhansky (Genetics and the origin of species. Columbia University Press, New York, 1937) and others, and the expanded version of this system of theories, are outlined. Finally, I document that symbiogenesis (i.e., primary endosymbiosis, a process that gave rise to the first eukaryotic cells), ongoing directional natural selection, and the dynamic Earth (plate tectonics, i.e., geological events that both created and destroyed terrestrial and aquatic habitats) were the key processes responsible for the documented macroevolutionary patterns in all five kingdoms of life. Since the evolutionary development of the earliest archaic bacteria more than 3,500 mya, the biosphere of our dynamic planet has been dominated by prokaryotic microbes. Eubacteria, Archaea, and Cyanobacteria are, together with eukaryotic microorganisms (marine phytoplankton, etc.), the hidden "winners" in the Darwinian struggle for existence in nature.

Evolutionary plant physiology: Charles Darwin's forgotten synthesis.

Charles Darwin dedicated more than 20 years of his life to a variety of investigations on higher plants (angiosperms). It has been implicitly assumed that these studies in the fields of descriptive botany and experimental plant physiology were carried out to corroborate his principle of descent with modification. However, Darwin's son Francis, who was a professional plant biologist, pointed out that the interests of his father were both of a physiological and an evolutionary nature. In this article, we describe Darwin's work on the physiology of higher plants from a modern perspective, with reference to the following topics: circumnutations, tropisms and the endogenous oscillator model; the evolutionary patterns of auxin action; the root-brain hypothesis; phloem structure and photosynthesis research; endosymbioses and growth-promoting bacteria; photomorphogenesis and phenotypic plasticity; basal metabolic rate, the Pfeffer-Kleiber relationship and metabolic optimality theory with respect to adaptive evolution; and developmental constraints versus functional equivalence in relationship to directional natural selection. Based on a review of these various fields of inquiry, we deduce the existence of a Darwinian (evolutionary) approach to plant physiology and define this emerging scientific discipline as the experimental study and theoretical analysis of the functions of green, sessile organisms from a phylogenetic perspective.

Light and plant development: the discovery of phototropins by Winslow R. Briggs (1928-2019).

The American biologist Winslow Russel Briggs (1928-2019) was a global leader in plant physiology, genetics and photobiology. In this contribution, we try to share our knowledge of the remarkable career of this outstanding scientist. After earning his PhD at Harvard (Cambridge, Massachusetts), he started his independent research program at Stanford University (California). Among many major contributions was his elegant experiment that conclusively demonstrated the role of auxin transport in the phototropic bending response of grass coleoptiles. During subsequent years as Professor of biology at Harvard University, Briggs focused on phytochrome and photomorphogenesis. In 1973, he re-located to Stanford to become Director of the Department of Plant Biology, Carnegie Institution for Science, and faculty member in the Biology Department at Stanford University. After his retirement (1993), he continued his research on "light and plant development" as an emeritus at Carnegie until the day of his death on February 11, 2019. Through his long research career, Briggs stayed at the cutting edge by re-inventing himself from a plant physiologist, to biochemist, geneticist, and molecular biologist. He made numerous discoveries, including the LOV-domain photoreceptor phototropin. Winslow Briggs, who was also a naturalist and gifted pianist, inspired and promoted the work of generations of young scientists - as mentor, colleague and friend.