Introduction

The goal of this article is to reintroduce and reconsider the implications of a seminal paper written by the famous German botanist Julius Sachs (1832 – 1897) (Fig. 1). The salient concept proposed in his paper is that of the energid (Energide), which Sachs defined as “a nucleus together with the corresponding protoplasm that is governed by it” in his paper entitled “Physiologische Notizen. II. Beiträge zur Zellentheorie. a) Energiden und Zellen” (Physiological Notes. II. Contributions to the theory of the cell. a) Energids and cells) (Sachs 1892, p. 59). A first translation of this paper into English accompanies this introductory article online and in this issue of Biological Theory. Herein, we argue that the concept of the energid remains pertinent even in the age of molecular biology, because the idea that the nucleus can only “control” so much cytoplasm presaged the discovery of messenger RNA. Moreover, the historical resistance to the energid concept revolved around a deep-seated philosophical debate between those adhering to the cell theory as articulated originally by Matthias Schleiden (1804 – 1881) and Theodor Schwann (1810 – 1882) versus the organismal theory as articulated by advocates such as Rudolf Virchow (1821 – 1902) and Kurt Goldstein (1878 – 1965), a controversy that to some degree continues on into recent time in the context of interpreting developmental data (as summarized by Baluska and Lyons 2018; see also Gregg 1959).

Fig. 1
figure 1

(from Wikimedia Commons, https://commons.wikimedia.org/wiki/File:Julius_Sachs.jpg#filehistory)

A portrait of Julius Sachs taken in 1893

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In the following sections, we briefly review the career of Julius Sachs, present a synopsis of his conceptualization of the energid, trace its importance during the development of the dichotomy between the symplast (i.e., the living components of a cell, tissue, or entire organism) and the apoplast (i.e., the metabolically inert components of a cell, tissue, or entire organism), and discuss its relevance to the cell theory and the organismic theory as an emergent debate following the Schleiden–Schwann concept of the cell. Importantly, although Sachs is traditionally thought of as a botanist, particularly a plant physiologist, his inclination and training made him a biological polymath. As a consequence, his conceptualization of the energid is as relevant to the zoologist and mycologist as it to the botanist (Gimmler 1984).

A Brief Review of the Major Contributions of Julius Sachs

The career of Julius Sachs has been described in the classical monograph of Pringsheim (1932), from which the portrait shown in Fig. 1 was reproduced. Recently, we reviewed his life and achievements to justify the historical background permitting him to be called “the father of plant physiology” (see Kutschera and Niklas 2018a, b). This appellation is justified here by noting that in his relatively short academic career as a scientist (working in Prague, Tharandt, Poppelsdorf/Bonn, Freiburg, and in Würzburg), Sachs published four comprehensive and profoundly influential textbooks: the Handbuch der Experimental-Physiologie der Pflanzen in 1865 (Handbook of Experimental Plant Physiology), the Lehrbuch der Botanik in 1868, (Textbook of Botany, fourth edition in 1874), the Geschichte der Botanik in 1875 (History of Botany), and, his magnum opus, the Vorlesungen über Pfanzen-Physiologie (Lectures on the Physiology of Plants) in 1882 and a second edition in 1887. With these major contributions to the literature and his many practical contributions to agriculture (e.g., abandoning the expensive silicon-soil supplemental treatments so popular with the farmers of his day), Sachs almost single-handedly created what is called today experimental physiology, as well as plant molecular and systems biology (Kutschera and Niklas 2018b).

What typically goes unnoticed is the fact that Sachs was an exceptionally broadly trained biologist. For example, when he was 21 years old, Sachs published a paper on the anatomy of the widely distributed and economically important European crayfish (Astacus astacus) (Sachs 1853). This publication reveals that Sachs was as well trained in zoology as in botany (as well as a skilled artist) with a remarkably broad understanding of cellular and organismic morphology and physiology (Kutschera and Baluska 2015). This assertion is particularly relevant here because it adds some measure of authority to Sachs’s proposition that the term “cell” (Zelle), in the sense of the “Elementarorganismus” or the “basic, minimal living unit” (Brücke 1861), is misleading. Accordingly, it should be replaced by the term “energid” (Energide), which Sachs (1892) defined as “a nucleus together with the corresponding protoplasm that is governed by it.” Given his broad biological training and interests, we have every reason to believe that Sachs’s concept of the energid was not meant to be limited to plants, but rather that it was meant to apply equally to all eukaryotes (plants, animals, and fungi) regardless of whether they are unicellular or multicellular. We shall return to this point, but only after discussing the concept of the energid in greater detail and placing it in the context of the “cellular versus organismic” debate.

The Concept of the Energid (Energide)

In 1878, Sachs published a little-known article in the Sitzungsberichte der Physikalisch-Medizinischen Gesellschaft Würzburg (Meeting reports of the Physical-Medical Society of Würzburg). In this note entitled "Ueber nichtzelluläre Pflanzen” (On noncellular plants), Sachs (1878) briefly introduced his ideas concerning the energid. However, in his Vorlesungen über Pflanzen-Physiologie, Sachs (1887) did not introduce this novel concept. He mentioned that a discussion as to the nature of the cell was beyond the scope of his popular treatment of the physiological processes occurring in plants and algae, written for a general audience. Five years later, in a journal paper dealing with this topic, Sachs (1892) makes three explicit assertions: (1) the energid (Energide) is a nucleus and the protoplasm that is governed by it, (2) the nucleus and the cytoplasm it controls must be regarded as the fundamental building block out of which all organisms are constructed, and (3) the concepts of the energid and the cell, as articulated by Robert Hooke (1635–1702) in 1665 and subsequently canonized in the cell theory by Matthias J. Schleiden (1804–1881) and Theodor Schwann (1810–1882) in 1839, are not the same things. There is no a priori reason why the nucleus and its attending cytoplasm need be spatially confined or delimited by either a cell membrane or a cell wall (as in animals and plants, respectively).

In hindsight, it is tempting to see the first of these three assertions as foreshadowing the existence of mRNA for two reasons. First, Sachs assigns the nucleus as having the leading role in the energid, rather than the cytoplasm; and, second, as a physiologist he implicitly considers the controlling factor to be chemical in nature. Sachs’s second and third assertions are equally intriguing because when taken together they are a subtle (albeit clear) attack on the prevailing concept of the cell as a spatially defined organic entity. Indeed, later in his paper, Sachs points out that many “cells” (in the traditional sense of the word), particularly in the land plants and algae, are multinucleate, e.g., bast fibers and algae such as Caulerpa (Fig. 2). Three years later, Sachs (1895) published a second article on his concept of the energid, wherein he added some details, without changing his basic ideas as articulated in 1892.

Fig. 2
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Caulerpa, a coenocytic (multinucleated unicellular) marine green alga (original photo by K. J. Niklas)

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It should be noted that the eminent Swiss zoologist/anatomist and physiologist Albert von Kölliker (1817 – 1905), who was a colleague of Sachs at the University of Würzburg, accepted Sachs’s ideas and applied them to the tissues of animals. However, Kölliker’s article (1897) was published in a little-known local journal and consequently had little or no long-lasting affect, as detailed below.

From the Energid to the Symplast-Apoplast Concept

The eminent German botanist Wilhelm Pfeffer (1845 – 1920) is considered to be a co-founder of experimental plant physiology (Kutschera and Niklas 2018a, b), based on his editing and contributing to the monumental monograph entitled Pflanzenphysiologie (Plant Physiology), published in 1895. The second edition of this two-volume book (rewritten by Pfeffer 1897) appeared in print five months after Sachs had died. Unfortunately, Julius Sachs was a very dogmatic person, especially during his final years, when he suffered from undisclosed illnesses, which may have been related to his persistent and heavy smoking (Pringsheim 1932; Gimmler 1984; Kutschera and Briggs 2009; Kutschera and Niklas 2018a, b). This may be why his paper on the “Energiden und Zellen” (Sachs 1892) was written in a polemical style, which displeased many of his colleagues.

Although an adherent of many of Sachs’s insights and theories, Pfeffer (1897) only briefly referred to the energid concept of Sachs (1878), wherein he proposed the existence of “unicellular plants,” and then thoroughly rejected this idea of his former mentor. Contra Sachs, Pfeffer (1897) advocated the view that a protoplast can contain either one nucleus (monoplast) or numerous nuclei (symplast). The terms “monoplast” and “symplast” were first coined by the botanist Johannes Hanstein (1822 –1880). In his Botanische Abhandlungen, Hanstein argued that "Verschmelzungen mehrerer Mono- oder Protoplasten (dürften) in ihrer Ganzheit als 'symplasten' zu charakterisieren sein” (the fusions of several mono- or protoplasts (may be) characterized in their completeness as ‘symplasts’) (Hanstein 1880). Pfeffer (1897) argued further that the mass of cytoplasm containing numerous nuclei may be influenced by several nuclei, not just one, as suggested by Sachs (1892, 1895). Nevertheless, Pfeffer (1897) defined a multinucleated protoplast as a “symplast.”

Three decades later, the word “symplast” was used by the German botanist Ernst Münch (1876 – 1946), notably in his influential book Die Stoffbewegungen in der Pflanzen (Material Flow in Plants). In addition, Münch (1930) reintroduced the concept of the symplast (i.e., the living metabolically active part of a cell) versus the apoplast (i.e., the non-metabolically active parts within a cell). Hence, we can reconstruct a logical line of descent, starting with the concept of the energid (Sachs 1892, 1895) and the idea of the symplast (Hanstein 1880; Pfeffer 1897) to the division of the multicellular bodyplan into the symplast and the apoplast (Münch 1930). Thus, the ideas of Sachs (1892, 1895) are still alive today, but in a modified form (see Knoblauch and Peters 2017).

The “Cellular Versus Organismic” Debate

As noted in the introduction, two competing theories have been proposed regarding the basic architectural composition of biological entities (and ultimately the nature of multicellularity in late divergent lineages such as the land plants and metazoans). These two theories can be called the cell theory and the organismal theory as articulated respectively by Rudolf Virchow’s (1821 – 1902) proclamation “Omis cellula e cellula” (each cell comes from another cell) and Heinrich de Bary’s (1831 – 1888) counterproposal that “Die Pflanze bildet Zellen, nicht die Zelle bildet Pflanzen” (plants make cells, cells do not build plants). In essence both of these theories emerged as an affirmation of (or as a negative reaction to) the notion that all organisms are either single-celled or composed of many cells, a perspective that can be called the Schleiden–Schwann Weltanschauungen. The fundamental developmental and phylogenetic precepts of both of these theories are provided in Table 1.

Table 1 Developmental and Phylogenetic Precepts of the Cell and Organismal Theories
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Perhaps the best expression of how the organismal theory relates to multicellularity can be found in the cellular architecture of the land plants (and many algal lineages as diverse as the brown and red algae). In these organisms, the cytoplasm is not really partitioned into individual cells because the entire cytoplasm is a more or less continuous phase from one cell to another, which is only incompletely compartmentalized by cell walls. In the parlance of the German botanist Ernst Münch, the body plan of the land plants consists of a single symplast incompletely subdivided by an apoplast. The terms “symplast” and “apoplast” refer to the living and nonliving component within an organism (Münch 1930; see Knoblauch and Peters 2017).

Unlike cell division in animals, cellular division in the land plants involves the intercalation of a cell wall. Upon the completion of cell division and the formation of the cell wall, anatomically complex intercellular strands of cytoplasm passing through the intervening cell wall (called plasmodesmata) interconnect the protoplasm of adjoining cells, thereby forming a continuous symplast throughout the multicellular body plan of the land plants. It is because of this difference in cell delimitation that the cell theory concept relies on qualitative homology criteria rather than positional criteria. However, in plants positional criteria are of greater significance in judgments of cell and organism relationships. It is because of this conceptual delineation that the American botanist Donald R. Kaplan (1938 – 2007) concluded that, “the procrustean and artificial nature of past interpretations have resulted from either the misapplication of homology criteria or the attempt to force plant histogenesis into animal cell models that are inappropriate” (Kaplan 1992; see also Niklas and Kaplan 1991). This idea has been corroborated by numerous studies, as summarized in recent textbooks on the physiology and evolution of plants (Niklas 2016; Kutschera 2019).

Conclusions

The relevancy of the energid concept to recent advancements in biology has resurfaced in a variety of contexts, including the evolutionary origin of the eukaryotic cell. Indeed, it has been argued that resistance to the energid concept is linked in part to an opposition to accepting the endosymbiotic origin of the nucleus (see Baluska and Lyons 2018). Whether this conjecture is true remains problematic particularly from a contemporary perspective, because the failure to cite the older literature is as easily attributable to a predilection among many researchers to ignore (or be unaware of) classical studies as it is a reflection of disagreeing with “old and out of date” concepts. However, our review of Sachs’s original publications causes us to find considerable merit in the energid conceptualization in addressing a broad spectrum of biological issues, such as the discovery of mRNA. It also relates to the application of research tools, like genomics, proteomics, and metabolomics, in the sense that the interpretation of data collected using these tools must consider multicellular organisms as highly integrated phenotypes rather than as disconnected confederations of “cellular aggregates.” In some contexts, analyses by necessity must focus at the level of the individual cell. In other contexts, it is necessary to focus on the entire organism, even if it is constructed of only a few cells. It is for this reason that we here provide a German-to-English translation of Sachs’s seminal paper, in our companion article on this topic (https://doi.org/10.1007/s13752-022-00399-w).