Xylogenesis, Genetic and Environmental Regulation
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lAWA Journal, Vol. 17 (3),1996: 269-310 XYLOGENESIS, GENETIC AND ENVIRONMENTAL REGULATION - A REVIEW- by Rodney Arthur Savidge Faculty of Forestry & Environmental Management, University of New Brunswick, Fredericton, NB E3B 6C2, Canada SUMMARY A critique is provided of the physical and chemical control of primary and secondary xylem development in terms of mechanics, genetics, phylogenetics, and the larger field of plant physiology. Strengths and weaknesses of the phytohormone theory of vascular development are analyzed. Homeobox genes, sub-cellular phytohormone localization, anatomical responses to varied phytohormone ratios and dosages, polar auxin transport, second messengers, radial fluxes in water potential, in tercellular signalling, lignin biochemistry, and the phylogenetic position of bryophytes in relation to xylogenesis are identified as some areas for future research. Homeodomain proteins are addressed in terms of cambial initials and cell-fate determination, and other genetic and environmen tal factors controlling differentiation of diverse cellular phenotypes are reviewed. As a 'continuum hypothesis', it is proposed that the extent of secondary wall sculpturing during tracheary element differentiation is a function of the duration of homeotic gene expression. Key words: Xylem, cambium, phytohormones, homeobox genes, second messenger, water potential, lignin, bryophytes, 'continuum hypothesis'. INTRODUCTION No plant meristem can be more abundantly obtained in pure form than the cambial zone from trees, and no developing tissue can be more readily had for molecular physi ology studies than that comprising cambial derivatives on their way to becoming wood. Curiously, the opportunities for progress have not yet been fully appreciated in the field of plant biology and, consequently, much remains to be done before any solid conclusion can be drawn about how xylogenesis is regulated in any woody species. The objective here is not simply to provide a conceptual bridge from static anatomical observations of mature woody elements to the perceived molecular dynamics of xylo genesis, but also and even more pointedly to provide students of wood anatomy with both an awareness of the limitations of current understanding and an appreciation of opportunities for future research. Wood is the most abundant form of biomass in the terrestrial biosphere; however, the vegetative sporophytic structures of higher plants comprise a variety of tissues in *) Dedicated to the memory of Philip Frank Wareing (1914-1996), pioneer in cambial physology. Downloaded from Brill.com10/09/2021 12:10:54AM via free access 270 IAWA Journal, Vol. 17 (3),1996 addition to xylem, including epidermis., endodermis, cortex, pith, phloem, photosyn thetic tissues, rhytidome, root caps, and meristems, and the function of each is presum ably just as essential as that of xylem for plant growth and survival. While it is clear that most plant tissues arise directly from meristems, knowledge about the factors initiating and controlling the formation of any kind of tissue development is still rudi mentary. In most species, xylem comprises differentiated cells of more than one type; that is, it is a complex tissue. Explaining how adjoining cells, initially of similar ap pearance and identical genetic constitution, come to appear fundamentally different presents one of the most fascinating challenges in biology. The rudiments of the theory that seasonal cambial growth and wood formation are under phytohormonal regulation arose at least a century ago (see Savidge & Wareing 198 I b for a historical review, Aloni 1995, and Little & Pharis 1995 for recent re views). The theory can be stated to the effect that phytohormones (notably auxin, but also others) produced in and exported from non-vascular tissues, such as apical meristems and leaves, promote vascular development in those cells making up their transport corridors. Following more than a half century of research, there can be no doubt that the theory has substantial merit. On the other hand, it might be more correct to say that the phytohormone theory for vascular development has never had to be defended against serious alternatives, than to argue that it has solidly withstood re peated challenges. Only by doing everything reasonable to disprove and displace a theory can it gain real credibility. Although opportunities for research with phytohormones are discussed below, my primary aim here is to re-examine some more fundamental considerations in order to develop a broader and deeper perspective about possible control mechanisms in xylem morphogenesis. LOGIC UNDERLYING PHYSIOLOGICAL INVESTIGATIONS Physiology is the study of the growth, development and functioning of a living organ ism and how those processes are regulated by the organism itself as well as by its external environment. As indicated in Figure I, morphology, anatomy, cytology, ge netics, biochemistry, and ultrastructural investigations all come under the umbrella of 1'llYSIOLOGy MORPHOLOGY Anatomy Cytology Fine structure studies Genetics Molecular structure Biochemistry Thermodynamics Organic chemistry Mechanical theory Inorganic chemistry Electromagnetic theory Physical chemistry Nuclear physics Quantum mechanical theory Fig. 1. Physiology as a multi-disciplinary science concerned with explaining how morphogenesis occurs. Downloaded from Brill.com10/09/2021 12:10:54AM via free access Savidge - Xylogenesis 271 physiology, each presenting a different physical or chemical 'window' on the control of morphogenesis. Plant physiology attempts to integrate this multi-disciplinary infor mation into a larger, coordinated picture to explain how plants capture energy and assimilate carbon dioxide, water, inorganic ions and other substances into physically and chemically complex forms of biomass. The first principle of biology is that 'Laws of chemistry and physics govern living systems', and physiology ultimately reduces to considerations of the organism as all three states of matter (comprising thousands of different molecular species) and differ ent kinds of energy interacting in space over time. Physical chemistry is concerned with very similar problems to those of nuclear physics, and phenomena addressed by both reduce to considerations that are explained in terms of quantum mechanical theory (Fig. 1). Thus, although a scientist may choose to see and analyze a phenomenon such as xylogenesis using a physical, chemical or genetical approach, biological phenom ena per se must involve interactions of matter and energy that cannot occur in isola tion. In this light, any singular physical, chemical or genetical explanation advanced for the regulation of xylogenesis (for example, control by pressure, auxin, or DNA binding proteins) can at best be regarded as merely a starting point in understanding; it should not discourage testing of new ideas and continuing integration of knowledge. Approaches toward explaining the control of physiological processes at tissue or finer levels can logically be separated into considerations of intrinsic and extrinsic factors (Fig. 2). Intrinsic factors are those generated internally by the plant itself, and extrinsic factors constitute everything else -living and non-living - affecting the plant. Not all extrinsic factors are exclusively external, nor do all intrinsic factors remain exclusively internal to the plant. For example, microorganisms as extrinsic factors occur commonly within plants (e.g., xylem-limited bacteria and endophytes) as well as externally, and parasites (e.g., mistletoe) or fungi (e.g., mycorrhizae) may simulta neously reside in both locations (Ng et al. 1982; Fett et al. 1987). Intrinsically gener ated factors such as ethylene may emanate from a plant and elicit a response as a component of the plant's extrinsic environment. Factor (intrinsic or extrinsic) role? I PROMOTER INHIBITOR I I nature? nature? I I I I PHYSICAL CHEMICAL PHYSICAL CHEMICAL I I I I identity? identity? identity? identity? I I I I mobility? mobility? mobility? mobility? Fig. 2. Flow diagram indicating questions that should be answered at the beginning of any physiological investigation. Downloaded from Brill.com10/09/2021 12:10:54AM via free access 272 IAWA Journal, Vol. 17 (3), 1996 The investigative process to explain the control of morphogenesis traditionally has be gun by determining whether intrinsic or extrinsic promoters or inhibitors exist (Fig. 2). To accomplish this, a bioassay simulating whatever aspect of morphogenesis happens to be under investigation must be devised. Five complimentary bioassay systems have been used to investigate the regulation of xylogenesis. I) Cell-free soluble, particulate and organellar systems have been investigated by biochemists and biophysicists to determine the enzymes, kinds of energy, and other factors affecting development at the sub-cellular level (Bevan & Northcote 1979; Demura & Fukuda 1993; Northcote 1993; Forster & Savidge 1995; Udagama-Randeniya & Savidge 1995). Enzymatic bioassays can, upon isolation of the enzyme, lead to characterization and manipulation of genes associated with cellular differentiation or morphogenesis (Demura & Fukuda 1994; Antosiewicz et al. 1995). Biophysical investigations can lead to a better understanding of the relationship between structure and function (Hasenstein & Rayle 1984; Roberts 1992; Wildon et al. 1992; Roberts & Haigler 1994). In addition, thermodynamic analyses can provide a rational basis for predicting the likelihood of a particular