Annual Review of Plant Biology - Volume 50, 1999

During photosynthesis, energy from solar radiation is used to convert atmospheric carbon dioxide into intermediates that are used within and outside the chloroplast for a multitude of metabolic pathways. The daily fixed carbon is exported from the chloroplasts as triose phosphates and 3-phosphoglycerate. In contrast, nongreen plastids rely on the import of carbon, mainly hexose phosphates. Most organelles require the import of phosphoenolpyruvate as an immediate substrate for carbon to enter the shikimate pathway, leading to a variety of important secondary compounds. The envelope membrane of plastids contains specific translocators that are involved in these transport processes. Elucidation of the molecular structure of some of these translocators during the past few years has provided new insights in the functioning of particular translocators. This review focuses on the characterization of different classes of phosphate translocators in plastids that mediate the transport of the phosphorylated compounds in exchange with inorganic phosphate.

In plants the biosynthesis of prenyllipids and isoprenoids proceeds via two independent pathways: (a) the cytosolic classical acetate/mevalonate pathway for the biosynthesis of sterols, sesquiterpenes, triterpenoids; and (b) the alternative, non-mevalonate 1-deoxy-d-xylulose-5-phosphate (DOXP) pathway for the biosynthesis of plastidic isoprenoids, such as carotenoids, phytol (a side-chain of chlorophylls), plastoquinone-9, isoprene, mono-, and diterpenes. Both pathways form the active C5-unit isopentenyl diphosphate (IPP) as the precursor from which all other isoprenoids are formed via head-to-tail addition. This review summarizes current knowledge of the novel 1-deoxy-d-xylulose-5-phosphate (DOXP) pathway for isopentenyl diphosphate biosynthesis, apparently located in plastids. The DOXP pathway of IPP formation starts from D-glyceraldehyde-3-phosphate (GA-3-P) and pyruvate, with DOXP-synthase as the starting enzyme. This pathway provides new insight into the regulation of chloroplast metabolism.

Although the loss of green color in senescent leaves and ripening fruits is a spectacular natural phenomenon, research on chlorophyll breakdown has been largely neglected until recently. This review summarizes knowledge about the fate of chlorophyll in degreening tissues that has been gained during the past few years. Structures of end- and intermediary products of degradation as well as the biochemistry of the porphyrin-cleaving reaction have been elucidated. The intracellular localization of the catabolic pathway is particularly important in the regulation of chlorophyll breakdown. None of the genes encoding the related catabolic enzymes has so far been isolated, which makes chlorophyll degradation an area of opportunity for future research.

The first plant protein kinase sequences were reported as recently as 1989, but by mid-1998 there were more than 500, including 175 in Arabidopsis thaliana alone. Despite this impressive pace of discovery, progress in understanding the detailed functions of protein kinases in plants has been slower. Protein serine/threonine kinases from A. thaliana can be divided into around a dozen major groups based on their sequence relationships. For each of these groups, studies on animal and fungal homologs are briefly reviewed, and direct studies of their physiological functions in plants are then discussed in more detail. The network of protein-serine/threonine kinases in plant cells appears to act as a “central processor unit” (cpu), accepting input information from receptors that sense environmental conditions, phytohormones, and other external factors, and converting it into appropriate outputs such as changes in metabolism, gene expression, and cell growth and division.

Plant foods contain almost all of the mineral and organic nutrients established as essential for human nutrition, as well as a number of unique organic phytochemicals that have been linked to the promotion of good health. Because the concentrations of many of these dietary constituents are often low in edible plant sources, research is under way to understand the physiological, biochemical, and molecular mechanisms that contribute to their transport, synthesis and accumulation in plants. This knowledge can be used to develop strategies with which to manipulate crop plants, and thereby improve their nutritional quality. Improvement strategies will differ between various nutrients, but generalizations can be made for mineral or organic nutrients. This review focuses on the plant nutritional physiology and biochemistry of two essential human nutrients, iron and vitamin E, to provide examples of the type of information that is needed, and the strategies that can be used, to improve the mineral or organic nutrient composition of plants.

The fern gametophyte has interested plant biologists for the past century because its structure and development is simple and amenable to investigation. Past studies have described many aspects of its development, including germination of the spore, patterns of cell division and differentiation, photomorphogenic or light-regulated responses, sex determination and differentiation of gametangia, hormone and pheromone responses, and fertilization. Several genes that are predicted to regulate some of these processes have been recently cloned, making it possible to analyze how these processes are controlled at a molecular level. The emergence of the fern Ceratopteris richardii as a model organism for readily identifying and characterizing mutations that affect key developmental processes in gametophytes makes it a powerful tool for dissecting the molecular mechanisms underlying these processes. If advances in gene cloning techniques and transformation are forthcoming in Ceratopteris, it is likely that the study of developmental processes in ferns will significantly contribute to our understanding of plant development and evolution beyond that which can be learned solely from studying angiosperms.

C4 plants, including maize, Flaveria, amaranth, sorghum, and an amphibious sedge Eleocharis vivipara, have been employed to elucidate the molecular mechanisms and signaling pathways that control C4 photosynthesis gene expression. Current evidence suggests that pre-existing genes were recruited for the C4 pathway after acquiring potent and surprisingly diverse regulatory elements. This review emphasizes recent advances in our understanding of the creation of C4 genes, the activities of the C4 gene promoters consisting of synergistic and combinatorial enhancers and silencers, the use of 5′ and 3′ untranslated regions for transcriptional and posttranscriptional regulations, and the function of novel transcription factors. The research has also revealed new insights into unique or universal mechanisms underlying cell-type specificity, coordinate nuclear-chloroplast actions, hormonal, metabolic, stress and light responses, and the control of enzymatic activities by phosphorylation and reductive processes.

Phytohormones influence many diverse developmental processes ranging from seed germination to root, shoot, and flower formation. Recently, mutational analysis using the model plant Arabidopsis thaliana has been instrumental in determining the individual components of specific hormone signal transduction pathways. Moreover, epistasis and suppressor studies are beginning to explain how these genes and their products relate to one another. While no hormone transduction pathway is completely understood, the genes identified to date suggest that simple molecular rules can be established to explain how plant hormone signals are transduced. This review describes some of the shared characteristics of plant hormone signal transduction pathways and the properties for informational transfer common to many of the genes that specify the transduction of the signal.

The past few decades have witnessed exciting progress in studies on the biosynthesis of cellulose. In the bacterium Acetobacter xylinum, discovery of the activator of the cellulose synthase, cyclic diguanylic acid, opened the way for obtaining high rates of in vitro synthesis of cellulose. This, in turn, led to purification of the cellulose synthase and for the cloning of genes that encode the catalytic subunit and other proteins that bind the activator and regulate its synthesis and degradation, or that control secretion and crystallization of the microfibrils. In higher plants, a family of genes has been discovered that show interesting similarities and differences from the gene in bacteria that encodes the catalytic subunit of the synthase. Genetic evidence now supports the concept that members of this family encode the catalytic subunit in these organisms, with various members showing tissue-specific expression. Although the cellulose synthase has not yet been purified to homogeneity from plants, recent progress in this area suggests that this will soon be accomplished.

Nitrate reductase (NR; EC 1.6.6.1-3) catalyzes NAD(P)H reduction of nitrate to nitrite. NR serves plants, algae, and fungi as a central point for integration of metabolism by governing flux of reduced nitrogen by several regulatory mechanisms. The NR monomer is composed of a ∼100-kD polypeptide and one each of FAD, heme-iron, and molybdenum-molybdopterin (Mo-MPT). NR has eight sequence segments: (a) N-terminal “acidic” region; (b) Mo-MPT domain with nitrate-reducing active site; (c) interface domain; (d) Hinge 1 containing serine phosphorylated in reversible activity regulation with inhibition by 14-3-3 binding protein; (e) cytochrome b domain; (f) Hinge 2; (g) FAD domain; and (h) NAD(P)H domain. The cytochrome b reductase fragment contains the active site where NAD(P)H transfers electrons to FAD. A complete three-dimensional dimeric NR structure model was built from structures of sulfite oxidase and cytochrome b reductase. Key active site residues have been investigated. NR structure, function, and regulation are now becoming understood.

Crassulacean acid metabolism (CAM) is an adaptation of photosynthesis to limited availability of water or CO2. CAM is characterized by nocturnal CO2 fixation via the cytosolic enzyme PEP carboxylase (PEPC), formation of PEP by glycolysis, malic acid accumulation in the vacuole, daytime decarboxylation of malate and CO2 re-assimilation via ribulose-1,5-bisphosphate carboxylase (RUBISCO), and regeneration of storage carbohydrates from pyruvate and/or PEP by gluconeogenesis. Within this basic framework, the pathway exhibits an extraordinary range of metabolic plasticity governed by environmental, developmental, tissue-specific, hormonal, and circadian cues. Characterization of genes encoding key CAM enzymes has shown that a combination of transcriptional, posttranscriptional, translational, and posttranslational regulatory events govern the expression of the pathway. Recently, this information has improved our ability to dissect the regulatory and signaling events that mediate the expression and operation of the pathway. Molecular analysis and sequence information have also provided new ways of assessing the evolutionary origins of CAM. Genetic and physiological analysis of transgenic plants currently under development will improve our further understanding of the molecular genetics of CAM.

The involvement of excited and highly reactive intermediates in oxygenic photosynthesis poses unique problems for algae and plants in terms of potential oxidative damage to the photosynthetic apparatus. Photoprotective processes prevent or minimize generation of oxidizing molecules, scavenge reactive oxygen species efficiently, and repair damage that inevitably occurs. This review summarizes several photoprotective mechanisms operating within chloroplasts of plants and green algae. The recent use of genetic and molecular biological approaches is providing new insights into photoprotection, especially with respect to thermal dissipation of excess absorbed light energy, alternative electron transport pathways, chloroplast antioxidant systems, and repair of photosystem II.

Arbuscular mycorrhizae are symbiotic associations formed between a wide range of plant species including angiosperms, gymnosperms, pteridophytes, and some bryophytes, and a limited range of fungi belonging to a single order, the Glomales. The symbiosis develops in the plant roots where the fungus colonizes the apoplast and cells of the cortex to access carbon supplied by the plant. The fungal contribution to the symbiosis is complex, but a major aspect includes the transfer of mineral nutrients, particularly phosphate from the soil to the plant. Development of this highly compatible association requires the coordinate molecular and cellular differentiation of both symbionts to form specialized interfaces over which bi-directional nutrient transfer occurs. Recent insights into the molecular events underlying these aspects of the symbiosis are discussed.

Polysaccharides and proteins are secreted to the inner surface of the growing cell wall, where they assemble into a network that is mechanically strong, yet remains extensible until the cells cease growth. This review focuses on the agents that directly or indirectly enhance the extensibility properties of growing walls. The properties of expansins, endoglucanases, and xyloglucan transglycosylases are reviewed and their postulated roles in modulating wall extensibility are evaluated. A summary model for wall extension is presented, in which expansin is a primary agent of wall extension, whereas endoglucanases, xyloglucan endotransglycosylase, and other enzymes that alter wall structure act secondarily to modulate expansin action.

Leaves are produced in succession on the shoot apical meristem (SAM) of a plant. The three landmark stages in leaf morphogenesis include initiation, acquisition of suborgan identities, and tissue differentiation. The expression of various genes relative to these steps in leaf morphogenesis is described. KNOTTED-like homeobox (KNOX) genes, FLO/LFY, and floral homeotic genes may be involved in generation of leaf shape and complexity. The differences between compound leaves and simple leaves in gene expression characteristics and morphogenetic patterns are discussed.

This review discusses how the pressure probe has evolved from an instrument for measuring cell turgor and other water relations parameters into a device for sampling the contents of individual higher plant cells in situ in the living plant. Together with a suite of microanalytical techniques it has permitted the mapping of water and solute relations at the resolution of single cells and has the potential to link quantitatively the traditionally separate areas of water relations and metabolism. The development of the probe is outlined and its modification to measure root pressure and xylem tension described. The deployment of the pressure probe to determine and map turgor, hydraulic conductivity, reflection coefficient, cell rheological properties, solute concentrations and enzyme activities at the resolution of single cells is discussed. The controversy surrounding the interpretation of results obtained with the xylem-pressure probe is included. Possible further developments of the probe and applications of single cell sampling are suggested.

The shikimate pathway links metabolism of carbohydrates to biosynthesis of aromatic compounds. In a sequence of seven metabolic steps, phosphoenolpyruvate and erythrose 4-phosphate are converted to chorismate, the precursor of the aromatic amino acids and many aromatic secondary metabolites. All pathway intermediates can also be considered branch point compounds that may serve as substrates for other metabolic pathways. The shikimate pathway is found only in microorganisms and plants, never in animals. All enzymes of this pathway have been obtained in pure form from prokaryotic and eukaryotic sources and their respective DNAs have been characterized from several organisms. The cDNAs of higher plants encode proteins with amino terminal signal sequences for plastid import, suggesting that plastids are the exclusive locale for chorismate biosynthesis. In microorganisms, the shikimate pathway is regulated by feedback inhibition and by repression of the first enzyme. In higher plants, no physiological feedback inhibitor has been identified, suggesting that pathway regulation may occur exclusively at the genetic level. This difference between microorganisms and plants is reflected in the unusually large variation in the primary structures of the respective first enzymes. Several of the pathway enzymes occur in isoenzymic forms whose expression varies with changing environmental conditions and, within the plant, from organ to organ. The penultimate enzyme of the pathway is the sole target for the herbicide glyphosate. Glyphosate-tolerant transgenic plants are at the core of novel weed control systems for several crop plants.

Asymmetric cell divisions generate cells with different fates. In plants, where cells do not move relative to another cell, the specification and orientation of these divisions is an important mechanism to generate the overall cellular pattern during development. This review summarizes our knowledge of selected cases of asymmetric cell division in plants, in the context of recent insights into mechanisms underlying this process in bacteria, algae, yeast, and animals.

Many microorganisms possess inducible mechanisms that concentrate CO2 at the carboxylation site, compensating for the relatively low affinity of Rubisco for its substrate, and allowing acclimation to a wide range of CO2 concentrations. The organization of the carboxysomes in prokaryotes and of the pyrenoids in eukaryotes, and the presence of membrane mechanisms for inorganic carbon (Ci) transport, are central to the concentrating mechanism. The presence of multiple Ci transporting systems in cyanobacteria has been indicated. Certain genes involved in structural organization, Ci transport and the energization of the latter have been identified. Massive Ci fluxes associated with the CO2-concentrating mechanism have wide-reaching ecological and geochemical implications.

Many plants increase in freezing tolerance upon exposure to low nonfreezing temperatures, a phenomenon known as cold acclimation. In this review, recent advances in determining the nature and function of genes with roles in freezing tolerance and the mechanisms involved in low temperature gene regulation and signal transduction are described. One of the important conclusions to emerge from these studies is that cold acclimation includes the expression of certain cold-induced genes that function to stabilize membranes against freeze-induced injury. In addition, a family of Arabidopsis transcription factors, the CBF/DREB1 proteins, have been identified that control the expression of a regulon of cold-induced genes that increase plant freezing tolerance. These results along with many of the others summarized here further our understanding of the basic mechanisms that plants have evolved to survive freezing temperatures. In addition, the findings have potential practical applications as freezing temperatures are a major factor limiting the geographical locations suitable for growing crop and horticultural plants and periodically account for significant losses in plant productivity.

Photoreduction of dioxygen in photosystem I (PSI) of chloroplasts generates superoxide radicals as the primary product. In intact chloroplasts, the superoxide and the hydrogen peroxide produced via the disproportionation of superoxide are so rapidly scavenged at the site of their generation that the active oxygens do not inactivate the PSI complex, the stromal enzymes, or the scavenging system itself. The overall reaction for scavenging of active oxygens is the photoreduction of dioxygen to water via superoxide and hydrogen peroxide in PSI by the electrons derived from water in PSII, and the water-water cycle is proposed for these sequences. An overview is given of the molecular mechanism of the water-water cycle and microcompartmentalization of the enzymes participating in it. Whenever the water-water cycle operates properly for scavenging of active oxygens in chloroplasts, it also effectively dissipates excess excitation energy under environmental stress. The dual functions of the water-water cycle for protection from photoinihibition are discussed.

Silicon is present in plants in amounts equivalent to those of such macronutrient elements as calcium, magnesium, and phosphorus, and in grasses often at higher levels than any other inorganic constituent. Yet except for certain algae, including prominently the diatoms, and the Equisetaceae (horsetails or scouring rushes), it is not considered an essential element for plants. As a result it is routinely omitted from formulations of culture solutions and considered a nonentity in much of plant physiological research. But silicon-deprived plants grown in conventional nutrient solutions to which silicon has not been added are in many ways experimental artifacts. They are often structurally weaker than silicon-replete plants, abnormal in growth, development, viability, and reproduction, more susceptible to such abiotic stresses as metal toxicities, and easier prey to disease organisms and to herbivores ranging from phytophagous insects to mammals. Many of these same conditions afflict plants in silicon-poor soils—and there are such. Taken together, the evidence is overwhelming that silicon should be included among the elements having a major bearing on plant life.

Phosphorus is one of the major plant nutrients that is least available in the soil. Consequently, plants have developed numerous morphological, physiological, biochemical, and molecular adaptations to acquire phosphate (Pi). Enhanced ability to acquire Pi and altered gene expression are the hallmarks of plant adaptation to Pi deficiency. The intricate mechanisms involved in maintaining Pi homeostasis reflect the complexity of Pi acquisition and translocation in plants. Recent discoveries of multiple Pi transporters have opened up opportunities to study the molecular basis of Pi acquisition by plants. An increasing number of genes are now known to be activated under Pi starvation. Some of these genes may be involved in Pi acquisition, transfer, and signal transduction during Pi stress. This review provides an overview of plant adaptations leading to enhanced Pi acquisition, with special emphasis on recent developments in the molecular biology of Pi acquisition.

The root system of a plant is as complicated as the shoot in its diversity, in its reactions with the matrix of substances, and with the myriad organisms that surround it. Laboratory studies blind us to the complexity found by careful study of roots in soil. This complexity is illustrated in the much-studied corn root system, covering the changes along the framework roots: the surface tissues and their interactions with the soil, the water-conducting xylem, whose gradual elaboration dictates the water status of the root. A conspicuous manifestation of the changes is the rhizosheath, whose microflora differs from that on the mature bare zones. The multitude of fine roots is the most active part of the system in acquiring water and nutrients, with its own multitude of root tips, sites of intense chemical activity, that strongly modify the soil they contact, mobilize reluctant ions, immobilize toxic ions, coat the soil particles with mucilage, and select the microflora.