Annual Review of Plant Biology

Published by Annual Reviews
Print ISSN: 1040-2519
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Promoters that respond to otherwise inactive chemicals will enhance the tools available for analyzing gene function in vivo and for altering defined traits of plants at will. Approaches to provide such tools have yielded plant promoters that respond to compounds activating defense genes. In addition, the transfer of regulatory elements from prokaryotes, insects, and mammals has opened new avenues to construct chemically inducible promoters that respond to signals normally not recognized by plants. This review describes results and applications of these two approaches.
 
Perhaps in keeping with their enigmatic name, 14-3-3 proteins offer a seemingly bewildering array of opportunities for interaction with signal transduction pathways. In each organism there are many isoforms that can form both homo- and heterodimers, and many biochemical activities have been attributed to the 14-3-3 group. The potential for diversity-and also confusion-is high. The mammalian literature on 14-3-3 proteins provides an appropriate context to appreciate the potential roles of 14-3-3s in plant signal transduction pathways. In addition, functional and structural themes emerge when 14-3-3s are examined and compiled in ways that draw attention to their participation in protein phosphorylation and protein-protein interactions. These themes allow examination of plant 14-3-3s from two perspectives: the ways in which plant 14-3- 3s contribute to and extend ideas already described in animals, and the ways that plant 14-3-3s present unique contributions to the field. The crystal structure of an animal 14-3- 3 has been solved. When considered with the evolutionary stability of large segments of the 14-3-3 protein, the structure illuminates several aspects of 14-3-3 function. However, diversity in other regions of the 14-3-3s and their presence as multigene families offer many opportunities for cell-specific specialization of individual functions.
 
The vacuole of plant cells plays an important role in the homeostasis of the cell. It is involved in the regulation of cytoplasmic pH, sequestration of toxic ions and xenobiotics, regulation of cell turgor, storage of amino acids, sugars and CO2 in the form of malate, and possibly as a source for elevating cytoplasmic calcium. All these activities are driven by two primary active transport mechanisms present in the vacuolar membrane (tonoplast). These two mechanisms employ high-energy metabolites to pump protons into the vacuole, establishing a proton electrochemical potential that mediates the transport of a diverse range of solutes. Within the past few years, great advances at the molecular and functional levels have been made on the characterization and identification of these mechanisms. The aim of this review is to summarize these studies in the context of the physiology of the plant cell.
 
The determination of the order of genes along cereal chromosomes indicates that the cereals can be described as a single genetic system. Such a framework provides an opportunity to combine data generated from the studies on different cereals, enables chromosome evolution to be traced, and sheds light on key structures involved in cereal chromosome pairing. Centromeric and telomeric regions have been highlighted as important in these processes.
 
Functions of Ti-plasmid–encoded virulence proteins in Agrobacterium and in plants 
The phytopathogenic bacterium Agrobacterium tumefaciens genetically transforms plants by transferring a portion of the resident Ti-plasmid, the T-DNA, to the plant. Accompanying the T-DNA into the plant cell is a number of virulence (Vir) proteins. These proteins may aid in T-DNA transfer, nuclear targeting, and integration into the plant genome. Other virulence proteins on the bacterial surface form a pilus through which the T-DNA and the transferred proteins may translocate. Although the roles of these virulence proteins within the bacterium are relatively well understood, less is known about their roles in the plant cell. In addition, the role of plant-encoded proteins in the transformation process is virtually unknown. In this article, I review what is currently known about the functions of virulence and plant proteins in several aspects of the Agrobacterium transformation process.
 
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.
 
Cytochrome P450-dependent monooxygenases are a large group of heme-containing enzymes, most of which catalyze NADPH- and O2-dependent hydroxylation reactions. The cloning of plant P450s has been hampered because these membrane-localized proteins are typically present in low abundance and are often unstable to purification. Since the cloning of the first plant P450 gene in 1990, there has been an explosion in the rate at which genes encoding plant P450s have been identified. These successes have largely been the result of advances in purification techniques, as well as the application of alternative methods such as mutant- and PCR-based cloning strategies. The availability of these cloned genes has made possible the analysis of P450 gene regulation and may soon reveal aspects of the evolution of P450s in plants. This new knowledge will significantly improve our understanding of many metabolic pathways and may permit their manipulation in the near future.
 
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.
 
Jasmonate functions and responsive genes
Jasmonic acid and its derivatives can modulate aspects of fruit ripening, production of viable pollen, root growth, tendril coiling, and plant resistance to insects and pathogens. Jasmonate activates genes involved in pathogen and insect resistance, and genes encoding vegetative storage proteins, but represses genes encoding proteins involved in photosynthesis. Jasmonic acid is derived from linolenic acid, and most of the enzymes in the biosynthetic pathway have been extensively characterized. Modulation of lipoxygenase and allene oxide synthase gene expression in transgenic plants raises new questions about the compartmentation of the biosynthetic pathway and its regulation. The activation of jasmonic acid biosynthesis by cell wall elicitors, the peptide systemin, and other compounds will be related to the function of jasmonates in plants. Jasmonate modulates gene expression at the level of translation, RNA processing, and transcription. Promoter elements that mediate responses to jasmonate have been isolated. This review covers recent advances in our understanding of how jasmonate biosynthesis is regulated and relates this information to knowledge of jasmonate modulated gene expression.
 
During meiosis, homologous chromosomes are brought together to be recombined and segregated into separate haploid gametes. This requires two cell divisions, an elaborate prophase with five substages, and specialized mechanisms that regulate the association of sister chromatids. This review focuses on plant chromosomes and chromosome-associated structures, such as recombination nodules and kinetochores, that ensure accurate meiotic chromosome segregation.
 
Sucrose-phosphate synthase (SPS; E.C. 2.4.1.14) is the plant enzyme thought to play a major role in sucrose biosynthesis. In photosynthetic and nonphotosynthetic tissues, SPS is regulated by metabolites and by reversible protein phosphorylation. In leaves, phosphorylation modulates SPS activity in response to light/dark signals and end-product accumulation. SPS is phosphorylated on multiple seryl residues in vivo, and the major regulatory phosphorylation site involved is Ser158 in spinach leaves and Ser162 in maize leaves. Regulation of the enzymatic activity of SPS appears to involve calcium, metabolites, and novel "coarse" control of the protein phosphatase that activates SPS. Activation of SPS also occurs during osmotic stress of leaf tissue in darkness, which may function to facilitate sucrose formation for osmoregulation. Manipulation of SPS expression in vivo confirms the role of this enzyme in the control of sucrose biosynthesis.
 
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.
 
Changes in relative levels of cis-unsaturated molecular species of PG. (A) Transgenic tobacco plants transformed with pBI121 (control), with pSQ (cDNA for squash GPAT), and with pAR (cDNA for Arabidopsis GPAT). Values were calculated from the data in Reference 79. (B) Arabidopsis plants: wild type, a transgenic plant transformed with the plsB gene, and the fab1 mutant. Values were calculated from the data in References 155 and 156. Open areas correspond to the sum of all the cis-unsaturated molecular species, and the shaded areas correspond to the sum of the saturated and trans-monounsaturated molecular species.
Genes for acyl-lipid desaturases that have been cloned from cyanobacteria
Changes in molecular species composition after manipulation of genes for desaturases in cyanobacteria. Reproduced from Murata & Wada (83). (A) Mutation of the ∆6 and ∆12 desaturases in Synechocystis sp. PCC6803 (144). (B) Introduction of the ∆12 desaturase by transformation with the desA gene from Synechocystis sp. PCC6803 (143). T-desA, a strain transformed with the desA gene.  
Photoinhibition of photosynthesis in wild-type and Fad6/desA::Km r cells of Synechocystis sp. PCC6803 grown at 34°C. •−• , Wild type; ° − ° , Fad6/desA::Km r. Reproduced from
Photoinhibition of photosynthesis in wild-type and Fad6/desA::Km r cells of Synechocystis sp. PCC6803 grown at 34°C. @BULLET−@BULLET , Wild type; ° − ° , Fad6/desA::Km r . Reproduced from  
The contribution of membrane lipids, particularly the level of unsaturation of fatty acids, to chilling sensitivity of plants has been intensively discussed for many years. We have demonstrated that the chilling sensitivity can be manipulated by modulating levels of unsaturation of fatty acids of membrane lipids by the action of acyl-lipid desaturases and glycerol-3-phosphate acyltransferase. This review covers recent studies on genetic manipulation of these enzymes in transgenic tobacco and cyanobacteria with special emphasis on the crucial importance of the unsaturation of membrane lipids in protecting the photosynthetic machinery from photoinhibition under cold conditions. Furthermore, we review the molecular mechanism of temperature-induced desaturation of fatty acids and introduce our hypothesis that changes in the membrane fluidity is the initial event of the expression of desaturase genes.
 
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.
 
Sugars have important signaling functions throughout all stages of the plant's life cycle. This review presents our current understanding of the different mechanisms of sugar sensing and sugar-induced signal transduction, including the experimental approaches used. In plants separate sensing systems are present for hexose and sucrose. Hexokinase-dependent and -independent hexose sensing systems can further be distinguished. There has been progress in understanding the signal transduction cascade by analyzing the function of the SNF1 kinase complex and the regulatory PRL1 protein. The role of sugar signaling in seed development and in seed germination is discussed, especially with respect to the various mechanisms by which sugar signaling controls gene expression. Finally, recent literature on interacting signal transduction cascades is discussed, with particular emphasis on the ethylene and ABA signal transduction pathways.
 
The rhizosphere is the zone of soil immediately surrounding plant roots that is modified by root activity. In this critical zone, plants perceive and respond to their environment. As a consequence of normal growth and development, a large range of organic and inorganic substances are exchanged between the root and soil, which inevitably leads to changes in the biochemical and physical properties of the rhizosphere. Plants also modify their rhizosphere in response to certain environmental signals and stresses. Organic anions are commonly detected in this region, and their exudation from plant roots has now been associated with nutrient deficiencies and inorganic ion stresses. This review summarizes recent developments in the understanding of the function, mechanism, and regulation of organic anion exudation from roots. The benefits that plants derive from the presence of organic anions in the rhizosphere are described and the potential for biotechnology to increase organic anion exudation is highlighted.
 
While the concept of H+-coupling has dominated studies of energy-dependent organic solute transport in plants for over two decades, recent studies have demonstrated the existence of a group of organic solute transporters, belonging to the ATP-binding cassette (ABC) superfamily, that are directly energized by MgATP rather than by a transmembrane H+-electrochemical potential difference. Originally identified in microbial and animal cells, the ABC superfamily is one of the largest and most widespread protein families known. Competent in the transport of a broad range of substances including sugars, peptides, alkaloids, inorganic anions, and lipids, all ABC transporters are constituted of one or two copies each of an integral membrane sector and cytosolically oriented ATP-binding domain. To date, two major subclasses, the multidrug resistance-associated proteins (MRPs) and multidrug resistance proteins (MDRs) (so named because of the phenotypes conferred by their animal prototypes), have been identified molecularly in plants. However, only the MRPs have been defined functionally. This review therefore focuses on the functional capabilities, energetics, organization, and regulation of the plant MRPs. Otherwise known as GS-X pumps, or glutathione-conjugate or multispecific organic anion Mg2+-ATPases, the MRPs are considered to participate in the transport of exogenous and endogenous amphipathic anions and glutathionated compounds from the cytosol into the vacuole. Encoded by a multigene family and possessing a unique domain organization, the types of processes that likely converge and depend on plant MRPs include herbicide detoxification, cell pigmentation, the alleviation of oxidative damage, and the storage of antimicrobial compounds. Additional functional capabilities might include channel regulation or activity, and/or the transport of heavy metal chelates. The identification of the MRPs, in particular, and the demonstration of a central role for ABC transporters, in general, in plant function not only provide fresh insights into the molecular basis of energy-dependent solute transport but also offer the prospect for manipulating and investigating many fundamental processes that have hitherto evaded analysis at the transport level.
 
Schematic diagram of the architecture of the VP1/ABI3-like proteins. The maize VP1 (92), A. thaliana ABI3 (38), rice OsVP1 (47), and Phaseolus vulgaris PvALF (19) proteins display a similar and novel structural organization. They contain, in particular, four domains of high amino acid sequence identity: the A domain located in the large acidic ( − ) N-terminal region and three basic domains designated as B1, B2, and B3 in order from the N terminus. The sizes of these proteins range from 691 (VP1) to 752 (PvALF) amino acids. 
Main characteristics of the various mutations known to affect ABA sensitivity
cis-acting promoter elements involved in the activation of gene expression by ABA
The plant hormone abscisic acid (ABA) plays a major role in seed maturation and germination, as well as in adaptation to abiotic environmental stresses. ABA promotes stomatal closure by rapidly altering ion fluxes in guard cells. Other ABA actions involve modifications of gene expression, and the analysis of ABA-responsive promoters has revealed a diversity of potential cis-acting regulatory elements. The nature of the ABA receptor(s) remains unknown. In contrast, combined biophysical, genetic, and molecular approaches have led to considerable progress in the characterization of more downstream signaling elements. In particular, substantial evidence points to the importance of reversible protein phosphorylation and modifications of cytosolic calcium levels and pH as intermediates in ABA signal transduction. Exciting advances are being made in reassembling individual components into minimal ABA signaling cascades at the single-cell level.
 
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.
 
Oxygen deficiency in the rooting zone occurs with poor drainage after rain or irrigation, causing depressed growth and yield of dryland species, in contrast with native wetland vegetation that tolerates such conditions. This review examines how roots are injured by O2 deficiency and how metabolism changes during acclimation to low concentrations of O2. In the root apical meristem, cell survival is important for the future development; metabolic changes under anoxia help maintain cell survival by generating ATP anaerobically and minimizing the cytoplasmic acidosis associated with cell death. Behind the apex, where cells are fully expanded, ethylene-dependent death and lysis occurs under hypoxia to form continuous, gas-filled channels (aerenchyma) conveying O2 from the leaves. This selective sacrifice of cells may resemble programmed cell death and is distinct from cell death caused by anoxia. Evidence concerning alternative possible mechanisms of anoxia tolerance and avoidance is presented.
 
While uninucleate and unicellular, Acetabularia acetabulum establishes and maintains functionally and morphologically distinct body regions and executes phase changes like those in vascular plants. Centimeters tall at maturity, this species has allowed unusual experimental approaches. Amputations revealed fates of nucleate and enucleate portions from both wild type and mutants. Historically, graft chimeras between nucleate and enucleate portions suggested that morphological instructions were supplied by the nucleus but resided in the cytoplasm and could be expressed interspecifically. Recently, graft chimeras enabled rescue of mutants arrested in vegetative phase. Since the 1930s, when Acetabularia provided the first evidence for the existence of mRNAs, a dogma has arisen that it uses long-lived mRNAs to effect morphogenesis. While the evidence favors translational control, the postulated mRNAs have not been identified, and the mechanism of morphogenesis remains unknown. Amenable to biochemistry, physiology, and both classical and molecular genetics, Acetabularia may contribute yet new insights into plant development and morphogenesis.
 
Structure of a simple plasmodesma. See text for details. Adapted from References 11, 17, and 28.  
Summary of structural and functional characteristics of leaf plasmodesmata a
Cellular routes for local and systemic movement of plant viruses. T, trichome; E, epidermal cells; MC, mesophyll cells; BS, bundle sheath cells; PP, phloem parenchyma cells; CC, companion cells; SE, sieve elements. Arrows indicate viral movement. Viral spread between trichome, epidermis, and mesophyll cells represents local, cell-to-cell movement. Plasmodesmata between bundle sheath and phloem parenchyma cells are thought to mediate transition from local to systemic movement, which then proceeds through the sieve elements to other plant organs (25, 63).
Despite a potentially key role in cell-to-cell communication, plant intercellular connections-the plasmodesmata-have long been a biological "black box." Little is known about their protein composition, regulatory mechanisms, or transport pathways. However, recent studies have shed some light on plasmodesmal function. These connections have been shown to actively traffic proteins and protein-nucleic acid complexes between plant cells. This review describes these transport processes-specifically, cell-to-cell movement of plant viruses as well as endogenous cellular proteins-and discusses their possible mechanism(s). For comparison and to provide a broader perspective on the plasmodesmal transport process, the current model for nuclear import, the only other known example of transport of large proteins and protein-nucleic acid complexes through a membrane pore, is summarized. Finally, the function of plasmodesmata as communication boundaries within plant tissue is discussed.
 
Desaturation of a fatty acid first involves the enzymatic removal of a hydrogen from a methylene group in an acyl chain, a highly energy-demanding step that requires an activated oxygen intermediate. Two types of desaturases have been identified, one soluble and the other membrane-bound, that have different consensus motifs. Database searching for these motifs reveals that these enzymes belong to two distinct multifunctional classes, each of which includes desaturases, hydroxylases, and epoxidases that act on fatty acids or other substrates. The soluble class has a consensus motif consisting of carboxylates and histidines that coordinate an active site diiron cluster. The integral membrane class contains a different consensus motif composed of histidines. Biochemical and structural similarities between the integral membrane enzymes suggest that this class also uses a diiron cluster for catalysis. Soluble and membrane enzymes have been successfully re-engineered for substrate specificity and reaction outcome. It is anticipated that rational design of these enzymes will result in new and desired activities that may form the basis for improved oil crops.
 
Biochemical reactions and mutants of plant nitrogen assimilation enzymes 
Nitrogen assimilation is a vital process controlling plant growth and development. Inorganic nitrogen is assimilated into the amino acids glutamine, glutamate, asparagine, and aspartate, which serve as important nitrogen carriers in plants. The enzymes glutamine synthetase (GS), glutamate synthase (GOGAT), glutamate dehydrogenase (GDH), aspartate aminotransferase (AspAT), and asparagine synthetase (AS) are responsible for the biosynthesis of these nitrogen-carrying amino acids. Biochemical studies have revealed the existence of multiple isoenzymes for each of these enzymes. Recent molecular analyses demonstrate that each enzyme is encoded by a gene family wherein individual members encode distinct isoenzymes that are differentially regulated by environmental stimuli, metabolic control, developmental control, and tissue/cell-type specificity. We review the recent progress in using molecular-genetic approaches to delineate the regulatory mechanisms controlling nitrogen assimilation into amino acids and to define the physiological role of each isoenzyme involved in this metabolic pathway.
 
The physical basis and evidence in support of the cohesion-tension theory of the ascent of sap in plants are reviewed. The focus is on the recent discussion of challenges to the cohesion-tension mechanism based on measurements with the pressure probe. Limitations of pressure probes to measure tensions (negative pressures) in intact transpiring plants are critically assessed. The possible role of the cohesion-tension mechanism during the acquisition of water and solutes by plant roots is discussed.
 
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.
 
Electron micrograph showing cells in the infected zone of a soybean root nodule. The infected cells containing large numbers of symbiosomes are clearly seen on either side of an uninfected cell (uc) and an air space (as). The peribacteroid membrane of a symbiosome is indicated (arrow head) in the right-hand infected cell.
Infection of legume roots or stems with soil bacteria of the Rhizobiaceae results in the formation of nodules that become symbiotic nitrogen-fixing organs. Within the infected cells of these nodules, bacteria are enveloped in a membrane of plant origin, called the peribacteroid membrane (PBM), and divide and differentiate to form nitrogen-fixing bacteroids. The organelle-like structure comprised of PBM and bacteroids is termed the symbiosome, and is the basic nitrogen-fixing unit of the nodule. The major exchange of nutrients between the symbiotic partners is reduced carbon from the plant, to fuel nitrogenase activity in the bacteroid, and fixed nitrogen from the bacteroid, which is assimilated in the plant cytoplasm. However, many other metabolites are also exchanged. The metabolic interaction between the plant and the bacteroids is regulated by a series of transporters and channels on the PBM and the bacteroid membrane, and these form the focus of this review.
 
Plants have developed finely tuned, cellular mechanisms to respond to a variety of intrinsic and extrinsic stimuli. In several examples, these responses necessitate rearrangements of the cytoplasm that are coordinated by a network of actin microfilaments and microtubules, dynamic polymers collectively known as the cytoskeleton. This review focuses on five different cellular responses in which the actin cytoskeleton redistributes following extracellular stimulation: pollen tube tip growth and the self-incompatibility response; root hair responses to bacterial nodulation factors; light-mediated plastid positioning; nonhost resistance to fungal attack; and guard cell shape and turgor changes. For each of these systems, there is reasonable knowledge about what signals induce the plant response and the function(s) of the actin rearrangement. This review aims to build beyond a description of cytoskeletal changes and look at specific actin-binding proteins that have been implicated as effectors of each response, as sites of action for second messengers, and as fundamental coordinators of actin dynamics.
 
Cytokinins are structurally diverse and biologically versatile. The chemistry and physiology of cytokinin have been studied extensively, but the regulation of cytokinin biosynthesis, metabolism, and signal transduction is still largely undefined. Recent advances in cloning metabolic genes and identifying putative receptors portend more rapid progress based on molecular techniques. This review centers on cytokinin metabolism with connecting discussions on biosynthesis and signal transduction. Important findings are summarized with emphasis on metabolic enzymes and genes. Based on the information generated to date, implications and future research directions are presented.
 
After a long period of little change, the basic concepts of lignin biosynthesis have been challenged by new results from genetic modification of lignin content and composition. New techniques for making directed genetic changes in plants, as well as improvements in the analytical techniques used to determine lignin content and composition in plant cell walls, have been used in experimental tests of the accepted lignin biosynthetic pathway. The lignins obtained from genetically modified plants have shown unexpected properties, and these findings have extended the known range of variation in lignin content and composition. These results argue that the accepted lignin biosynthetic pathway is either incomplete or incorrect, or both; and also suggest that plants may have a high level of metabolic plasticity in the formation of lignins. If this is so, the properties of novel lignins could be of significant scientific and practical interest.
 
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.
 
When plants are exposed to light intensities in excess of those that can be utilized in photosynthetic electron transport, nonphotochemical dissipation of excitation energy is induced as a mechanism for photoprotection of photosystem II. The features of this process are reviewed, particularly with respect to the molecular mechanisms involved. It is shown how the dynamic properties of the proteins and pigments of the chlorophyll a/b light-harvesting complexes of photosystem II first enable the level of excitation energy to be sensed via the thylakoid proton gradient and subsequently allow excess energy to be dissipated as heat by formation of a nonphotochemical quencher. The nature of this quencher is discussed, together with a consideration of how the variation in capacity for energy dissipation depends on specific features of the composition of the light-harvesting system. Finally, the prospects for future progress in understanding the regulation of light harvesting are assessed.
 
The cytochromes that function in photosynthesis in cyanobacteria, algae, and higher plants have, like the other photosynthetic catalysts, been largely conserved in their structure and function during evolution. Cyanobacteria and algae contain cytochrome c6, which is not found in higher plants and which may enhance survival in their planktonic mode of life. Cyanobacteria and algae contain another cytochrome, low-potential c549, which is not found in higher plants. This cytochrome has a structural role in PSII and may contribute to anaerobic survival. There is a third unique cytochrome, cytochrome M, in the planktonic photosynthesizers, and its function is unknown. New evidence is appearing to indicate evolution of cytochrome interaction mechanisms during the evolution of photosynthesis. The ease of cytochrome gene manipulation in cyanobacteria and in Chlamydomonas reinhardtii now provides great advantages in understanding of photosynthesis. The solution of tertiary and quaternary structures of cytochromes and cytochrome complexes will provide structural and functional detail at atomic resolution.
 
Recent advances in the cell, developmental, and molecular biology of alkaloid biosynthesis have heightened our appreciation for the complexity and importance of plant secondary pathways. Several biosynthetic genes involved in the formation of tropane, benzylisoquinoline, and terpenoid indole alkaloids have now been isolated. The early events of signal perception, the pathways of signal transduction, and the function of gene promoters have been studied in relation to the regulation of alkaloid metabolism. Enzymes involved in alkaloid biosynthesis are associated with diverse subcellular compartments including the cytosol, vacuole, tonoplast membrane, endoplasmic reticulum, chloroplast stroma, thylakoid membranes, and perhaps unique "biosynthetic" or transport vesicles. Localization studies have shown that sequential alkaloid biosynthetic enzymes can also occur in distinct cell types, suggesting the intercellular transport of pathway intermediates. Isolated genes have also been used to genetically alter the accumulation of specific alkaloids and other plant secondary metabolites. Metabolic modifications include increased indole alkaloid levels, altered tropane alkaloid accumulation, elevated serotonin synthesis, reduced indole glucosinolate production, redirected shikimate metabolism, and increased cell wall-bound tyramine formation. This review discusses the biochemistry, cell biology, molecular regulation, and metabolic engineering of alkaloid biosynthesis in plants.
 
Plants, some fungi, and protists contain a cyanide-resistant, alternative mitochondrial respiratory pathway. This pathway branches at the ubiquinone pool and consists of an alternative oxidase encoded by the nuclear gene Aox1. Alternative pathway respiration is only linked to proton translocation at Complex 1 (NADH dehydrogenase). Alternative oxidase expression is influenced by stress stimuli-cold, oxidative stress, pathogen attack-and by factors constricting electron flow through the cytochrome pathway of respiration. Control is exerted at the levels of gene expression and in response to the availability of carbon and reducing potential. Posttranslational control involves reversible covalent modification of the alternative oxidase and activation by specific carbon metabolites. This dynamic system of coarse and fine control may function to balance upstream respiratory carbon metabolism and downstream electron transport when these coupled processes become imbalanced as a result of changes in the supply of, or demand for, carbon, reducing power, and ATP.
 
Recent progress has been made in the genetic dissection of angiosperm shoot apical meristem (SAM) structure and function. Genes required for proper SAM development have been identified in a variety of species through the isolation of mutants. In addition, genes with expression patterns indicating they play a role in SAM function have been identified molecularly. The processes of SAM formation, self-renewal, and pattern formation within the SAM are examined with an emphasis on the contributions of recent classical and molecular genetic experiments to our understanding of this basic problem in plant developmental biology.
 
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.
 
The structure of the familiar antioxidant L-ascorbic acid (vitamin C) was described in 1933 yet remarkably, its biosynthesis in plants remained elusive until only recently. It became clear from radioisotopic labeling studies in the 1950s that plant ascorbic acid biosynthesis does not proceed in toto via a route similar to that in mammals. The description in 1996 of an Arabidopsis thaliana mutant deficient in ascorbic acid prompted renewed research effort in this area, and subsequently in 1998 a new pathway was discovered that is backed by strong biochemical and molecular genetic evidence. This pathway proceeds through the intermediates GDP-D-mannose, L-galactose, and L-galactono-1,4-lactone. Much research has focused on the properties of the terminal enzyme responsible for conversion of the aldonolactone to ascorbate, and on related enzymes in both mammals and fungi. Two of the plant biosynthetic genes have been studied at the molecular level and additional ascorbate-deficient A. thaliana mutants may hold the key to other proteins involved in plant ascorbate metabolism. An analysis of the biosynthesis of ascorbate and its analogues in algae and fungi as well as the study of alternative proposed pathways should broaden our understanding of ascorbate metabolism in plants. With a biosynthetic pathway in hand, research on areas such as the control of ascorbate biosynthesis and the physiological roles of ascorbate should progress rapidly.
 
Homology-dependent gene silencing phenomena in plants have received considerable attention, especially when it was discovered that the presence of homologous sequences not only affected the stability of transgene expression, but that the activity of endogenous genes could be altered after insertion of homologous transgenes into the genome. Homology-mediated inactivation most likely comprises at least two different molecular mechanisms that induce gene silencing at the transcriptional or posttranscriptional level, respectively. In this review we discuss different mechanistic models for plant-specific inactivation mechanisms and their relationship with repeat-specific silencing phenomena in other species.
 
The chemical structures of the primary cell walls of the grasses and their progenitors differ from those of all other flowering plant species. They vary in the complex glycans that interlace and cross-link the cellulose microfibrils to form a strong framework, in the nature of the gel matrix surrounding this framework, and in the types of aromatic substances and structural proteins that covalently cross-link the primary and secondary walls and lock cells into shape. This review focuses on the chemistry of the unique polysaccharides, aromatic substances, and proteins of the grasses and how these structural elements are synthesized and assembled into dynamic and functional cell walls. Despite wide differences in wall composition, the developmental physiology of grasses is similar to that of all flowering plants. Grass cells respond similarly to environmental cues and growth regulators, exhibit the same alterations in physical properties of the wall to allow cell growth, and possess similar patterns of wall biogenesis during the development of specific cell and tissue types. Possible unifying mechanisms of growth are suggested to explain how grasses perform the same wall functions as other plants but with different constituents and architecture.
 
Plant responses to salinity stress are reviewed with emphasis on molecular mechanisms of signal transduction and on the physiological consequences of altered gene expression that affect biochemical reactions downstream of stress sensing. We make extensive use of comparisons with model organisms, halophytic plants, and yeast, which provide a paradigm for many responses to salinity exhibited by stress-sensitive plants. Among biochemical responses, we emphasize osmolyte biosynthesis and function, water flux control, and membrane transport of ions for maintenance and re-establishment of homeostasis. The advances in understanding the effectiveness of stress responses, and distinctions between pathology and adaptive advantage, are increasingly based on transgenic plant and mutant analyses, in particular the analysis of Arabidopsis mutants defective in elements of stress signal transduction pathways. We summarize evidence for plant stress signaling systems, some of which have components analogous to those that regulate osmotic stress responses of yeast. There is evidence also of signaling cascades that are not known to exist in the unicellular eukaryote, some that presumably function in intercellular coordination or regulation of effector genes in a cell-/tissue-specific context required for tolerance of plants. A complex set of stress-responsive transcription factors is emerging. The imminent availability of genomic DNA sequences and global and cell-specific transcript expression data, combined with determinant identification based on gain- and loss-of-function molecular genetics, will provide the infrastructure for functional physiological dissection of salt tolerance determinants in an organismal context. Furthermore, protein interaction analysis and evaluation of allelism, additivity, and epistasis allow determination of ordered relationships between stress signaling components. Finally, genetic activation and suppression screens will lead inevitably to an understanding of the interrelationships of the multiple signaling systems that control stress-adaptive responses in plants.
 
Regulation of the contents and volume of vacuoles in plant cells depends on the coordinated activities of transporters and channels located in the tonoplast (vacuolar membrane). The three major components of the tonoplast are two proton pumps, the vacuolar H+-ATPase (V-ATPase) and H+-pyrophosphatase (V-PPase), and aquaporins. The tertiary structure of the V-ATPase complex and properties of its subunits have been characterized by biochemical and genetic techniques. These studies and a comparison with the F-type ATPase have enabled estimation of the dynamics of V-ATPase activity during catalysis. V-PPase, a simple proton pump, has been identified and cloned from various plant species and other organisms, such as algae and phototrophic bacteria, and functional motifs of the enzyme have been determined. Aquaporin, serving as the water channel, is the most abundant protein in the tonoplast in most plants. A common molecular architecture of aquaporins in mammals and plants has been determined by two-dimensional crystallographic analysis. Furthermore, recent molecular biological studies have revealed several other types of tonoplast transporters, such as the Ca2+-ATPase, Ca2+/H+ antiporter and Na+/H+ antiporter. Many other transporters and channels in the tonoplast remain to be identified; their activities have already been detected. This review presents an overview of the field and discusses recent findings on the tonoplast protein components that have been identified and their physiological consequences.
 
This review summarizes current knowledge about genes whose products function in the transport of various cationic macronutrients (K, Ca) and micronutrients (Cu, Fe, Mn, and Zn) in plants. Such genes have been identified on the basis of function, via complementation of yeast mutants, or on the basis of sequence similarity, via database analysis, degenerate PCR, or low stringency hybridization. Not surprisingly, many of these genes belong to previously described transporter families, including those encoding Shaker-type K+ channels, P-type ATPases, and Nramp proteins. ZIP, a novel cation transporter family first identified in plants, also seems to be ubiquitous; members of this family are found in protozoa, yeast, nematodes, and humans. Emerging information on where in the plant each transporter functions and how each is controlled in response to nutrient availability may allow creation of food crops with enhanced mineral content as well as crops that bioaccumulate or exclude toxic metals.
 
Photosystem I is the light-driven plastocyanin-ferredoxin oxidoreductase in the thylakoid membranes of cyanobacteria and chloroplasts. In recent years, sophisticated spectroscopy, molecular genetics, and biochemistry have been used to understand the light conversion and electron transport functions of photosystem I. The light-harvesting complexes and internal antenna of photosystem I absorb photons and transfer the excitation energy to P700, the primary electron donor. The subsequent charge separation and electron transport leads to the reduction of ferredoxin. The photosystem I proteins are responsible for the precise arrangement of cofactors and determine redox properties of the electron transfer centers. With the availability of genomic information and the structure of photosystem I, one can now probe the functions of photosystem I proteins and cofactors. The strong reductant produced by photosystem I has a central role in chloroplast metabolism, and thus photosystem I has a critical role in the metabolic networks and physiological responses in plants.
 
Brassinosteroids (BRs) are growth-promoting natural products found at low levels in pollen, seeds, and young vegetative tissues throughout the plant kingdom. Detailed studies of BR biosynthesis and metabolism, coupled with the recent identification of BR-insensitive and BR-deficient mutants, has greatly expanded our view of steroids as signals controlling plant growth and development. This review examines the microchemical and molecular genetic analyses that have provided convincing evidence for an essential role of BRs in diverse developmental programs, including cell expansion, vascular differentiation, etiolation, and reproductive development. Recent advances relevant to the molecular mechanisms of BR-regulated gene expression and BR signal transduction are also discussed.
 
Phloem unloading of systemic macromolecules is restricted to major veins. (a) Control leaf of tobacco showing three distinct vein classes. (b) Systemic silencing of the nitrite reductase gene is first seen as chlorosis around the class III veinal network. (Figure courtesy of Hervé Vaucheret.). (c) Phloem unloading of GFP from class III veins in a tobacco leaf. The GFP was expressed in source leaves under the CC-specific promoter SUC2, and was subsequently translocated to, and unloaded within, the sink leaf (See Reference 62). (d) Phloem unloading of a tobacco etch virus (TEV) construct expressing GFP. Virus exit (seen as green fluorescence) is first seen from the class III veinal network. The xylem of this leaf was allowed to transpire Texas red in order to reveal the minor vein networks. Note that virus unloading does not occur from minor veins. (Figure courtesy of Sophie Haupt.)
The phloem of higher plants translocates a diverse range of macromolecules including proteins, RNAs, and pathogens. This review considers the origin and destination of such macromolecules. A survey of the literature reveals that the majority of phloem-mobile macromolecules are synthesized within companion cells and enter the sieve elements through the branched plasmodesmata that connect these cells. Examples of systemic macromolecules that originate outside the companion cell are rare and are restricted to viral and subviral pathogens and putative RNA gene-silencing signals, all of which involve a relay system in which the macromolecule is amplified in each successive cell along the pathway to companion cells. Evidence is presented that xenobiotic macromolecules may enter the sieve element by a default pathway as they do not possess the necessary signals for retention in the sieve element-companion cell complex. Several sink tissues possess plasmodesmata with a high-molecular-size exclusion limit, potentially allowing the nonspecific escape of a wide range of small (<50-kDa) macromolecules from the phloem. Larger macromolecules and systemic mRNAs appear to require facilitated transport through sink plasmodesmata. The fate of phloem-mobile macromolecules is considered in relation to current models of long-distance signaling in plants.
 
(A) The LRR structural unit. L, leucine or another aliphatic amino acid; x, any amino acid. (B) Amino acid alignment of the LRR region of the flax rust resistance proteins L6 and L11. (Identical residues are indicated by dots.) These proteins are identical in the TIR and NBS regions (residues 1-600) and differ at 33 positions in the LRR region, principally in or close to the xxLxLxx motif (overlined) of the LRR units.
In "gene-for-gene" interactions between plants and their pathogens, incompatibility (no disease) requires a dominant or semidominant resistance (R) gene in the plant, and a corresponding avirulence (Avr) gene in the pathogen. Many plant/pathogen interactions are of this type. R genes are presumed to (a) enable plants to detect Avr-gene-specified pathogen molecules, (b) initiate signal transduction to activate defenses, and (c) have the capacity to evolve new R gene specificities rapidly. Isolation of R genes has revealed four main classes of R gene sequences whose products appear to activate a similar range of defense mechanisms. Discovery of the structure of R genes and R gene loci provides insight into R gene function and evolution, and should lead to novel strategies for disease control.
 
The generation and analysis of plant chimeras and other genetic mosaics have been used to deduce patterns of cell division and cell fate during plant development and to demonstrate the existence of clonally distinct cell lineages in the shoot meristems of higher plants. Cells derived from these lineages do not have fixed developmental fates but rely on positional information to determine their patterns of division and differentiation. Chimeras with cells that differ genetically for specific developmental processes have been experimentally generated by a variety of methods. This review focuses on studies of intercellular interactions during plant development as well as of the coordination of cells during meristem function and organogenesis. Recent experiments combining mosaic analysis with molecular analysis of developmental mutants have begun to shed light on the nature of the signals involved in these processes and the mechanisms by which they are transmitted and received among cells.
 
Epigenetic silencing of transgenes and endogenous genes can occur at the transcriptional level (TGS) or at the posttranscriptional level (PTGS). Because they can be induced by transgenes and viruses, TGS and PTGS probably reflect alternative (although not exclusive) responses to two important stress factors that the plant's genome has to face: the stable integration of additional DNA into chromosomes and the extrachromosomal replication of a viral genome. TGS, which results from the impairment of transcription initiation through methylation and/or chromatin condensation, could derive from the mechanisms by which transposed copies of mobile elements and T-DNA insertions are tamed. PTGS, which results from the degradation of mRNA when aberrant sense, antisense, or double-stranded forms of RNA are produced, could derive from the process of recovery by which cells eliminate pathogens (RNA viruses) or their undesirable products (RNA encoded by DNA viruses). Mechanisms involving DNA-DNA, DNA-RNA, or RNA-RNA interactions are discussed to explain the various pathways for triggering (trans)gene silencing in plants.
 
Top-cited authors
Graham D Farquhar
  • Australian National University
Christine H Foyer
  • University of Birmingham
Graham Noctor
  • Université Paris-Sud 11
Richard Dixon
  • University of North Texas
Ray Bressan
  • Purdue University