Annual Review of Plant Biology - Volume 53, 2002

Lysine is one of the most limiting essential amino acids in vegetative foods consumed by humans and livestock. In addition to serving as a building block of proteins, lysine is also a precursor for glutamate, an important signaling amino acid that regulates plant growth and responses to the environment. Recent genetic, molecular, and biochemical evidence suggests that lysine synthesis and catabolism are regulated by novel concerted mechanisms. These include intracellular compartmentalization of enzymes and metabolites, complex transcriptional and posttranscriptional controls of genes encoding enzymes in lysine metabolism during plant growth and development, as well as interactions between different metabolic fluxes. The recent advances in our understanding of the regulation of lysine metabolism in plants may also prove valuable for future production of high-lysine crops.

The shoot apical meristem (SAM) of higher plants functions as a site of continuous organogenesis within which a small pool of pluripotent stem cells replenishes the cells incorporated into lateral organs. This article summarizes recent results demonstrating that the fate of stem cells in Arabidopsis shoot and floral meristems is controlled by overlapping spatial and temporal signaling systems. Stem cell maintenance is an active process requiring constant communication between neighboring groups of SAM cells. Information flows via a ligand-receptor signal transduction pathway, resulting in the formation of a spatial feedback loop that stabilizes the size of the stem cell population. Termination of stem cell activity during flower development is achieved by a temporal feedback loop involving both stem cell maintenance genes and flower patterning genes. These investigations are providing exciting insights into the components and activities of the stem cell regulatory pathway and into the interaction of this pathway with molecular mechanisms that control floral patterning.

Nonselective cation channels are a diverse group of ion channels characterized by their low discrimination between many essential and toxic cations. They are ubiquitous in plant tissues and are active in the plasma membrane, tonoplast, and other endomembranes. Members of this group are likely to function in low-affinity nutrient uptake, in distribution of cations within and between cells, and as plant Ca²⁺ channels. They are gated by diverse mechanisms, which can include voltage, cyclic nucleotides, glutamate, reactive oxygen species, and stretch. These channels dominate tonoplast cation transport, and the selectivity and gating mechanisms of tonoplast nonselective cation channels are comprehensively reviewed here. This review presents the first classification of plant nonselective cation channels and the first full description of nonselective cation channel candidate sequences in the Arabidopsis genome.

Diatoms are unicellular photosynthetic eukaryotes that contribute close to one quarter of global primary productivity. In spite of their ecological success in the world's oceans, very little information is available at the molecular level about their biology. Their most well-known characteristic is the ability to generate a highly ornamented silica cell wall, which made them very popular study organisms for microscopists in the last century. Recent advances, such as the development of a range of molecular tools, are now allowing the dissection of diatom biology, e.g., for understanding the molecular and cellular basis of bioinorganic pattern formation of their cell walls and for elucidating key aspects of diatom ecophysiology. Making diatoms accessible to genomics technologies will potentiate greatly these efforts and may lead to the use of diatoms to construct submicrometer-scale silica structures for the nanotechnology industry.

Cell separation is a critical process that takes place throughout the life cycle of a plant. It enables roots to emerge from germinating seeds, cotyledons, and leaves to expand, anthers to dehisce, fruit to ripen, and organs to be shed. The focus of this review is to examine how processes such as abscission and dehiscence are regulated and the ways new research strategies are helping us to understand the mechanisms involved in bringing about a reduction in cell-to-cell adhesion. The opportunities for using this information to manipulate cell separation for the benefit of agriculture and horticulture are evaluated.

Among the heavy metal-binding ligands in plant cells the phytochelatins (PCs) and metallothioneins (MTs) are the best characterized. PCs and MTs are different classes of cysteine-rich, heavy metal-binding protein molecules. PCs are enzymatically synthesized peptides, whereas MTs are gene-encoded polypeptides. Recently, genes encoding the enzyme PC synthase have been identified in plants and other species while the completion of the Arabidopsis genome sequence has allowed the identification of the entire suite of MT genes in a higher plant. Recent advances in understanding the regulation of PC biosynthesis and MT gene expression and the possible roles of PCs and MTs in heavy metal detoxification and homeostasis are reviewed.

Vascular tissues, xylem and phloem, are differentiated from meristematic cells, procambium, and vascular cambium. Auxin and cytokinin have been considered essential for vascular tissue differentiation; this is supported by recent molecular and genetic analyses. Xylogenesis has long been used as a model for study of cell differentiation, and many genes involved in late stages of tracheary element formation have been characterized. A number of mutants affecting vascular differentiation and pattern formation have been isolated in Arabidopsis. Studies of some of these mutants have suggested that vascular tissue organization within the bundles and vascular pattern formation at the organ level are regulated by positional information.

Nitrate is the major source of nitrogen (N) for plants growing in aerobic soils. However, the NO3⁻ ion is also used by plants as a signal to reprogram plant metabolism and to trigger changes in plant architecture. A striking example is the way that a root system can react to a localized source of NO3⁻ by activating the NO3⁻ uptake system and proliferating lateral roots preferentially within the NO3⁻-rich zone. That roots are able to respond autonomously in this fashion implies the existence of local signaling pathways that are sensitive to local changes in the external NO3⁻ concentration. On the other hand, long-range signaling pathways are also needed to modulate these responses according to the plant's N status and to coordinate the allocation of resources between the root and the shoot. This review examines these signaling mechanisms and their interactions with sugar-sensing and hormonal response pathways.

Temperature stresses experienced by plants can be classified into three types: those occurring at (a) temperatures below freezing, (b) low temperatures above freezing, and (c) high temperatures. This review outlines how biological substances that are deeply related to these stresses, such as heat-shock proteins, glycinebetaine as a compatible solute, membrane lipids, etc., and also detoxifiers of active oxygen species, contribute to temperature stress tolerance in plants. Also presented here are the uses of genetic engineering techniques to improve the adaptability of plants to temperature stress by altering the levels and composition of these substances in the living organism. Finally, the future prospects for molecular breeding are discussed.

Salt and drought stress signal transduction consists of ionic and osmotic homeostasis signaling pathways, detoxification (i.e., damage control and repair) response pathways, and pathways for growth regulation. The ionic aspect of salt stress is signaled via the SOS pathway where a calcium-responsive SOS3-SOS2 protein kinase complex controls the expression and activity of ion transporters such as SOS1. Osmotic stress activates several protein kinases including mitogen-activated kinases, which may mediate osmotic homeostasis and/or detoxification responses. A number of phospholipid systems are activated by osmotic stress, generating a diverse array of messenger molecules, some of which may function upstream of the osmotic stress–activated protein kinases. Abscisic acid biosynthesis is regulated by osmotic stress at multiple steps. Both ABA-dependent and -independent osmotic stress signaling first modify constitutively expressed transcription factors, leading to the expression of early response transcriptional activators, which then activate downstream stress tolerance effector genes.

Lipid peroxidation is common to all biological systems, both appearing in developmentally and environmentally regulated processes of plants. The hydroperoxy polyunsaturated fatty acids, synthesized by the action of various highly specialized forms of lipoxygenases, are substrates of at least seven different enzyme families. Signaling compounds such as jasmonates, antimicrobial and antifungal compounds such as leaf aldehydes or divinyl ethers, and a plant-specific blend of volatiles including leaf alcohols are among the numerous products. Cloning of many lipoxygenases and other key enzymes within the lipoxygenase pathway, as well as analyses by reverse genetic and metabolic profiling, revealed new reactions and the first hints of enzyme mechanisms, multiple functions, and regulation. These aspects are reviewed with respect to activation of this pathway as an initial step in the interaction of plants with pathogens, insects, or abiotic stress and at distinct stages of development.

Plants respond to herbivore attack with a bewildering array of responses, broadly categorized as direct and indirect defenses, and tolerance. Plant-herbivore interactions are played out on spatial scales that include the cellular responses, well-studied in plant-pathogen interactions, as well as responses that function at whole-plant and community levels. The plant's wound response plays a central role but is frequently altered by insect-specific elicitors, giving plants the potential to optimize their defenses. In this review, we emphasize studies that advance the molecular understanding of elicited direct and indirect defenses and include verifications with insect bioassays. Large-scale transcriptional changes accompany insect-induced resistance, which is organized into specific temporal and spatial patterns and points to the existence of herbivore-specific trans-activating elements orchestrating the responses. Such organizational elements could help elucidate the molecular control over the diversity of responses elicited by herbivore attack.

In this review the kinetic properties of both phytochrome A and B measured by in vivo spectroscopy in Arabidopsis are described. Inactivation of phyA is mediated by destruction and that of phyB by fast dark reversion. Recent observations, describing a complex interaction network of various phytochromes and cryptochromes, are also discussed. The review describes recent analysis of light-dependent nuclear translocation of phytochromes and genetic and molecular dissection of phyA- and phyB-mediated signal transduction. After nuclear transport, both phyA- and phyB-mediated signal transduction probably include the formation of light-dependent transcriptional complexes. Although this hypothesis is quite attractive and probably true for some responses, it cannot account for the complex network of phyA-mediated signaling and the interaction with the circadian clock. In addition, the biological function of phytochromes localized in the cytosol remains to be elucidated.

Plant cells are unique in that they contain four species of α-ketoacid dehydrogenase complex: plastidial pyruvate dehydrogenase, mitochondrial pyruvate dehydrogenase, α-ketoglutarate (2-oxoglutarate) dehydrogenase, and branched-chain α-ketoacid dehydrogenase. All complexes include multiple copies of three components: an α-ketoacid dehydrogenase/decarboxylase, a dihydrolipoyl acyltransferase, and a dihydrolipoyl dehydrogenase. The mitochondrial pyruvate dehydrogenase complex additionally includes intrinsic regulatory protein-kinase and -phosphatase enzymes. The acyltransferases form the intricate geometric core structures of the complexes. Substrate channeling plus active-site coupling combine to greatly enhance the catalytic efficiency of these complexes. These α-ketoacid dehydrogenase complexes occupy key positions in intermediary metabolism, and a basic understanding of their properties is critical to genetic and metabolic engineering. The current status of knowledge of the biochemical, regulatory, structural, genomic, and evolutionary aspects of these fascinating multienzyme complexes are reviewed.

The plant hormone auxin is a simple molecule similar to tryptophan, yet it elicits a diverse array of responses and is involved in the regulation of growth and development throughout the plant life cycle. The ability of auxin to bring about such diverse responses appears to result partly from the existence of several independent mechanisms for auxin perception. Furthermore, one prominent mechanism for auxin signal transduction involves the targeted degradation of members of a large family of transcriptional regulators that appear to participate in complex and competing dimerization networks to modulate the expression of a wide range of genes. These models for auxin signaling now offer a framework in which to test how each specific response to auxin is brought about.

Rapid progress in rice genomics is making it possible to undertake detailed structural and functional comparisons of genes involved in various biological processes among rice and other plant species, such as Arabidopsis. In this review, we summarize the current status of rice genomics. We then select two important areas of research, reproductive development and defense signaling, and compare the functions of rice and orthologous genes in other species involved in these processes. The analysis revealed that apparently orthologous genes can also display divergent functions. Changes in functions and regulation of orthologous genes may represent a basis for diversity among plant species. Such comparative genomics in other plant species will provide important information for future work on the evolution of higher plants.

The ability of plant organs to use gravity as a guide for growth, named gravitropism, has been recognized for over two centuries. This growth response to the environment contributes significantly to the upward growth of shoots and the downward growth of roots commonly observed throughout the plant kingdom. Root gravitropism has received a great deal of attention because there is a physical separation between the primary site for gravity sensing, located in the root cap, and the site of differential growth response, located in the elongation zones (EZs). Hence, this system allows identification and characterization of different phases of gravitropism, including gravity perception, signal transduction, signal transmission, and curvature response. Recent studies support some aspects of an old model for gravity sensing, which postulates that root-cap columellar amyloplasts constitute the susceptors for gravity perception. Such studies have also allowed the identification of several molecules that appear to function as second messengers in gravity signal transduction and of potential signal transducers. Auxin has been implicated as a probable component of the signal that carries the gravitropic information between the gravity-sensing cap and the gravity-responding EZs. This has allowed the identification and characterization of important molecular processes underlying auxin transport and response in plants. New molecular models can be elaborated to explain how the gravity signal transduction pathway might regulate the polarity of auxin transport in roots. Further studies are required to test these models, as well as to study the molecular mechanisms underlying a poorly characterized phase of gravitropism that is independent of an auxin gradient.

Ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco) catalyzes the first step in net photosynthetic CO2 assimilation and photorespiratory carbon oxidation. The enzyme is notoriously inefficient as a catalyst for the carboxylation of RuBP and is subject to competitive inhibition by O2, inactivation by loss of carbamylation, and dead-end inhibition by RuBP. These inadequacies make Rubisco rate limiting for photosynthesis and an obvious target for increasing agricultural productivity. Resolution of X-ray crystal structures and detailed analysis of divergent, mutant, and hybrid enzymes have increased our insight into the structure/function relationships of Rubisco. The interactions and associations relatively far from the Rubisco active site, including regulatory interactions with Rubisco activase, may present new approaches and strategies for understanding and ultimately improving this complex enzyme.