Annual Review of Plant Biology - Volume 47, 1996

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.

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 biological impact of any DNA damaging agent is a combined function of the chemical nature of the induced lesions and the efficiency and accuracy of their repair. Although much has been learned from microbes and mammals about both the repair of DNA damage and the biological effects of the persistence of these lesions, much remains to be learned about the mechanism and tissue-specificity of repair in plants. This review focuses on recent work on the induction and repair of DNA damage in higher plants, with special emphasis on UV-induced DNA damage products.

Posttranslational modification of proteins by phosphorylation is a universal mechanism for regulating diverse biological functions. Recognition that many cellular proteins are reversibly phosphorylated in response to external stimuli or intracellular signals has generated an ongoing interest in identifying and characterizing plant protein kinases and protein phosphatases that modulate the phosphorylation status of proteins. This review discusses recent advances in our understanding of the structure, regulation, and function of plant protein phosphatases. Three major classes of enzymes have been reported in plants that are homologues of the mammalian type-1, -2A, and -2C protein serine/threonine phosphatases. Molecular genetic and biochemical studies reveal a role for some of these enzymes in signal transduction, cell cycle progression, and hormonal regulation. Studies also point to the presence of additional phosphatases in plants that are unrelated to these major classes.

Glutathione S-transferases (GSTs) play roles in both normal cellular metabolism as well as in the detoxification of a wide variety of xenobiotic compounds, and they have been intensively studied with regard to herbicide detoxification in plants. A newly discovered plant GST subclass has been implicated in numerous stress responses, including those arising from pathogen attack, oxidative stress, and heavy-metal toxicity. In addition, plant GSTs play a role in the cellular response to auxins and during the normal metabolism of plant secondary products like anthocyanins and cinnamic acid. This review presents the current knowledge about the functions of GSTs in regard to both herbicides and endogenous substrates. The catalytic mechanism of GST activity as well as the fate of glutathione S-conjugates are reviewed. Finally, a summary of what is known about the gene structure and regulation of plant GSTs is presented.

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.

This review discusses the organization and regulation of the glycolytic pathway in plants and compares and contrasts plant and nonplant glycolysis. Plant glycolysis exists both in the cytosol and plastid, and the parallel reactions are catalyzed by distinct nuclear-encoded isozymes. Cytosolic glycolysis is a complex network containing alternative enzymatic reactions. Two alternate cytosolic reactions enhance the pathway's ATP yield through the use of pyrophosphate in place of ATP. The cytosolic glycolytic network may provide an essential metabolic flexibility that facilitates plant development and acclimation to environmental stress. The regulation of plant glycolytic flux is assessed, with a focus on the fine control of enzymes involved in the metabolism of fructose-6-phosphate and phosphoenolpyruvate. Plant and nonplant glycolysis are regulated from the “bottom up” and “top down,” respectively. Research on tissue- and developmental-specific isozymes of plant glycolytic enzymes is summarized. Potential pitfalls associated with studies of glycolytic enzymes are considered. Some glycolytic enzymes may be multifunctional proteins involved in processes other than carbohydrate metabolism.

Light control of plant development is most dramatically illustrated by seedling development. Seedling development patterns under light (photomorphogenesis) are distinct from those in darkness (skotomorphogenesis or etiolation) with respect to gene expression, cellular and subcellular differentiation, and organ morphology. A complex network of molecular interactions couples the regulatory photoreceptors to developmental decisions. Rapid progress in defining the roles of individual photoreceptors and the downstream regulators mediating light control of seedling development has been achieved in recent years, predominantly because of molecular genetic studies in Arabidopsis thaliana and other species. This review summarizes those important recent advances and highlights the working models underlying the light control of cellular development. We focus mainly on seedling morphogenesis in Arabidopsis but include complementary findings from other species.

Dioxygenases are nonheme iron-containing enzymes important in the biosynthesis of plant signaling compounds such as abscisic acid, gibberellins, and ethylene and also of secondary metabolites, notably flavonoids and alkaloids. Plant dioxygenases fall into two classes: lipoxygenases and 2-oxoacid-dependent dioxygenases. The latter catalyze hydroxylation, epoxidation, and desaturation reactions; some enzymes catalyze more than one type of reaction in successive steps in a biosynthetic pathway. This review highlights recent discoveries on both enzyme groups, particularly in relation to gibberellin biosynthesis, in vivo activity of 1-aminocyclopropane-1-carboxylate oxidase, and molecular structure/function relationships. Similarities between the roles of monooxygenases and dioxygenases are also discussed.

Since plant phosphoenolpyruvate carboxylase (PEPC) was last reviewed in the Annual Review of Plant Physiology over a decade ago (O'Leary 1982), significant advances have been made in our knowledge of this oligomeric, cytosolic enzyme. This review highlights this exciting progress in plant PEPC research by focusing on the three major areas of recent investigation: the enzymology of the protein; its posttranslational regulation by reversible protein phosphorylation and opposing metabolite effectors; and the structure, expression, and molecular evolution of the nuclear PEPC genes. It is hoped that the next ten years will be equally enlightening, especially with respect to the three-dimensional structure of the plant enzyme, the molecular analysis of its highly regulated protein-Ser/Thr kinase, and the elucidation of its associated signal-transduction pathways in various plant cell types.

Xylem cells develop from procambial or cambial initials in situ, and they can also be induced from parenchyma cells by wound stress and/or a combination of phytohormones in vitro. Recent molecular and biochemical studies have identified some of the genes and proteins involved in xylem differentiation, which have led to an understanding of xylem differentiation based on comparisons of events in situ and in vitro. As a result, differentiation into tracheary elements (TEs) has been divided into two processes. The “early” process involves the origination and development of procambial initials in situ. In vitro, the early process of transdifferentiation involves the dedifferentiation of cells and subsequent differentiation of dedifferentiated cells into TE precursor cells. The “late” process, observed both in situ and in vitro, involves a variety of events specific to TE formation, most of which have been observed in association with secondary wall thickenings and programmed cell death. In this review, I summarize these events, including coordinated expression of genes that are involved in secondary wall formation.

This review focuses on four interrelated processes in the plant endomembrane system: compartmentation of proteins in subdomains of the endoplasmic reticulum, mechanisms that determine whether storage proteins are retained within the ER lumen or transported out, the origin and function of biochemically distinct vacuoles or prevacuolar organelles, and the cellular processes by which proteins are sorted to vacuolar compartments. We postulate that ER-localized protein bodies are formed by a series of orderly events of protein synthesis, protein concentration, and protein assembly in subdomains of the ER. Protein concentration, which facilitates protein-to-protein interactions and subsequent protein assembly, may be achieved by the interactions with chaperones and by the localization of storage protein mRNAs. We also describe recent developments on the coexistence of two biochemically distinguishable vacuolar compartments, the possible direct role of the ER in vacuole biogenesis, and proposed mechanisms for transport of proteins from the ER or Golgi apparatus to the vacuole.

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.

Molecular studies of drought stress in plants use a variety of strategies and include different species subjected to a wide range of water deficits. Initial research has by necessity been largely descriptive, and relevant genes have been identified either by reference to physiological evidence or by differential screening. A large number of genes with a potential role in drought tolerance have been described, and major themes in the molecular response have been established. Particular areas of importance are sugar metabolism and late-embryogenesis-abundant (LEA) proteins. Studies have begun to examine mechanisms that control the gene expression, and putative regulatory pathways have been established. Recent attempts to understand gene function have utilized transgenic plants. These efforts are of clear agronomic importance.

The aerial surfaces of plants are covered with a wax layer that is primarily a waterproof barrier but that also provides protection against environmental stresses. The ubiquitous presence of cuticular wax is testimony to its essential function. Genetic and environmental factors influence wax quantity and composition, which suggests that it is an actively regulated process. The basic biochemistry of wax production has been elucidated over the past three decades; however, we still know very little about its regulation. This review presents a discussion along with new perspectives on the regulatory aspects of wax biosynthesis. Among the topics discussed are the partitioning of fatty acid precursors into wax biosynthesis and the elongation of fatty acids with particular emphasis on the nature of the acyl primer, and the role of ATP in fatty acid elongation. The recent cloning of wax biosynthetic genes and the transport of wax to plant surfaces are also discussed.

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.

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.

The cytochrome b6f complex functions in oxygenic photosynthetic membranes as the redox link between the photosynthetic reaction center complexes II and I and also functions in proton translocation. It is an ideal integral membrane protein complex in which to study structure and function because of the existence of a large amount of primary sequence data, purified complex, the emergence of structures, and the ability of flash kinetic spectroscopy to assay function in a readily accessible ms–100 μs time domain. The redox active polypeptides are cytochromes f and b6 (organelle encoded) and the Rieske iron-sulfur protein (nuclear encoded) in a mol wt = 210,000 dimeric complex that is believed to contain 22–24 transmembrane helices. The high resolution structure of the lumen-side domain of cytochrome f shows it to be an elongate (75 Å long) mostly β-strand, two-domain protein, with the N-terminal α-amino group as orthogonal heme ligand and an internal linear 11-Å bound water chain. An unusual electron transfer event, the oxidant-induced reduction of a significant fraction of the p (lumen)-side cytochrome b heme by plastosemiquinone indicates that the electron transfer pathway in the b6f complex can be described by a version of the Q-cycle mechanism, originally proposed to describe similar processes in the mitochondrial and bacterial bc1 complexes.

Plant gene responses to changing carbohydrate status can vary markedly. Some genes are induced, some are repressed, and others are minimally affected. As in microorganisms, sugar-sensitive plant genes are part of an ancient system of cellular adjustment to critical nutrient availability. However, in multicellular plants, sugar-regulated expression also provides a mechanism for control of resource distribution among tissues and organs. Carbohydrate depletion upregulates genes for photosynthesis, remobilization, and export, while decreasing mRNAs for storage and utilization. Abundant sugar levels exert opposite effects through a combination of gene repression and induction. Long-term changes in metabolic activity, resource partitioning, and plant form result. Sensitivity of carbohydrate-responsive gene expression to environmental and developmental signals further enhances its potential to aid acclimation. The review addresses the above from molecular to whole-plant levels and considers emerging models for sensing and transducing carbohydrate signals to responsive genes.