Annual Review of Plant Biology - Volume 59, 2008

The author identifies three individuals who played major roles in the development of his scientific career: his chemistry professor at the University of Colorado, Reuben Gustavson; his Ph.D. supervisor at the University of Chicago, Birgit Vennesland; and his friend and departmental colleague of 55 years at the University of California, Paul Stumpf. He also mentions students, postdoctoral scholars, and professional colleagues he encountered during his career of nearly 50 years as a plant biochemist. Finally, the article describes the author's research on cyanogenic plants. These plants contain hydrogen cyanide in a bound form that is usually released when the plant tissue is macerated. Cyanogenic plants contain cyanogenic glycosides in which the hydroxyl groups of cyanohydrins (α-hydroxynitriles) of aldehydes or ketones are covalently linked to a sugar, usually D-glucose. The biosynthesis, localization, and degradation, by hydrolysis, of these compounds have been examined, especially in sorghum and flax seedlings.

A decade-long investigation of nitric oxide (NO) functions in plants has led to its characterization as a biological mediator involved in key physiological processes. Despite the wealth of information gathered from the analysis of its functions, until recently little was known about the mechanisms by which NO exerts its effects. In the past few years, part of the gap has been bridged. NO modulates the activity of proteins through nitrosylation and probably tyrosine nitration. Furthermore, NO can act as a Ca²⁺-mobilizing messenger, and researchers are beginning to unravel the mechanisms underlying the cross talk between NO and Ca²⁺. Nonetheless, progress in this area of research is hindered by our ignorance of the pathways for NO production in plants. This review summarizes the basic concepts of NO signaling in animals and discusses new insights into NO enzymatic sources and molecular signaling in plants.

Herbivorous insects use diverse feeding strategies to obtain nutrients from their host plants. Rather than acting as passive victims in these interactions, plants respond to herbivory with the production of toxins and defensive proteins that target physiological processes in the insect. Herbivore-challenged plants also emit volatiles that attract insect predators and bolster resistance to future threats. This highly dynamic form of immunity is initiated by the recognition of insect oral secretions and signals from injured plant cells. These initial cues are transmitted within the plant by signal transduction pathways that include calcium ion fluxes, phosphorylation cascades, and, in particular, the jasmonate pathway, which plays a central and conserved role in promoting resistance to a broad spectrum of insects. A detailed understanding of plant immunity to arthropod herbivores will provide new insights into basic mechanisms of chemical communication and plant-animal coevolution and may also facilitate new approaches to crop protection and improvement.

Leaves and stems are ultimately derived from the shoot apical meristem (SAM); leaves arise from the peripheral zone of the SAM and stem tissue is derived from both the peripheral and central zones of the SAM. Both the peripheral and central regions of the SAM are formed during embryogenesis when the basic body plan of the plant is established. Interplay between points of maximal concentration of auxin and specific patterns of transcription of both auxin-responsive transcription factors and other patterning genes subdivide the embryo along both the apical-basal and central-peripheral axes. Differential gene expression along these axes leads to the differentiation of tissues, lateral organs, meristems, and boundary regions, each with varying responsiveness to auxin. Subsequent shoot growth and development is a reiteration of basic patterning processes established during embryogenesis.

The use of chlorophyll fluorescence to monitor photosynthetic performance in algae and plants is now widespread. This review examines how fluorescence parameters can be used to evaluate changes in photosystem II (PSII) photochemistry, linear electron flux, and CO2 assimilation in vivo, and outlines the theoretical bases for the use of specific fluorescence parameters. Although fluorescence parameters can be measured easily, many potential problems may arise when they are applied to predict changes in photosynthetic performance. In particular, consideration is given to problems associated with accurate estimation of the PSII operating efficiency measured by fluorescence and its relationship with the rates of linear electron flux and CO2 assimilation. The roles of photochemical and nonphotochemical quenching in the determination of changes in PSII operating efficiency are examined. Finally, applications of fluorescence imaging to studies of photosynthetic heterogeneity and the rapid screening of large numbers of plants for perturbations in photosynthesis and associated metabolism are considered.

Storage oil mobilization starts with the onset of seed germination. Oil bodies packed with triacylglycerol (TAG) exist in close proximity with glyoxysomes, the single membrane–bound organelles that house most of the biochemical machinery required to convert fatty acids derived from TAG to 4-carbon compounds. The 4-carbon compounds in turn are converted to soluble sugars that are used to fuel seedling growth. Biochemical analysis over the last 50 years has identified the main pathways involved in this process, including β-oxidation, the glyoxylate cycle, and gluconeogenesis. In the last few years molecular genetic dissection of the overall process in the model oilseed species Arabidopsis has provided new insight into its complexity, particularly with respect to the specific role played by individual enzymatic steps and the subcellular compartmentalization of the glyoxylate cycle. Both abscisic acid (ABA) and sugars inhibit storage oil mobilization and a substantial degree of the control appears to operate at the transcriptional level.

Glutathione, a tripeptide with the sequence γ-Glu-Cys-Gly, exists either in a reduced form with a free thiol group or in an oxidized form with a disulfide between two identical molecules. We describe here briefly the pathways involved in the synthesis, reduction, polymerization, and degradation of glutathione, as well as its distribution throughout the plant and its redox buffering capacities. The function of glutathione in xenobiotic and heavy metal detoxification, plant development, and plant-pathogen interactions is also briefly discussed. Several lines of evidence indicate that glutathione and glutaredoxins (GRXs) are implicated in the response to oxidative stress through the regeneration of enzymes involved in peroxide and methionine sulfoxide reduction. Finally, emerging functions for plant GRXs and glutathione concern the regulation of protein activity via glutathionylation and the capacity of some GRXs to bind iron sulfur centers and for some of them to transfer FeS clusters into apoproteins.

Only five major types of sensory photoreceptors (BLUF-proteins, cryptochromes, phototropins, phytochromes, and rhodopsins) are used in nature to regulate developmental processes, photosynthesis, photoorientation, and control of the circadian clock. Sensory photoreceptors of algae and protists are exceptionally rich in structure and function; light-gated ion channels and photoactivated adenylate cyclases are unique examples. During the past ten years major progress has been made with respect to understanding the function, photochemistry, and structure of key sensory players of the algal kingdom.

Plant genomes encode hundreds of proteases, which represent dozens of unrelated families. The biological role of these proteases is mostly unknown, but mutant alleles, gene silencing, and overexpression studies have provided phenotypes for a growing number of proteases. The aim of this review is to show the diversity of the processes that are regulated by proteases, and to summarize the current knowledge of the underlying molecular mechanisms. The emerging picture is that plant proteases are key regulators of a striking variety of biological processes, including meiosis, gametophyte survival, embryogenesis, seed coat formation, cuticle deposition, epidermal cell fate, stomata development, chloroplast biogenesis, and local and systemic defense responses. The functional diversity correlates with the molecular data: Proteases are specifically expressed in time and space and accumulate in different subcellular compartments. Their substrates and activation mechanisms are elusive, however, and represent a challenging topic for further research.

Bioactive gibberellins (GAs) are diterpene plant hormones that are biosynthesized through complex pathways and control diverse aspects of growth and development. Biochemical, genetic, and genomic approaches have led to the identification of the majority of the genes that encode GA biosynthesis and deactivation enzymes. Recent studies have highlighted the occurrence of previously unrecognized deactivation mechanisms. It is now clear that both GA biosynthesis and deactivation pathways are tightly regulated by developmental, hormonal, and environmental signals, consistent with the role of GAs as key growth regulators. In some cases, the molecular mechanisms for fine-tuning the hormone levels are beginning to be uncovered. In this review, I summarize our current understanding of the GA biosynthesis and deactivation pathways in plants and fungi, and discuss how GA concentrations in plant tissues are regulated during development and in response to environmental stimuli.

Higher plants display a variety of architectures that are defined by the degree of branching, internodal elongation, and shoot determinancy. Studies on the model plants of Arabidopsis thaliana and tomato and on crop plants such as rice and maize have greatly strengthened our understanding on the molecular genetic bases of plant architecture, one of the hottest areas in plant developmental biology. The identification of mutants that are defective in plant architecture and characterization of the corresponding and related genes will eventually enable us to elucidate the molecular mechanisms underlying plant architecture. The achievements made so far in studying plant architecture have already allowed us to pave a way for optimizing the plant architecture of crops by molecular design and improving grain productivity.

Phytochromes are red/far-red light photoreceptors that convert the information contained in external light into biological signals. The decoding process starts with the perception of red light, which occurs through photoisomerization of a chromophore located within the phytochrome, leading to structural changes that include the disruption of intramolecular interactions between the N- and C-terminal domains of the phytochrome. This disruption exposes surfaces required for interactions with other proteins. In contrast, the perception of far-red light reverses the photoisomerization, restores the intramolecular interaction, and closes the interacting surfaces. Light information represented by the concentration of opened interacting surfaces is converted into biological signals through the modulating activity of interacting proteins. This review summarizes plant phytochromes, phytochrome-interacting proteins, and signal transmission from phytochromes to their interacting proteins.

Flooding is an environmental stress for many natural and man-made ecosystems worldwide. Genetic diversity in the plant response to flooding includes alterations in architecture, metabolism, and elongation growth associated with a low O2 escape strategy and an antithetical quiescence scheme that allows endurance of prolonged submergence. Flooding is frequently accompanied with a reduction of cellular O2 content that is particularly severe when photosynthesis is limited or absent. This necessitates the production of ATP and regeneration of NAD⁺ through anaerobic respiration. The examination of gene regulation and function in model systems provides insight into low-O2-sensing mechanisms and metabolic adjustments associated with controlled use of carbohydrate and ATP. At the developmental level, plants can escape the low-O2 stress caused by flooding through multifaceted alterations in cellular and organ structure that promote access to and diffusion of O2. These processes are driven by phytohormones, including ethylene, gibberellin, and abscisic acid. This exploration of natural variation in strategies that improve O2 and carbohydrate status during flooding provides valuable resources for the improvement of crop endurance of an environmental adversity that is enhanced by global warming.

This review considers some of the mechanistic processes that involve roots in the soil nitrogen (N) cycle, and their implications for the ecological functions that retain N within ecosystems: 1) root signaling pathways for N transport systems, and feedback inhibition, especially for NO3⁻ uptake; 2) dependence on the mycorrhizal and Rhizobium/legume symbioses and their tradeoffs for N acquisition; 3) soil factors that influence the supply of NH4⁺ and NO3⁻ to roots and soil microbes; and 4) rhizosphere processes that increase N cycling and retention, such as priming effects and interactions with the soil food web. By integrating information on these plant-microbe-soil N processes across scales and disciplinary boundaries, we propose ideas for better manipulating ecological functions and processes by which the environment provides for human needs, i.e., ecosystem services. Emphasis is placed on agricultural systems, effects of N deposition in natural ecosystems, and ecosystem responses to elevated CO2 concentrations. This shows the need for multiscale approaches to increase human dependence on a biologically based N supply.

Trichomes and root hairs differentiate from epidermal cells in the aerial tissues and roots, respectively. Because trichomes and root hairs are easily accessible, particularly in the model plant Arabidopsis, their development has become a well-studied model of cell differentiation and growth. Molecular genetic analyses using Arabidopsis mutants have demonstrated that the differentiation of trichomes and root hair/hairless cells is regulated by similar molecular mechanisms. Transcriptional complexes regulate differentiation into trichome cells and root hairless cells, and formation of the transcriptional complexes is inhibited in neighboring cells. Control of cell growth after fate determination has also been analyzed using Arabidopsis mutants. The progression of endoreduplication cycles, reorientation of microtubules, and organization of the actin cytoskeleton play important roles in trichome growth. Various cellular components such as ion channels, the actin cytoskeleton, microtubules and cell wall materials, and intracellular signal transduction act to establish and maintain root hair tip growth.

Seed dormancy provides a mechanism for plants to delay germination until conditions are optimal for survival of the next generation. Dormancy release is regulated by a combination of environmental and endogenous signals with both synergistic and competing effects. Molecular studies of dormancy have correlated changes in transcriptomes, proteomes, and hormone levels with dormancy states ranging from deep primary or secondary dormancy to varying degrees of release. The balance of abscisic acid (ABA):gibberellin (GA) levels and sensitivity is a major, but not the sole, regulator of dormancy status. ABA promotes dormancy induction and maintenance, whereas GA promotes progression from release through germination; environmental signals regulate this balance by modifying the expression of biosynthetic and catabolic enzymes. Mediators of environmental and hormonal response include both positive and negative regulators, many of which are feedback-regulated to enhance or attenuate the response. The net result is a slightly heterogeneous response, thereby providing more temporal options for successful germination.

Trehalose metabolism and signaling is an area of emerging significance. In less than a decade our views on the importance of trehalose metabolism and its role in plants have gone through something of a revolution. An obscure curiosity has become an indispensable regulatory system. Mutant and transgenic plants of trehalose synthesis display wide-ranging and unprecedented phenotypes for the perturbation of a metabolic pathway. Molecular physiology and genomics have provided a glimpse of trehalose biology that had not been possible with conventional techniques, largely because the products of the synthetic pathway, trehalose 6-phosphate (T6P) and trehalose, are in trace abundance and difficult to measure in most plants. A consensus is emerging that T6P plays a central role in the coordination of metabolism with development. The discovery of trehalose metabolism has been one of the most exciting developments in plant metabolism and plant science in recent years. The field is fast moving and this review highlights the most recent insights.

The phytohormone auxin is a key factor in plant growth and development. Forward and reverse genetic strategies have identified important molecular components in auxin perception, signaling, and transport. These advances resulted in the identification of some of the underlying regulatory mechanisms as well as the emergence of functional frameworks for auxin action. This review focuses on the feedback loops that form an integrative part of these regulatory mechanisms.

The ubiquitin/26S proteasome pathway largely mediates selective proteolysis in the nucleus and cytosol. This pathway catalyzes covalent attachment of ubiquitin (UBQ) to substrate proteins in an E1-E2-E3 cascade. Ubiquitin E3 ligases interact with substrates to catalyze UBQ transfer from E2 to substrate. Within the E3 ligase superfamily, cullin RING ligases (CRLs) are significant in plants because they are linked to hormonal signaling, developmental programs, and environmental responses. Thus, knowledge of CRL regulation is required for a complete understanding of these processes. A major mechanism modulating CRL activity is modification of the cullin subunit by RUB (RELATED TO UBIQUITIN), a ubiquitin-like protein, and demodification by the COP9 signalosome (CSN). CULLIN-ASSOCIATED NEDD8-DISSOCIATED 1 (CAND1) interacts with CRLs, affecting both rubylation and derubylation. Described here are the pathways, regulation, and biological function of rubylation and derubylation, as well as future directions and outstanding questions.

The ancestors of modern cyanobacteria invented O2-generating photosynthesis some 3.6 billion years ago. The conversion of water and CO2 into energy-rich sugars and O2 slowly transformed the planet, eventually creating the biosphere as we know it today. Eukaryotes didn't invent photosynthesis; they co-opted it from prokaryotes by engulfing and stably integrating a photoautotrophic prokaryote in a process known as primary endosymbiosis. After approximately a billion of years of coevolution, the eukaryotic host and its endosymbiont have achieved an extraordinary level of integration and have spawned a bewildering array of primary producers that now underpin life on land and in the water. No partnership has been more important to life on earth. Secondary endosymbioses have created additional autotrophic eukaryotic lineages that include key organisms in the marine environment. Some of these organisms have subsequently reverted to heterotrophic lifestyles, becoming significant pathogens, microscopic predators, and consumers. We review the origins, integration, and functions of the different plastid types with special emphasis on their biochemical abilities, transfer of genes to the host, and the back supply of proteins to the endosymbiont.