Annual Review of Plant Biology - Volume 64, 2013

The existence of specialized microdomains in plasma membranes, postulated for almost 25 years, has been popularized by the concept of lipid or membrane rafts. The idea that detergent-resistant membranes are equivalent to lipid rafts, which was generally abandoned after a decade of vigorous data accumulation, contributed to intense discussions about the validity of the raft concept. The existence of membrane microdomains, meanwhile, has been verified by unequivocal independent evidence. This review summarizes the current state of research in plants and fungi with respect to common aspects of both kingdoms. In these organisms, principally immobile microdomains large enough for microscopic detection have been visualized. These microdomains are found in the context of cell-cell interactions (plant symbionts and pathogens), membrane transport, stress, and polarized growth, and the data corroborate at least three mechanisms of formation. As documented in this review, modern methods of visualization of lateral membrane compartments are also able to uncover the functional relevance of membrane microdomains.

A Casparian strip–bearing endodermis is a feature that has been invariably present in the roots of ferns and angiosperms for approximately 400 million years. As the innermost cortical layer that surrounds the central vasculature of roots, the endodermis acts as a barrier to the free diffusion of solutes from the soil into the stele. Based on an enormous body of anatomical and physiological work, the protective endodermal diffusion barrier is thought to be of major importance for many aspects of root biology, reaching from efficient water and nutrient transport to defense against soil-borne pathogens. Until recently, however, we were ignorant about the genes and mechanisms that drive the differentiation of this intricately structured barrier. Recent work in Arabidopsis has now identified the first major players in Casparian strip formation. A mechanistic understanding of endodermal differentiation will finally allow us to specifically interfere with endodermal barrier function and study the effects on plant growth and survival under various stress conditions. Here, I critically review the major findings and models related to endodermal structure and function from other plant species and assess them in light of recent molecular data from Arabidopsis, pointing out where the older, descriptive work can provide a framework and inspiration for further molecular dissection.

Intracellular signaling from plastids to the nucleus, called retrograde signaling, coordinates the expression of nuclear and plastid genes and is essential for plastid biogenesis and for maintaining plastid function at optimal levels. Recent identification of several components involved in plastid retrograde generation, transmission, and control of nuclear gene expression has provided significant insight into the regulatory network of plastid retrograde signaling. Here, we review the current knowledge of multiple plastid retrograde signaling pathways, which are derived from distinct sources, and of possible plastid signaling molecules. We describe the retrograde signaling–dependent regulation of nuclear gene expression, which involves multilayered transcriptional control, as well as the transcription factors involved. We also summarize recent advances in the identification of key components mediating signal transduction from plastids to the nucleus.

Plastids (chloroplasts) have long been recognized to have originated by endosymbiosis of a cyanobacterium, but their subsequent evolutionary history has proved complex because they have also moved between eukaryotes during additional rounds of secondary and tertiary endosymbioses. Much of this history has been revealed by genomic analyses, but some debates remain unresolved, in particular those relating to secondary red plastids of the chromalveolates, especially cryptomonads. Here, I examine several fundamental questions and assumptions about endosymbiosis and plastid evolution, including the number of endosymbiotic events needed to explain plastid diversity, whether the genetic contribution of the endosymbionts to the host genome goes far beyond plastid-targeted genes, and whether organelle origins are best viewed as a singular transition involving one symbiont or as a gradual transition involving a long line of transient food/symbionts. I also discuss a possible link between transporters and the evolution of protein targeting in organelle integration.

Photosystem II (PSII) is an integral-membrane, multisubunit complex that initiates electron flow in oxygenic photosynthesis. The biogenesis of this complex machine involves the concerted assembly of at least 20 different polypeptides as well as the incorporation of a variety of inorganic and organic cofactors. Many factors have recently been identified that constitute an integrative network mediating the stepwise assembly of PSII components. One recurring theme is the subcellular organization of the assembly process in specialized membranes that form distinct biogenesis centers. Here, we review our current knowledge of the molecular components and events involved in PSII assembly and their high degree of evolutionary conservation.

The alternative oxidase is a membrane-bound ubiquinol oxidase found in the majority of plants as well as many fungi and protists, including pathogenic organisms such as Trypanosoma brucei. It catalyzes a cyanide- and antimycin-A-resistant oxidation of ubiquinol and the reduction of oxygen to water, short-circuiting the mitochondrial electron-transport chain prior to proton translocation by complexes III and IV, thereby dramatically reducing ATP formation. In plants, it plays a key role in cellular metabolism, thermogenesis, and energy homeostasis and is generally considered to be a major stress-induced protein. We describe recent advances in our understanding of this protein's structure following the recent successful crystallization of the alternative oxidase from T. brucei. We focus on the nature of the active site and ubiquinol-binding channels and propose a mechanism for the reduction of oxygen to water based on these structural insights. We also consider the regulation of activity at the posttranslational and retrograde levels and highlight challenges for future research.

Isoprenoid biosynthesis is essential for all living organisms, and isoprenoids are also of industrial and agricultural interest. All isoprenoids are derived from prenyl diphosphate (prenyl-PP) precursors. Unlike isoprenoid biosynthesis in other living organisms, prenyl-PP, as the precursor of all isoprenoids in plants, is synthesized by two independent pathways: the mevalonate (MVA) pathway in the cytoplasm and the 2-C-methyl-d-erythritol 4-phosphate (MEP) pathway in plastids. This review focuses on progress in our understanding of how the precursors for isoprenoid biosynthesis are synthesized in the two subcellular compartments, how the underlying pathway gene networks are organized and regulated, and how network perturbations impact each pathway and plant development. Because of the wealth of data on isoprenoid biosynthesis, we emphasize research in Arabidopsis thaliana and compare the synthesis of isoprenoid precursor molecules in this model plant with their synthesis in other prokaryotic and eukaryotic organisms.

C4 photosynthesis under optimal conditions enables higher-efficiency use of light, water, and nitrogen than the C3 form used by many crops. It is associated with the most productive terrestrial plants and crops but is largely limited to the tropics and subtropics. It has been argued that the C4 photosynthetic apparatus is inherently limited to warm environments. A small group of C4 species appear to have overcome this, and in contrast to the major C4 crop, maize, these species are able to acclimate their photosynthetic apparatus to chilling conditions. This review explores the mechanisms underlying this difference as well as the potential of introducing these changes into maize and other warm-climate C4 crops.

Identifying the correct subcellular locations for all enzymes and metabolites in plant metabolic networks is a major challenge, but is critically important for the success of the new generation of large-scale metabolic models that are driving a network-level appreciation of metabolic behavior. Even though the subcellular compartmentation of many central metabolic processes is thought to be well understood, recent gene-by-gene studies have revealed several unexpected enzyme localizations. Metabolite transport between subcellular compartments is crucial because it fundamentally affects the metabolic network structure. Although new metabolite transporters are being steadily identified, modeling work suggests that we have barely scratched the surface of the catalog of intracellular metabolite transporter proteins. In addition to compartmentation among organelles, it is increasingly apparent that microcompartment formation via the interactions of enzyme groups with intracellular membranes, the cytoskeleton, or other proteins is an important regulatory mechanism. In particular, this mechanism can promote metabolite channeling within the metabolic microcompartment, which can help control reaction specificity as well as dictate flux routes through the network. This has clear relevance for both synthetic biology in general and the engineering of plant metabolic networks in particular.

Recent progress in the identification and characterization of pectin biosynthetic proteins and the discovery of pectin domain–containing proteoglycans are changing our view of how pectin, the most complex family of plant cell wall polysaccharides, is synthesized. The functional confirmation of four types of pectin biosynthetic glycosyltransferases, the identification of multiple putative pectin glycosyl- and methyltransferases, and the characteristics of the GAUT1:GAUT7 homogalacturonan biosynthetic complex with its novel mechanism for retaining catalytic subunits in the Golgi apparatus and its 12 putative interacting proteins are beginning to provide a framework for the pectin biosynthetic process. We propose two partially overlapping hypothetical and testable models for pectin synthesis: the consecutive glycosyltransferase model and the domain synthesis model.

Symbiotic nitrogen fixation by rhizobia in legume root nodules injects approximately 40 million tonnes of nitrogen into agricultural systems each year. In exchange for reduced nitrogen from the bacteria, the plant provides rhizobia with reduced carbon and all the essential nutrients required for bacterial metabolism. Symbiotic nitrogen fixation requires exquisite integration of plant and bacterial metabolism. Central to this integration are transporters of both the plant and the rhizobia, which transfer elements and compounds across various plant membranes and the two bacterial membranes. Here we review current knowledge of legume and rhizobial transport and metabolism as they relate to symbiotic nitrogen fixation. Although all legume-rhizobia symbioses have many metabolic features in common, there are also interesting differences between them, which show that evolution has solved metabolic problems in different ways to achieve effective symbiosis in different systems.

Plants host distinct bacterial communities on and inside various plant organs, of which those associated with roots and the leaf surface are best characterized. The phylogenetic composition of these communities is defined by relatively few bacterial phyla, including Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria. A synthesis of available data suggests a two-step selection process by which the bacterial microbiota of roots is differentiated from the surrounding soil biome. Rhizodeposition appears to fuel an initial substrate-driven community shift in the rhizosphere, which converges with host genotype–dependent fine-tuning of microbiota profiles in the selection of root endophyte assemblages. Substrate-driven selection also underlies the establishment of phyllosphere communities but takes place solely at the immediate leaf surface. Both the leaf and root microbiota contain bacteria that provide indirect pathogen protection, but root microbiota members appear to serve additional host functions through the acquisition of nutrients from soil for plant growth. Thus, the plant microbiota emerges as a fundamental trait that includes mutualism enabled through diverse biochemical mechanisms, as revealed by studies on plant growth–promoting and plant health–promoting bacteria.

Systemic acquired resistance (SAR) is an induced immune mechanism in plants. Unlike vertebrate adaptive immunity, SAR is broad spectrum, with no specificity to the initial infection. An avirulent pathogen causing local programmed cell death can induce SAR through generation of mobile signals, accumulation of the defense hormone salicylic acid, and secretion of the antimicrobial PR (pathogenesis-related) proteins. Consequently, the rest of the plant is protected from secondary infection for a period of weeks to months. SAR can even be passed on to progeny through epigenetic regulation. The Arabidopsis NPR1 (nonexpresser of PR genes 1) protein is a master regulator of SAR. Recent study has shown that salicylic acid directly binds to the NPR1 adaptor proteins NPR3 and NPR4, regulates their interactions with NPR1, and controls NPR1 protein stability. However, how NPR1 interacts with TGA transcription factors to activate defense gene expression is still not well understood. In addition, redox regulators, the mediator complex, WRKY transcription factors, endoplasmic reticulum–resident proteins, and DNA repair proteins play critical roles in SAR.