Annual Review of Plant Biology - Volume 65, 2014

This is a tale of a career in plant physiological ecology that enjoyed the freedom to address photosynthetic physiology and biochemistry in leaves of plants from diverse environments. It was supported by block funding (now sadly a thing of the past) for research at the Australian National University, by grants during appointments in the United States and in Germany, and by Columbia University. It became a “career experiment” in which long-term, high-trust support for curiosity-driven plant biology in Australia, and at times in the United States, led to surprisingly innovative results. Although the rich diversity of short-term competitive grant opportunities in the United States sustained ongoing research, it proved difficult to mobilize support for more risky long-term projects. A decade after the closure of the Biosphere 2 Laboratory, this article highlights the achievements of colleagues in experimental climate change research from 1998 to 2003.

Sucrose metabolism plays pivotal roles in development, stress response, and yield formation, mainly by generating a range of sugars as metabolites to fuel growth and synthesize essential compounds (including protein, cellulose, and starch) and as signals to regulate expression of microRNAs, transcription factors, and other genes and for crosstalk with hormonal, oxidative, and defense signaling. This review aims to capture the most exciting developments in this area by evaluating (a) the roles of key sucrose metabolic enzymes in development, abiotic stress responses, and plant–microbe interactions; (b) the coupling between sucrose metabolism and sugar signaling from extra- to intracellular spaces; (c) the different mechanisms by which sucrose metabolic enzymes could perform their signaling roles; and (d) progress on engineering sugar metabolism and transport for high yield and disease resistance. Finally, the review outlines future directions for research on sugar metabolism and signaling to better understand and improve plant performance.

Plant stature and development are governed by cell proliferation and directed cell growth. These parameters are determined largely by cell wall characteristics. Cellulose microfibrils, composed of hydrogen-bonded β-1,4 glucans, are key components for anisotropic growth in plants. Cellulose is synthesized by plasma membrane–localized cellulose synthase complexes. In higher plants, these complexes are assembled into hexameric rosettes in intracellular compartments and secreted to the plasma membrane. Here, the complexes typically track along cortical microtubules, which may guide cellulose synthesis, until the complexes are inactivated and/or internalized. Determining the regulatory aspects that control the behavior of cellulose synthase complexes is vital to understanding directed cell and plant growth and to tailoring cell wall content for industrial products, including paper, textiles, and fuel. In this review, we summarize and discuss cellulose synthesis and regulatory aspects of the cellulose synthase complex, focusing on Arabidopsis thaliana.

Phosphorus is an essential nutrient that is required for all major developmental processes and reproduction in plants. It is also a major constituent of the fertilizers required to sustain high-yield agriculture. Levels of phosphate—the only form of phosphorus that can be assimilated by plants—are suboptimal in most natural and agricultural ecosystems, and when phosphate is applied as fertilizer in soils, it is rapidly immobilized owing to fixation and microbial activity. Thus, cultivated plants use only approximately 20–30% of the applied phosphate, and the rest is lost, eventually causing water eutrophication. Recent advances in the understanding of mechanisms by which wild and cultivated species adapt to low-phosphate stress and the implementation of alternative bacterial pathways for phosphorus metabolism have started to allow the design of more effective breeding and genetic engineering strategies to produce highly phosphate-efficient crops, optimize fertilizer use, and reach agricultural sustainability with a lower environmental cost. In this review, we outline the current advances in research on the complex network of plant responses to low-phosphorus stress and discuss some strategies used to manipulate genes involved in phosphate uptake, remobilization, and metabolism to develop low-phosphate-tolerant crops, which could help in designing more efficient crops.

Iron is an essential element for all photosynthetic organisms. The biological use of this transition metal is as an enzyme cofactor, predominantly in electron transfer and catalysis. The main forms of iron cofactor are, in order of decreasing abundance, iron-sulfur clusters, heme, and di-iron or mononuclear iron, with a wide functional range. In plants and algae, iron-sulfur cluster assembly pathways of bacterial origin are localized in the mitochondria and plastids, where there is a high demand for these cofactors. A third iron-sulfur cluster assembly pathway is present in the cytosol that depends on the mitochondria but not on plastid assembly proteins. The biosynthesis of heme takes place mainly in the plastids. The importance of iron-sulfur cofactors beyond photosynthesis and respiration has become evident with recent discoveries of novel iron-sulfur proteins involved in epigenetics and DNA metabolism. In addition, increased understanding of intracellular iron trafficking is opening up research into how iron is distributed between iron cofactor assembly pathways and how this distribution is regulated.

Cyanogenic glycosides (CNglcs) are bioactive plant products derived from amino acids. Structurally, these specialized plant compounds are characterized as α-hydroxynitriles (cyanohydrins) that are stabilized by glucosylation. In recent years, improved tools within analytical chemistry have greatly increased the number of known CNglcs by enabling the discovery of less abundant CNglcs formed by additional hydroxylation, glycosylation, and acylation reactions. Cyanogenesis—the release of toxic hydrogen cyanide from endogenous CNglcs—is an effective defense against generalist herbivores but less effective against fungal pathogens. In the course of evolution, CNglcs have acquired additional roles to improve plant plasticity, i.e., establishment, robustness, and viability in response to environmental challenges. CNglc concentration is usually higher in young plants, when nitrogen is in ready supply, or when growth is constrained by nonoptimal growth conditions. Efforts are under way to engineer CNglcs into some crops as a pest control measure, whereas in other crops efforts are directed toward their removal to improve food safety. Given that many food crops are cyanogenic, it is important to understand the molecular mechanisms regulating cyanogenesis so that the impact of future environmental challenges can be anticipated.

Metabolic engineering can be used to modulate endogenous metabolic pathways in plants or introduce new metabolic capabilities in order to increase the production of a desirable compound or reduce the accumulation of an undesirable one. In practice, there are several major challenges that need to be overcome, such as gaining enough knowledge about the endogenous pathways to understand the best intervention points, identifying and sourcing the most suitable metabolic genes, expressing those genes in such a way as to produce a functional enzyme in a heterologous background, and, finally, achieving the accumulation of target compounds without harming the host plant. This article discusses the strategies that have been developed to engineer complex metabolic pathways in plants, focusing on recent technological developments that allow the most significant bottlenecks to be overcome.

The triterpenes are one of the most numerous and diverse groups of plant natural products. They are complex molecules that are, for the most part, beyond the reach of chemical synthesis. Simple triterpenes are components of surface waxes and specialized membranes and may potentially act as signaling molecules, whereas complex glycosylated triterpenes (saponins) provide protection against pathogens and pests. Simple and conjugated triterpenes have a wide range of applications in the food, health, and industrial biotechnology sectors. Here, we review recent developments in the field of triterpene biosynthesis, give an overview of the genes and enzymes that have been identified to date, and discuss strategies for discovering new triterpene biosynthetic pathways.

The diterpenoids are classically defined by their composition—four isoprenyl units (20 carbons)—and are generally derived from [E,E,E]-geranylgeranyl diphosphate (GGPP). Such metabolism seems to be ancient and has been extensively diversified, with ∼12,000 diterpenoid natural products known. Particularly notable are the gibberellin phytohormones, whose requisite biosynthesis has provided a genetic reservoir that gave rise to not only a large superfamily of ∼7,000 diterpenoids but also, to some degree, all plant terpenoid natural products. This review focuses on the diterpenoids, particularly the defining biosynthetic characteristics of the major superfamilies defined by the cyclization and/or rearrangement of GGPP catalyzed by diterpene synthases/cyclases, although it also includes some discussion of the important subsequent elaboration in the few cases where sufficient molecular genetic information is available. It additionally addresses the array of biological activity providing the selective pressures that drive the observed gene family expansion and diversification, along with biosynthetic gene clustering.

Photosynthetic organisms are continuously subjected to changes in light quantity and quality, and must adjust their photosynthetic machinery so that it maintains optimal performance under limiting light and minimizes photodamage under excess light. To achieve this goal, these organisms use two main strategies in which light-harvesting complex II (LHCII), the light-harvesting system of photosystem II (PSII), plays a key role both for the collection of light energy and for photoprotection. The first is energy-dependent nonphotochemical quenching, whereby the high-light-induced proton gradient across the thylakoid membrane triggers a process in which excess excitation energy is harmlessly dissipated as heat. The second involves a redistribution of the mobile LHCII between the two photosystems in response to changes in the redox poise of the electron transport chain sensed through a signaling chain. These two processes strongly diminish the production of damaging reactive oxygen species, but photodamage of PSII is unavoidable, and it is repaired efficiently.

Depending on the environment a young seedling encounters, the developmental program following seed germination could be skotomorphogenesis in the dark or photomorphogenesis in the light. Light signals are interpreted by a repertoire of photoreceptors followed by sophisticated gene expression networks, eventually resulting in developmental changes. The expression and functions of photoreceptors and key signaling molecules are highly coordinated and regulated at multiple levels of the central dogma in molecular biology. Light activates gene expression through the actions of positive transcriptional regulators and the relaxation of chromatin by histone acetylation. Small regulatory RNAs help attenuate the expression of light-responsive genes. Alternative splicing, protein phosphorylation/dephosphorylation, the formation of diverse transcriptional complexes, and selective protein degradation all contribute to proteome diversity and change the functions of individual proteins.

Precise allocation of limited resources between growth and defense is critical for plant survival. In shade-intolerant species, perception of competition signals by informational photoreceptors activates shade-avoidance responses and reduces the expression of defenses against pathogens and insects. The main mechanism underlying defense suppression is the simultaneous downregulation of jasmonate and salicylic acid signaling by low ratios of red:far-red radiation. Inactivation of phytochrome B by low red:far-red ratios appears to suppress jasmonate responses by altering the balance between DELLA and JASMONATE ZIM DOMAIN (JAZ) proteins in favor of the latter. Solar UVB radiation is a positive modulator of plant defense, signaling through jasmonate-dependent and jasmonate-independent pathways. Light, perceived by phytochrome B and presumably other photoreceptors, helps plants concentrate their defensive arsenals in photosynthetically valuable leaves. The discovery of connections between photoreceptors and defense signaling is revealing novel mechanisms that control key resource allocation decisions in plant canopies.

Investigators studying G protein–coupled signaling—often called the best-understood pathway in the world owing to intense research in medical fields—have adopted plants as a new model to explore the plasticity and evolution of G signaling. Much research on plant G signaling has not disappointed. Although plant cells have most of the core elements found in animal G signaling, differences in network architecture and intrinsic properties of plant G protein elements make G signaling in plant cells distinct from the animal paradigm. In contrast to animal G proteins, plant G proteins are self-activating, and therefore regulation of G activation in plants occurs at the deactivation step. The self-activating property also means that plant G proteins do not need and therefore do not have typical animal G protein–coupled receptors. Targets of activated plant G proteins, also known as effectors, are unlike effectors in animal cells. The simpler repertoire of G signal elements in Arabidopsis makes G signaling easier to manipulate in a multicellular context.

Cell-to-cell signaling is essential for many processes in plant growth and development, including coordination of cellular responses to developmental and environmental cues. Cumulative studies have demonstrated that peptide signaling plays a greater-than-anticipated role in such intercellular communication. Some peptides act as signals during plant growth and development, whereas others are involved in defense responses or symbiosis. Peptides secreted as signals often undergo posttranslational modification and proteolytic processing to generate smaller peptides composed of approximately 10 amino acid residues. Such posttranslationally modified small-peptide signals constitute one of the largest groups of secreted peptide signals in plants. The location of the modification group incorporated into the peptides by specific modification enzymes and the peptide chain length defined by the processing enzymes are critical for biological function and receptor interaction. This review covers 20 years of research into posttranslationally modified small-peptide signals in plants.

Pentatricopeptide repeat (PPR) proteins constitute one of the largest protein families in land plants, with more than 400 members in most species. Over the past decade, much has been learned about the molecular functions of these proteins, where they act in the cell, and what physiological roles they play during plant growth and development. A typical PPR protein is targeted to mitochondria or chloroplasts, binds one or several organellar transcripts, and influences their expression by altering RNA sequence, turnover, processing, or translation. Their combined action has profound effects on organelle biogenesis and function and, consequently, on photosynthesis, respiration, plant development, and environmental responses. Recent breakthroughs in understanding how PPR proteins recognize RNA sequences through modular base-specific contacts will help match proteins to potential binding sites and provide a pathway toward designing synthetic RNA-binding proteins aimed at desired targets.

Plastid division is fundamental to the biology of plant cells. Division by binary fission entails the coordinated assembly and constriction of four concentric rings, two internal and two external to the organelle. The internal FtsZ ring and external dynamin-like ARC5/DRP5B ring are connected across the two envelopes by the membrane proteins ARC6, PARC6, PDV1, and PDV2. Assembly-stimulated GTPase activity drives constriction of the FtsZ and ARC5/DRP5B rings, which together with the plastid-dividing rings pull and squeeze the envelope membranes until the two daughter plastids are formed, with the final separation requiring additional proteins. The positioning of the division machinery is controlled by the chloroplast Min system, which confines FtsZ-ring formation to the plastid midpoint. The dynamic morphology of plastids, especially nongreen plastids, is also considered here, particularly in relation to the production of stromules and plastid-derived vesicles and their possible roles in cellular communication and plastid functionality.

In eukaryotic RNA silencing, RNase-III classes of enzymes in the Dicer family process double-stranded RNA of cellular or exogenous origin into small-RNA (sRNA) molecules. sRNAs are then loaded into effector proteins known as ARGONAUTEs (AGOs), which, as part of RNA-induced silencing complexes, target complementary RNA or DNA for silencing. Plants have evolved a large variety of pathways over the Dicer–AGO consortium, which most likely underpins part of their phenotypic plasticity. Dicer-like proteins produce all known classes of plant silencing sRNAs, which are invariably stabilized via 2′-O-methylation mediated by HUA ENHANCER 1 (HEN1), potentially amplified by the action of several RNA-dependent RNA polymerases, and function through a variety of AGO proteins. Here, we review the known characteristics and biochemical properties of the core silencing factors found in the model plant Arabidopsis thaliana. We also describe how interactions between these core factors and more specialized proteins allow the production of a plethora of silencing sRNAs involved in a large array of biological functions. We emphasize in particular the biogenesis and activities of silencing sRNAs of endogenous origin.

Transposable elements (TEs) are the key players in generating genomic novelty by a combination of the chromosome rearrangements they cause and the genes that come under their regulatory sway. Genome size, gene content, gene order, centromere function, and numerous other aspects of nuclear biology are driven by TE activity. Although the origins and attitudes of TEs have the hallmarks of selfish DNA, there are numerous cases where TE components have been co-opted by the host to create new genes or modify gene regulation. In particular, epigenetic regulation has been transformed from a process to silence invading TEs and viruses into a key strategy for regulating plant genes. Most, perhaps all, of this epigenetic regulation is derived from TE insertions near genes or TE-encoded factors that act in trans. Enormous pools of genome data and new technologies for reverse genetics will lead to a powerful new era of TE analysis in plants.

Natural variants of crops are generated from wild progenitor plants under both natural and human selection. Diverse crops that are able to adapt to various environmental conditions are valuable resources for crop improvements to meet the food demands of the increasing human population. With the completion of reference genome sequences, the advent of high-throughput sequencing technology now enables rapid and accurate resequencing of a large number of crop genomes to detect the genetic basis of phenotypic variations in crops. Comprehensive maps of genome variations facilitate genome-wide association studies of complex traits and functional investigations of evolutionary changes in crops. These advances will greatly accelerate studies on crop designs via genomics-assisted breeding. Here, we first discuss crop genome studies and describe the development of sequencing-based genotyping and genome-wide association studies in crops. We then review sequencing-based crop domestication studies and offer a perspective on genomics-driven crop designs.