Annual Review of Plant Biology - Volume 57, 2006

MicroRNAs (miRNAs) are small, endogenous RNAs that regulate gene expression in plants and animals. In plants, these ∼21-nucleotide RNAs are processed from stem-loop regions of long primary transcripts by a Dicer-like enzyme and are loaded into silencing complexes, where they generally direct cleavage of complementary mRNAs. Although plant miRNAs have some conserved functions extending beyond development, the importance of miRNA-directed gene regulation during plant development is now particularly clear. Identified in plants less than four years ago, miRNAs are already known to play numerous crucial roles at each major stage of development—typically at the cores of gene regulatory networks, targeting genes that are themselves regulators, such as those encoding transcription factors and F-box proteins.

The catabolic pathway of chlorophyll (Chl) during senescence and fruit ripening leads to the accumulation of colorless breakdown products (NCCs). This review updates an earlier review on Chl breakdown published here in 1999 (69). It summarizes recent advances in the biochemical reactions of the pathway and describes the characterization of new NCCs and their formation inside the vacuole. Furthermore, I focus on the recent molecular identification of three chl catabolic enzymes, chlorophyllase, pheophorbide a oxygenase (PAO), and red Chl catabolite reductase (RCCR). The analysis of Chl catabolic mutants demonstrates the importance of Chl breakdown for plant development and survival. Mutants defective in PAO or RCCR develop a lesion mimic phenotype, due to the accumulation of breakdown intermediates. Thus, Chl breakdown is a prerequisite to detoxify the potentially phototoxic pigment within the vacuoles in order to permit the remobilization of nitrogen from Chl-binding proteins to proceed during senescence.

A substantial number of elegant experimental approaches have been developed to image the distribution and dynamics of DNA, mRNA, proteins, organelles, metabolites, and ions in living plant cells. Although the human brain can rapidly assimilate visual information, particularly when presented as animations and movies, it is much more challenging to condense the phenomenal amount of data present in three-, four-, or even five-dimensional images into statistically useful measurements. This review explores a range of in vivo fluorescence imaging applications in plants, with particular emphasis on where quantitative techniques are beginning to emerge.

Plant cells grow through increases in volume and cell wall surface area. The mature morphology of a plant cell is a product of the differential rates of expansion between neighboring zones of the cell wall during this process. Filamentous actin arrays are associated with plant cell growth, and the activity of actin-binding proteins is proving to be essential for proper cell morphogenesis. Actin-nucleating proteins participate in cell expansion and cell plate formation whereas the recycling of actin monomers is required to maintain actin dynamics and controlled growth. Coordination of actin-binding protein activity and other aspects of cytoskeletal behavior during cell development maintains cohesive cell expansion. Emerging plant signaling networks are proving to be powerful regulators of morphology-shaping cytoskeletal activity, and in this review we highlight current research in actin network regulation.

The acclimation of photosynthetic organisms to changes in light color is ubiquitous and may be best illustrated by the colorful process of complementary chromatic adaptation (CCA). During CCA, cyanobacterial cells change from brick red to bright blue green, depending on their light color environment. The apparent simplicity of this spectacular, photoreversible event belies the complexity of the cellular response to changes in light color. Recent results have shown that the regulation of CCA is also complex and involves at least three pathways. One is controlled by a phytochrome-class photoreceptor that is responsive to green and red light and a complex two-component signal transduction pathway, whereas another is based on sensing redox state. Studies of CCA are uncovering the strategies used by photosynthetic organisms during light acclimation and the means by which they regulate these responses.

Fluctuations in day length determine the time to flower in many plants and in potato are critical to promote differentiation of tubers. Day length is perceived in the leaves and under inductive conditions these synthesize a systemic signal that is transported to the underground stolons to induce tuber development. Flowering tobacco shoots grafted into potato stocks promote tuberization in the stocks, indicating that the floral and tuber-inducing signals might be similar. We describe recent progress in the identification of the molecular mechanisms underlying day-length recognition in potato. Evidence has been obtained for a conserved function of the potato orthologs of the CONSTANS (CO) and FLOWERING LOCUS T (FT) proteins in tuberization control under short days (SDs). These observations indicate that common regulatory pathways are involved in both flowering and tuberization photoperiodic responses in plants.

Laser microdissection (LM) utilizes a cutting or harvesting laser to isolate specific cells from histological sections; the process is guided by microscopy. This provides a means of removing selected cells from complex tissues, based only on their identification by microscopic appearance, location, or staining properties (e.g., immunohistochemistry, reporter gene expression, etc.). Cells isolated by LM can be a source of cell-specific DNA, RNA, protein or metabolites for subsequent evaluation of DNA modifications, transcript/protein/metabolite profiling, or other cell-specific properties that would be averaged with those of neighboring cell types during analysis of undissected complex tissues. Plants are particularly amenable to the application of LM; the highly regular tissue organization and stable cell walls of plants facilitate the visual identification of most cell types even in unstained tissue sections. Plant cells isolated by LM have been the starting point for a variety of genomic and metabolite studies of specific cell types.

Recent studies have revealed the operation of a long-distance communication network operating within the vascular system of higher plants. The evolutionary development of this network reflects the need to communicate environmental inputs, sensed by mature organs, to meristematic regions of the plant. One consequence of such a long-distance signaling system is that newly forming organs can develop properties optimized for the environment into which they will emerge, mature, and function. The phloem translocation stream of the angiosperms contains, in addition to photosynthate and other small molecules, a variety of macromolecules, including mRNA, small RNA, and proteins. This review highlights recent progress in the characterization of phloem-mediated transport of macromolecules as components of an integrated long-distance signaling network. Attention is focused on the role played by these proteins and RNA species in coordination of developmental programs and the plant's response to both environmental cues and pathogen challenge. Finally, the importance of developing phloem transcriptome and proteomic databases is discussed within the context of advances in plant systems biology.

The rhizosphere encompasses the millimeters of soil surrounding a plant root where complex biological and ecological processes occur. This review describes recent advances in elucidating the role of root exudates in interactions between plant roots and other plants, microbes, and nematodes present in the rhizosphere. Evidence indicating that root exudates may take part in the signaling events that initiate the execution of these interactions is also presented. Various positive and negative plant-plant and plant-microbe interactions are highlighted and described from the molecular to the ecosystem scale. Furthermore, methodologies to address these interactions under laboratory conditions are presented.

[Addendum]

During meiotic prophase I, traits are reassorted as a result of a highly organized process involving sister chromatid cohesion, homologous chromosome alignment, pairing, synapsis, and recombination. In the past two years, a number of components involved in this pathway, including Structure Maintenance of Chromosomes (SMC), MRE11, the RAD51 homologs, BRCA2, MSH4, MER3, and ZIP1, have been characterized in plants; in addition, several genes that encode components unique to plants, such as POOR HOMOLOGOUS SYNAPSIS 1 and AMEIOTIC 1, have been cloned. Based on these recent data, essentially from maize and Arabidopsis, we discuss the conserved and plant-specific aspects of meiosis commitment and meiotic prophase I features.

Glucosinolates are sulfur-rich, anionic natural products that upon hydrolysis by endogenous thioglucosidases called myrosinases produce several different products (e.g., isothiocyanates, thiocyanates, and nitriles). The hydrolysis products have many different biological activities, e.g., as defense compounds and attractants. For humans these compounds function as cancer-preventing agents, biopesticides, and flavor compounds. Since the completion of the Arabidopsis genome, glucosinolate research has made significant progress, resulting in near-complete elucidation of the core biosynthetic pathway, identification of the first regulators of the pathway, metabolic engineering of specific glucosinolate profiles to study function, as well as identification of evolutionary links to related pathways. Although much has been learned in recent years, much more awaits discovery before we fully understand how and why plants synthesize glucosinolates. This may enable us to more fully exploit the potential of these compounds in agriculture and medicine.

Bioinformatics plays an essential role in today's plant science. As the amount of data grows exponentially, there is a parallel growth in the demand for tools and methods in data management, visualization, integration, analysis, modeling, and prediction. At the same time, many researchers in biology are unfamiliar with available bioinformatics methods, tools, and databases, which could lead to missed opportunities or misinterpretation of the information. In this review, we describe some of the key concepts, methods, software packages, and databases used in bioinformatics, with an emphasis on those relevant to plant science. We also cover some fundamental issues related to biological sequence analyses, transcriptome analyses, computational proteomics, computational metabolomics, bio-ontologies, and biological databases. Finally, we explore a few emerging research topics in bioinformatics.

Leaves are extraordinarily variable in form, longevity, venation architecture, and capacity for photosynthetic gas exchange. Much of this diversity is linked with water transport capacity. The pathways through the leaf constitute a substantial (≥30%) part of the resistance to water flow through plants, and thus influence rates of transpiration and photosynthesis. Leaf hydraulic conductance (Kleaf) varies more than 65-fold across species, reflecting differences in the anatomy of the petiole and the venation architecture, as well as pathways beyond the xylem through living tissues to sites of evaporation. Kleaf is highly dynamic over a range of time scales, showing circadian and developmental trajectories, and responds rapidly, often reversibly, to changes in temperature, irradiance, and water supply. This review addresses how leaf structure and physiology influence Kleaf, and the mechanisms by which Kleaf contributes to dynamic functional responses at the level of both individual leaves and the whole plant.

Uncoupling proteins (UCPs) are membrane proteins that mediate purine nucleotide-sensitive free fatty acid-activated H⁺ flux through the inner mitochondrial membrane. After the discovery of UCP in higher plants in 1995, it was acknowledged that these proteins are widely distributed in eukaryotic organisms. The widespread presence of UCPs in eukaryotes implies that these proteins may have functions other than thermogenesis. In this review, we describe the current knowledge of plant UCPs, including their discovery, biochemical properties, distribution, gene family, gene expression profiles, regulation of gene expression, and evolutionary aspects. Expression analyses and functional studies on the plant UCPs under normal and stressful conditions suggest that UCPs regulate energy metabolism in the cellular responses to stress through regulation of the electrochemical proton potential (ΔμH+) and production of reactive oxygen species.

Flavonoids are secondary metabolites that accumulate in most plant seeds and are involved in physiological functions such as dormancy or viability. This review presents a current view of the genetic and biochemical control of flavonoid metabolism during seed development. It focuses mainly on proanthocyanidin accumulation in Arabidopsis, with comparisons to other related metabolic and regulatory pathways. These intricate networks and their fine-tuned regulation, once they are determined, should contribute to a better understanding of seed coat development and the control of PA and flavonol metabolism. In addition, flavonoids provide an interesting model to study various biological processes and metabolic and regulatory networks.

Cytokinins (CKs) play a crucial role in various phases of plant growth and development, but the basic molecular mechanisms of their biosynthesis and signal transduction only recently became clear. The progress was achieved by identifying a series of key genes encoding enzymes and proteins controlling critical steps in biosynthesis, translocation, and signaling. Basic schemes for CK homeostasis and root/shoot communication at the whole-plant level can now be devised. This review summarizes recent findings on the relationship between CK structural variation and activity, distinct features in CK biosynthesis between higher plants and Agrobacterium infected plants, CK translocation at whole-plant and cellular levels, and CKs as signaling molecules for nutrient status via root-shoot communication.

Technological advances in expression profiling and in the ability to collect minute quantities of tissues have come together to allow a growing number of global transcriptional studies at the cell level in plants. Microarray technology, with a choice of cDNA or oligo-based slides, is now well established, with commercial full-genome platforms for rice and Arabidopsis and extensive expressed sequence tag (EST)-based designs for many other species. Microdissection and cell sorting are two established methodologies that have been used in conjunction with microarrays to provide an early glimpse of the transcriptional landscape at the level of individual cell types. The results indicate that much of the transcriptome is compartmentalized. A minor but consistent percentage of transcripts appear to be unique to specific cell types. Functional analyses of cell-specific patterns of gene expression are providing important clues to cell-specific functions. The spatial dissection of the transcriptome has also yielded insights into the localized mediators of hormone inputs and promises to provide detail on cell-specific effects of microRNAs.

Biodiversity of plant shape is mainly attributable to biodiversity of leaf shape and the shape of floral organs, the modified leaves. However, the exact mechanisms of leaf-shape determination remain unclear due to the complexity of flat-structure organogenesis that includes the simultaneous cell cycling and cell enlargement in primordia. Recent studies in developmental and molecular genetics have revealed several important aspects of leaf-shape control mechanisms. For example, understanding of polar control in leaf-blade expansion has advanced greatly. A curious phenomenon called “compensated cell enlargement” found in leaf organogenesis studies should also provide interesting clues regarding the mechanisms of multicellular organ development. This paper reviews recent research findings with a focus on leaf development in Arabidopsis thaliana.

The haploid gametophyte stage of the moss life cycle is amenable to genetic and biochemical studies. Many species can be cultured on simple defined media, where growth is rapid, making them ideal material for metabolic studies. Developmental responses to hormones and to environmental inputs can be studied both at the level of individual cells and in multicellular tissues. The protonemal stage of gametophyte development comprises cell filaments that extend by the serial division of their apical cells, allowing the investigation of the generation and modification of cell polarity and the role of the cytoskeleton in these processes. Molecular techniques including gene inactivation by targeted gene replacement or by RNA interference, together with the nearly completed sequencing of the Physcomitrella patens genome, open the way for detailed study of the functions of genes involved in both development and metabolism.