Annual Review of Plant Biology - Volume 60, 2009

The author describes the circumstances and opportunities that led him to higher education and to pursue a research career in plant biology. He acknowledges the important roles a few individuals played in guiding him in his career. His early work on flowering was followed by studies on the physiological roles and the metabolism of gibberellins and abscisic acid. He describes how collaborations and technical developments advanced his research from measuring hormones by bioassay to their identification and quantification by mass spectrometry and cloning of hormone biosynthetic genes

Self-incompatibility (SI) is a genetically controlled system adopted by many flowering plants to avoid inbreeding and thus to maintain species diversity. Generally, self-pollen rejection occurs through active pollen and pistil recognition and subsequent signaling responses. So far, three different molecular controls of pollen and pistil recognition have been characterized and are exemplified by three families: the Solanaceae, the Papaveraceae, and the Brassicaceae. With more components involved in these SI systems coming to light, recent studies have provided intriguing insights into the downstream reactions that follow the initial SI signal perception. The process of pollen rejection is closely associated with rapid and effective proteolytic events, including the ubiquitin-proteasome pathway and the vacuolar sorting pathway. Here, we review our current understanding of the roles of proteolysis in SI responses of flowering plants.

Transposable elements make up a substantial proportion of most plant genomes. Because they are potentially highly mutagenic, transposons are controlled by a set of mechanisms whose function is to recognize and epigenetically silence them. Under most circumstances this process is highly efficient, and the vast majority of transposons are inactive. Nevertheless, transposons are activated by a variety of conditions likely to be encountered by natural populations, and even closely related species can have dramatic differences in transposon copy number. Transposon silencing has proved to be closely related to other epigenetic phenomena, and transposons are known to contribute directly and indirectly to regulation of host genes. Together, these observations suggest that naturally occurring changes in transposon activity may have had an important impact on the causes and consequences of epigenetic silencing in plants.

Many aspects of plant growth and development require specific protein interactions to carry out biochemical and cellular functions. Several proteins mediate these interactions, two of which specifically recognize phosophoproteins: 14-3-3 proteins and proteins with FHA domains. These are the only phosphobinding domains identified in plants. Both domains are present in animals and plants, and are used by plant proteins to regulate metabolic, developmental, and signaling pathways. 14-3-3s regulate sugar metabolism, proton gradients, and control transcription factor localization. FHA domains are modular domains often found in multidomain proteins that are involved in signal transduction and plant development.

Scientific inquiries in fields ranging from ecology to plant breeding assess phenotypic variation within a plant species either to explain its presence or utilize its consequences. Frequently this natural genetic variation is studied via mapping quantitative trait loci (QTLs); however, elucidation of the underlying molecular mechanisms is a continuing bottleneck. The genomic analysis of transcripts as individual phenotypes has led to the emerging field of expression QTL analysis. This field has begun both to delve into the ecological/evolutionary significance of this transcript variation as well as to use specific eQTLs to speed up our analysis of the molecular basis of quantitative traits. This review introduces eQTL analysis and begins to illustrate how these data can be applied to multiple research fields.

In eukaryotes, DNA is exchanged between endosymbiosis-derived compartments (mitochondria and chloroplasts) and the nucleus. Organelle-to-nucleus DNA transfer involves repair of double-stranded breaks by nonhomologous end-joining, and resulted during early organelle evolution in massive relocation of organelle genes to the nucleus. A large fraction of the products of the nuclear genes so acquired are retargeted to their ancestral compartment; many others now function in new subcellular locations. Almost all present-day nuclear transfers of mitochondrial or plastid DNA give rise to noncoding sequences, dubbed nuclear mitochondrial DNAs (NUMTs) and nuclear plastid DNAs (NUPTs). Some of these sequences were recruited as exons, thus introducing new coding sequences into preexisting nuclear genes by a novel mechanism. In organisms derived from secondary or tertiary endosymbiosis, serial gene transfers involving nucleus-to-nucleus migration of DNA have also occurred. Intercompartmental DNA transfer therefore represents a significant driving force for gene and genome evolution, relocating and refashioning genes and contributing to genetic diversity.

The nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins function as immune sensors in both plants and animals. NLR proteins recognize, directly or indirectly, pathogen-derived molecules and trigger immune responses. To function as a sensor, NLR proteins must be correctly folded and maintained in a recognition-competent state in the appropriate cellular location. Upon pathogen recognition, conformational changes and/or translocation of the sensors would activate the downstream immunity signaling pathways. Misfolded or used sensors are a threat to the cell and must be immediately inactivated and discarded to avoid inappropriate activation of downstream pathways. Such maintenance of NLR-type sensors requires the SGT1-HSP90 pair, a chaperone complex that is structurally and functionally conserved in eukaryotes. Deciphering how the chaperone machinery works would facilitate an understanding of the mechanisms of pathogen recognition and signal transduction by NLR proteins in both plants and animals.

The development of sustainable, low-carbon, liquid fuels from cellulosic biomass will require advances in many areas of science and engineering. This review describes the major topics of enquiry concerning cellulosic biofuels with an emphasis on those areas of research and development that include research problems of interest to plant biologists.

The oxylipin jasmonate (JA) regulates many aspects of growth, development, and environmental responses in plants, particularly defense responses against herbivores and necrotrophic pathogens. Mutants of Arabidopsis helped researchers define the biochemical pathway for synthesis of jasmonoyl-isoleucine (JA-Ile), the active form of JA hormone, and demonstrated that JA is required for plant survival of insect and pathogen attacks and for plant fertility. Transcriptional profiling led to the discovery of the JASMONATE ZIM-DOMAIN (JAZ) proteins, which are repressors of JA signaling. JA-Ile relieves repression by promoting binding of the JAZ proteins to the F-box protein CORONATINE INSENSITIVE1 (COI1) and their subsequent degradation by the ubiquitination/26S-proteasome pathway. Although we now have a much better understanding of the molecular mechanism of JA action, many questions remain. Experimental answers to these questions will expand our knowledge of oxylipin signaling in plants and animals and will also provide new tools for efforts to improve crop protection and reproductive performance.

The phloem transports nutrients, defensive compounds, and informational signals throughout vascular plants. Sampling the complex components of mobile phloem sap is difficult because of the damage incurred when the pressurized sieve tubes are breached. In this review we discuss sampling methods, the artifacts that can be introduced by different sampling procedures, the intricate pathways by which materials enter and exit the phloem, and the major types of compounds transported. Loading and unloading patterns are largely determined by the conductivity and number of plasmodesmata and the position-dependent function of solute-specific, plasma membrane transport proteins. Recent evidence indicates that mobile proteins and RNA are part of the plant's long-distance communication signaling system. Evidence also exists for the directed transport and sorting of macromolecules as they pass through plasmodesmata. A future challenge is to dissect the molecular and cellular aspects of long-distance macromolecular trafficking in the signal transduction pathways of the whole plant.

Selaginella (spikemoss) is an enigma in the plant kingdom. Although a fascination to botanists at the turn of the twentieth century, members of this genus are unremarkable in appearance, never flower, and are of no agronomic value. However, members of this genus are relicts from ancient times, and one has to marvel at how this genus has survived virtually unchanged in appearance for hundreds of millions of years. In light of the recent completion of the Selaginella moellendorffii genome sequence, this review is intended to survey what is known about Selaginella, with a special emphasis on recent inquiries into its unique biology and importance in understanding the early evolution of vascular plants.

Plants and algae often absorb too much light—more than they can actually use in photosynthesis. To prevent photo-oxidative damage and to acclimate to changes in their environment, photosynthetic organisms have evolved direct and indirect mechanisms for sensing and responding to excess light. Photoreceptors such as phototropin, neochrome, and cryptochrome can sense excess light directly and relay signals for chloroplast movement and gene expression responses. Indirect sensing of excess light through biochemical and metabolic signals can be transduced into local responses within chloroplasts, into changes in nuclear gene expression via retrograde signaling pathways, or even into systemic responses, all of which are associated with photoacclimation.

The lower eudicot genus Aquilegia holds enormous potential for investigating aspects of development, ecology, and evolution that are otherwise unrepresented among existing model systems. Its evolutionary history is of particular interest because it represents a phylogenetic midpoint between models such as Arabidopsis and Oryza but, at the same time, has experienced a recent adaptive radiation within the genus. To take advantage of these features, a collaborative group has developed a number of genetic and genomic resources for Aquilegia that have facilitated the study of its distinct morphology. This work has demonstrated that although the petaloid sepals of Aquilegia do not depend on B-class genes for their identity, these loci do control development of the petals, stamens, and novel staminodium. Overall, Aquilegia stands as a key example of the potential utility and speed of developing new genetic model systems.

Leaves and roots live in dramatically different habitats, but are parts of the same organism. Automated image processing of time-lapse records of these organs has led to understanding of spatial and temporal patterns of growth on time scales from minutes to weeks. Growth zones in roots and leaves show distinct patterns during a diel cycle (24 h period). In dicot leaves under nonstressful conditions these patterns are characterized by endogenous rhythms, sometimes superimposed upon morphogenesis driven by environmental variation. In roots and monocot leaves the growth patterns depend more strongly on environmental fluctuations. Because the impact of spatial variations and temporal fluctuations of above- and belowground environmental parameters must be processed by the plant body as an entire system whose individual modules interact on different levels, growth reactions of individual modules are often highly nonlinear. A mechanistic understanding of plant resource use efficiency and performance in a dynamically fluctuating environment therefore requires an accurate analysis of leaf and root growth patterns in conjunction with knowledge of major intraplant communication systems and metabolic pathways.

The technological advances in DNA sequencing over the past five years have changed our approaches to gene expression analysis, fundamentally altering the basic methods used and in most cases driving a shift from hybridization-based approaches to sequencing-based approaches. Quantitative, tag-based studies of gene expression were one of the earliest applications of these next-generation technologies, but the tremendous depth of sequencing facilitates de novo transcript discovery, which replaces traditional expressed sequence tag (EST) sequencing. In addition, these technologies have created new opportunities for understanding the generation, stability, and decay of RNA and the impacts of chromatin differences on gene expression. As we review the impact of these methods on plant biology, we also mention published studies from animal systems when the methods are broadly applicable. We can anticipate that the published work over the past few years is a harbinger of much broader studies that are yet to be published and are sure to further advance our understanding of plant genomes in a field changing at a dizzying pace.

Isoprenoids are a large and highly diverse group of natural products with many functions in plant primary and secondary metabolism. Isoprenoids are synthesized from common prenyl diphosphate precursors through the action of terpene synthases and terpene-modifying enzymes such as cytochrome P450 monooxygenases. Many isoprenoids have important applications in areas such as human health and nutrition, and much effort has been directed toward their production in microbial hosts. However, many hurdles must be overcome in the elucidation and functional microbial expression of the genes responsible for biosynthesis of an isoprenoid of interest. Here, we review investigations into isoprenoid function and gene discovery in plants as well as the latest advances in isoprenoid pathway engineering in both plant and microbial hosts.

The circadian clock regulates diverse aspects of plant growth and development and promotes plant fitness. Molecular identification of clock components, primarily in Arabidopsis, has led to recent rapid progress in our understanding of the clock mechanism in higher plants. Using mathematical modeling and experimental approaches, workers in the field have developed a model of the clock that incorporates both transcriptional and posttranscriptional regulation of clock genes. This cell-autonomous clock, or oscillator, generates rhythmic outputs that can be monitored at the cellular and whole-organism level. The clock not only confers daily rhythms in growth and metabolism, but also interacts with signaling pathways involved in plant responses to the environment. Future work will lead to a better understanding of how the clock and other signaling networks are integrated to provide plants with an adaptive advantage.

Microbe-associated molecular patterns (MAMPs) are molecular signatures typical of whole classes of microbes, and their recognition plays a key role in innate immunity. Endogenous elicitors are similarly recognized as damage-associated molecular patterns (DAMPs). This review focuses on the diversity of MAMPs/DAMPs and on progress to identify the corresponding pattern recognition receptors (PRRs) in plants. The two best-characterized MAMP/PRR pairs, flagellin/FLS2 and EF-Tu/EFR, are discussed in detail and put into a phylogenetic perspective. Both FLS2 and EFR are leucine-rich repeat receptor kinases (LRR-RKs). Upon treatment with flagellin, FLS2 forms a heteromeric complex with BAK1, an LRR-RK that also acts as coreceptor for the brassinolide receptor BRI1. The importance of MAMP/PRR signaling for plant immunity is highlighted by the finding that plant pathogens use effectors to inhibit PRR complexes or downstream signaling events. Current evidence indicates that MAMPs, DAMPs, and effectors are all perceived as danger signals and induce a stereotypic defense response.