Annual Review of Plant Biology - Current Issue

Plants take up metals, including essential micronutrients [iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn)] and the toxic heavy metal cadmium (Cd), from soil and accumulate these metals in their edible parts, which are direct and indirect intake sources for humans. Multiple transporters belonging to different families are required to transport a metal from the soil to different organs and tissues, but only a few of them have been fully functionally characterized. The transport systems (the transporters required for uptake, translocation, distribution, redistribution, and their regulation) differ with metals and plant species, depending on the physiological roles, requirements of each metal, and anatomies of different organs and tissues. To maintain metal homeostasis in response to spatiotemporal fluctuations of metals in soil, plants have developed sophisticated and tightly regulated mechanisms through the regulation of transporters at the transcriptional and/or posttranscriptional levels. The manipulation of some transporters has succeeded in generating crops rich in essential metals but low in Cd accumulation. A better understanding of metal transport systems will contribute to better and safer crop production.

One of life's decisive innovations was to harness the catalytic power of metals for cellular chemistry. With life's expansion, global atmospheric and biogeochemical cycles underwent dramatic changes. Although initially harmful, they permitted the evolution of multicellularity and the colonization of land. In land plants as primary producers, metal homeostasis faces heightened demands, in part because soil is a challenging environment for nutrient balancing. To avoid both nutrient metal limitation and metal toxicity, plants must maintain the homeostasis of metals within tighter limits than the homeostasis of other minerals. This review describes the present model of protein metalation and sketches its transfer from unicellular organisms to land plants as complex multicellular organisms. The inseparable connection between metal and redox homeostasis increasingly draws our attention to more general regulatory roles of metals. Mineral co-option, the use of nutrient or other metals for functions other than nutrition, is an emerging concept beyond that of nutritional immunity.

B vitamins are a source of coenzymes for a vast array of enzyme reactions, particularly those of metabolism. As metabolism is the basis of decisions that drive maintenance, growth, and development, B vitamin–derived coenzymes are key components that facilitate these processes. For over a century, we have known about these essential compounds and have elucidated their pathways of biosynthesis, repair, salvage, and degradation in numerous organisms. Only now are we beginning to understand their importance for regulatory processes, which are becoming an important topic in plants. Here, I highlight and discuss emerging evidence on how B vitamins are integrated into vital processes, from energy generation and nutrition to gene expression, and thereby contribute to the coordination of growth and developmental programs, particularly those that concern maintenance of a stable state, which is the foundational tenet of plant homeostasis.

This review focuses on the intricate relationship between plant polyamines and the genetic circuits and signaling pathways that regulate various developmental programs and the defense responses of plants when faced with biotic and abiotic aggressions. Particular emphasis is placed on genetic evidence supporting the involvement of polyamines in specific processes, such as the pivotal role of thermospermine in regulating xylem cell differentiation and the significant contribution of polyamine metabolism in enhancing plant resilience to drought. Based on the numerous studies describing effects of the manipulation of plant polyamine levels, two conceptually different mechanisms for polyamine activity are discussed: direct participation of polyamines in translational regulation and the indirect production of hydrogen peroxide as a defensive mechanism against pathogens. By describing the multifaceted functions of polyamines, this review underscores the profound significance of these compounds in enabling plants to adapt and thrive in challenging environments.

Photosynthesis has been using energy from sunlight to assimilate atmospheric CO2 for at least 3.5 billion years. Through evolution and natural selection, photosynthetic organisms have flourished in almost all aquatic and terrestrial environments. This is partly due to the diversity of light-harvesting complex (LHC) proteins, which facilitate photosystem assembly, efficient excitation energy transfer, and photoprotection. Structural advances have provided angstrom-level structures of many of these proteins and have expanded our understanding of the pigments, lipids, and residues that drive LHC function. In this review, we compare and contrast recently observed cryo-electron microscopy structures across photosynthetic eukaryotes to identify structural motifs that underlie various light-harvesting strategies. We discuss subtle monomer changes that result in macroscale reorganization of LHC oligomers. Additionally, we find recurring patterns across diverse LHCs that may serve as evolutionary stepping stones for functional diversification. Advancing our understanding of LHC protein–environment interactions will improve our capacity to engineer more productive crops.

Red and far-red light–sensing phytochromes are widespread in nature, occurring in plants, algae, fungi, and prokaryotes. Despite at least a billion years of evolution, their photosensory modules remain structurally and functionally similar. Conversely, nature has found remarkably different ways of transmitting light signals from the photosensor to diverse physiological responses. We summarize key features of phytochrome structure and function and discuss how these are correlated, from how the bilin environment affects the chromophore to how light induces cellular signals. Recent advances in the structural characterization of bacterial and plant phytochromes have resulted in paradigm changes in phytochrome research that we discuss in the context of present-day knowledge. Finally, we highlight questions that remain to be answered and suggest some of the benefits of understanding phytochrome structure and function.

Auxins, a group of central hormones in plant growth and development, are transported by a diverse range of transporters with distinct biochemical and structural properties. This review summarizes the current knowledge on all known auxin transporters with respect to their biochemical and biophysical properties and the methods used to characterize them. In particular, we focus on the recent advances that were made concerning the PIN-FORMED family of auxin exporters. Insights derived from solving their structures have improved our understanding of the auxin export process, and we discuss the current state of the art on PIN-mediated auxin transport, including the use of biophysical methods to examine their properties. Understanding the mechanisms of auxin transport is crucial for understanding plant growth and development, as well as for the development of more effective strategies for crop production and plant biotechnology.

Thirty years have passed since the discovery of the Mediator complex in yeast. We are witnessing breakthroughs and advances that have led to high-resolution structural models of yeast and mammalian Mediators in the preinitiation complex, showing how it is assembled and how it positions the RNA polymerase II and its C-terminal domain (CTD) to facilitate the CTD phosphorylation that initiates transcription. This information may be also used to guide future plant research on the mechanisms of Mediator transcriptional control. Here, we review what we know about the subunit composition and structure of plant Mediators, the roles of the individual subunits and the genetic analyses that pioneered Mediator research, and how transcription factors recruit Mediators to regulatory regions adjoining promoters. What emerges from the research is a Mediator that regulates transcription activity and recruits hormonal signaling modules and histone-modifying activities to set up an off or on transcriptional state that recruits general transcription factors for preinitiation complex assembly.

Despite lignin having long been viewed as an impediment to the processing of biomass for the production of paper, biofuels, and high-value chemicals, the valorization of lignin to fuels, chemicals, and materials is now clearly recognized as a critical element for the lignocellulosic bioeconomy. However, the intended application for lignin will likely require a preferred lignin composition and form. To that end, effective lignin valorization will require the integration of plant biology, providing optimal feedstocks, with chemical process engineering, providing efficient lignin transformations. Recent advances in our understanding of lignin biosynthesis have shown that lignin structure is extremely diverse and potentially tunable, while simultaneous developments in lignin refining have resulted in the development of several processes that are more agnostic to lignin composition. Here, we review the interface between in planta lignin design and lignin processing and discuss the advances necessary for lignin valorization to become a feature of advanced biorefining.

Understanding the mechanistic basis of epigenetic memory has proven to be a difficult task due to the underlying complexity of the systems involved in its establishment and maintenance. Here, we review the role of computational modeling in helping to unlock this complexity, allowing the dissection of intricate feedback dynamics. We focus on three forms of epigenetic memory encoded in gene regulatory networks, DNA methylation, and histone modifications and discuss the important advantages offered by plant systems in their dissection. We summarize the main modeling approaches involved and highlight the principal conceptual advances that the modeling has enabled through iterative cycles of predictive modeling and experiments. Lastly, we discuss remaining gaps in our understanding and how intertwined theory and experimental approaches might help in their resolution.

Multicellularity has emerged multiple times in evolution, enabling groups of cells to share a living space and reducing the burden of solitary tasks. While unicellular organisms exhibit individuality and independence, cooperation among cells in multicellular organisms brings specialization and flexibility. However, multicellularity also necessitates intercellular dependence and relies on intercellular communication. In plants, this communication is facilitated by plasmodesmata: intercellular bridges that allow the direct (cytoplasm-to-cytoplasm) transfer of information between cells. Plasmodesmata transport essential molecules that regulate plant growth, development, and stress responses. They are embedded in the extracellular matrix but exhibit flexibility, adapting intercellular flux to meet the plant's needs.

In this review, we delve into the formation and functionality of plasmodesmata and examine the capacity of the plant communication network to respond to developmental and environmental cues. We illustrate how environmental pressure shapes cellular interactions and aids the plant in adapting its growth.

The shoot meristem of land plants maintains the capacity for organ generation throughout its lifespan due to a group of undifferentiated stem cells. Most meristems are shaped like a dome with a precise spatial arrangement of functional domains, and, within and between these domains, cells interact through a network of interconnected signaling pathways. Intercellular communication in meristems is mediated by mobile transcription factors, small RNAs, hormones, and secreted peptides that are perceived by membrane-localized receptors. In recent years, we have gained deeper insight into the underlying molecular processes of the shoot meristem, and we discuss here how plants integrate internal and external inputs to control shoot meristem activities.

Initially identified as a key regulator of female fertility in Arabidopsis, the FERONIA (FER) receptor kinase is now recognized as crucial for almost all aspects of plant growth and survival. FER partners with a glycosylphosphatidylinositol-anchored protein of the LLG family to act as coreceptors on the cell surface. The FER-LLG coreceptor interacts with different RAPID ALKALINIZATION FACTOR (RALF) peptide ligands to function in various growth and developmental processes and to respond to challenges from the environment. The RALF-FER-LLG signaling modules interact with molecules in the cell wall, cell membrane, cytoplasm, and nucleus and mediate an interwoven signaling network. Multiple FER-LLG modules, each anchored by FER or a FER-related receptor kinase, have been studied, illustrating the functional diversity and the mechanistic complexity of the FER family signaling modules. The challenges going forward are to distill from this complexity the unifying schemes where possible and attain precision and refinement in the knowledge of critical details upon which future investigations can be built. By focusing on the extensively characterized FER, this review provides foundational information to guide the next phase of research on FER in model as well as crop species and potential applications for improving plant growth and resilience.

Leaves form veins whose patterns vary from a single vein running the length of the leaf to networks of staggering complexity where huge numbers of veins connect to other veins at both ends. For the longest time, vein formation was thought to be controlled only by the polar, cell-to-cell transport of the plant hormone auxin; recent evidence suggests that is not so. Instead, it turns out that vein patterning features are best accounted for by a combination of polar auxin transport, facilitated auxin diffusion through plasmodesma intercellular channels, and auxin signal transduction—though the latter's precise contribution remains unclear. Equally unclear remain the sites of auxin production during leaf development, on which that vein patterning mechanism ought to depend. Finally, whether that vein patterning mechanism can account for the variety of vein arrangements found in nature remains unknown. Addressing those questions will be the exciting challenge of future research.

Plant vascular tissues are crucial for the long-distance transport of water, nutrients, and a multitude of signal molecules throughout the plant body and, therefore, central to plant growth and development. The intricate development of vascular tissues is orchestrated by unique populations of dedicated stem cells integrating endogenous as well as environmental cues. This review summarizes our current understanding of vascular-related stem cell biology and of vascular tissue differentiation. We present an overview of the molecular and cellular mechanisms governing the maintenance and fate determination of vascular stem cells and highlight the interplay between intrinsic and external cues. In this context, we emphasize the role of transcription factors, hormonal signaling, and epigenetic modifications. We also discuss emerging technologies and the large repertoire of cell types associated with vascular tissues, which have the potential to provide unprecedented insights into cellular specialization and anatomical adaptations to distinct ecological niches.

Florets of cereal crops are the basic reproductive organs that produce grains for food or feed. The birth of a floret progresses through meristem initiation and floral organ identity specification and maintenance. During these processes, both endogenous and external cues can trigger a premature floral organ death, leading to reproductive failure. Recent advances in different cereal crops have identified both conserved and distinct regulators governing the birth of a floret. However, the molecular underpinnings of floral death are just beginning to be understood. In this review, we first provide a general overview of the current findings in the field of floral development in major cereals and outline different forms of floral deaths, particularly in the Triticeae crops. We then highlight the importance of vascular patterning and photosynthesis in floral development and reproductive success and argue for an expanded knowledge of floral birth–death balance in the context of agroecology.

Development is a chain reaction in which one event leads to another until the completion of a life cycle. Phase transitions are milestone events in the cycle of life. LEAFY COTYLEDON1 (LEC1), ABA INSENSITIVE3 (ABI3), FUSCA3 (FUS3), and LEC2 proteins, collectively known as LAFL, are master transcription factors (TFs) regulating seed and other developmental processes. Since the initial characterization of the LAFL genes, more than three decades of active research has generated tremendous amounts of knowledge about these TFs, whose roles in seed development and germination have been comprehensively reviewed. Recent advances in cell biology with genetic and genomic tools have allowed the characterization of the LAFL regulatory networks in previously challenging tissues at a higher throughput and resolution in reference species and crops. In this review, we provide a holistic perspective by integrating advances at the epigenetic, transcriptional, posttranscriptional, and protein levels to exemplify the spatiotemporal regulation of the LAFL networks in Arabidopsis seed development and phase transitions, and we briefly discuss the evolution of these TF networks.

The hypocotyl is the embryonic stem connecting the primary root to the cotyledons. Hypocotyl length varies tremendously depending on the conditions. This developmental plasticity and the simplicity of the organ explain its success as a model for growth regulation. Light and temperature are prominent growth-controlling cues, using shared signaling elements. Mechanisms controlling hypocotyl elongation in etiolated seedlings reaching the light differ from those in photoautotrophic seedlings. However, many common growth regulators intervene in both situations. Multiple photoreceptors including phytochromes, which also respond to temperature, control the activity of several transcription factors, thereby eliciting rapid transcriptional reprogramming. Hypocotyl growth often depends on sensing in green tissues and interorgan communication comprising auxin. Hypocotyl auxin, in conjunction with other hormones, determines epidermal cell elongation. Plants facing cues with opposite effects on growth control hypocotyl elongation through intricate mechanisms. We discuss the status of the field and end by highlighting open questions.

Endocytosis is an essential eukaryotic process that maintains the homeostasis of the plasma membrane proteome by vesicle-mediated internalization. Its predominant mode of operation utilizes the polymerization of the scaffold protein clathrin forming a coat around the vesicle; therefore, it is termed clathrin-mediated endocytosis (CME). Throughout evolution, the machinery that mediates CME is marked by losses, multiplications, and innovations. CME employs a limited number of conserved structural domains and folds, whose assembly and connections are species dependent. In plants, many of the domains are grouped into an ancient multimeric complex, the TPLATE complex, which occupies a central position as an interaction hub for the endocytic machinery. In this review, we provide an overview of the current knowledge regarding the structural aspects of plant CME, and we draw comparisons to other model systems. To do so, we have taken advantage of recent developments with respect to artificial intelligence–based protein structure prediction.

Stomata serve as the battleground between plants and plant pathogens. Plants can perceive pathogens, inducing closure of the stomatal pore, while pathogens can overcome this immune response with their phytotoxins and elicitors. In this review, we summarize new discoveries in stomata–pathogen interactions. Recent studies have shown that stomatal movement continues to occur in a close-open-close-open pattern during bacterium infection, bringing a new understanding of stomatal immunity. Furthermore, the canonical pattern-triggered immunity pathway and ion channel activities seem to be common to plant–pathogen interactions outside of the well-studied Arabidopsis–Pseudomonas pathosystem. These developments can be useful to aid in the goal of crop improvement. New technologies to study intact leaves and advances in available omics data sets provide new methods for understanding the fight at the stomatal gate. Future studies should aim to further investigate the defense–growth trade-off in relation to stomatal immunity, as little is known at this time.

Amphibious plants can grow and survive in both aquatic and terrestrial environments. This review explores the diverse adaptations that enable them to thrive in such contrasting habitats. Plants with amphibious lifestyles possess fascinating traits, and their phenotypic plasticity plays an important role in adaptations. Heterophylly, the ability to produce different leaf forms, is one such trait, with submerged leaves generally being longer, narrower, and thinner than aerial leaves. In addition to drastic changes in leaf contours, amphibious plants display significant anatomical and physiological changes, including a reduction in stomatal number and cuticle thickness and changes in photosynthesis mode. This review summarizes and compares the regulatory mechanisms and evolutionary origins of amphibious plants based on molecular biology studies actively conducted in recent years using novel model amphibious plant species. Studying amphibious plants will enhance our understanding of plant adaptations to aquatic environments.

Climate change profoundly affects the timing of seasonal activities of organisms, known as phenology. The impact of climate change is not unidirectional; it is also influenced by plant phenology as plants modify atmospheric composition and climatic processes. One important aspect of this interaction is the emission of biogenic volatile organic compounds (BVOCs), which link the Earth's surface, atmosphere, and climate. BVOC emissions exhibit significant diurnal and seasonal variations and are therefore considered essential phenological traits. To understand the dynamic equilibrium arising from the interplay between plant phenology and climate, this review presents recent advances in comprehending the molecular mechanisms underpinning plant phenology and its interaction with climate. We provide an overview of studies investigating molecular phenology, genome-wide gene expression analyses conducted in natural environments, and how these studies revolutionize the concept of phenology, shifting it from observable traits to dynamic molecular responses driven by gene–environment interactions. We explain how this knowledge can be scaled up to encompass plant populations, regions, and even the globe by establishing connections between molecular phenology, changes in plant distribution, species composition, and climate.

Plant specialized metabolites (PSMs) are variably distributed across taxa, tissues, and ecological contexts; this variability has inspired many theories about PSM function, which, to date, remain poorly tested because predictions have outpaced the available data. Advances in mass spectrometry–based metabolomics have enabled unbiased PSM profiling, and molecular biology techniques have produced PSM-free plants; the combination of these methods has accelerated our understanding of the complex ecological roles that PSMs play in plants. Synthetic biology techniques and workflows are producing high-value, structurally complex PSMs in quantities and purities sufficient for both medicinal and functional studies. These workflows enable the reengineering of PSM transport, externalization, structural diversity, and production in novel taxa, facilitating rigorous tests of long-standing theoretical predictions about why plants produce so many different PSMs in particular tissues and ecological contexts. Plants use their chemical prowess to solve ecological challenges, and synthetic biology workflows are accelerating our understanding of these evolved functions.

Viruses, causal agents of devastating diseases in plants, are obligate intracellular pathogens composed of a nucleic acid genome and a limited number of viral proteins. The diversity of plant viruses, their diminutive molecular nature, and their symplastic localization pose challenges to understanding the interplay between these pathogens and their hosts in the currently accepted framework of plant innate immunity. It is clear, nevertheless, that plants can recognize the presence of a virus and activate antiviral immune responses, although our knowledge of the breadth of invasion signals and the underpinning sensing events is far from complete. Below, I discuss some of the demonstrated or hypothesized mechanisms enabling viral recognition in plants, the step preceding the onset of antiviral immunity, as well as the strategies viruses have evolved to evade or suppress their detection.

Crops are plant species that were domesticated starting about 11,000 years ago from several centers of origin, most prominently the Fertile Crescent, East Asia, and Mesoamerica. From their domestication centers, these crops spread across the globe and had to adapt to differing environments as a result of this dispersal. We discuss broad patterns of crop spread, including the early diffusion of crops associated with the rise and spread of agriculture, the later movement via ancient trading networks, and the exchange between the Old and New Worlds over the last ∼550 years after the European colonization of the Americas. We also examine the various genetic mechanisms associated with the evolutionary adaptation of crops to their new environments after dispersal, most prominently seasonal adaptation associated with movement across latitudes, as well as altitudinal, temperature, and other environmental factors.

Biodiversity conservation requires conserving evolutionary potential—the capacity for wild populations to adapt. Understanding genetic diversity and evolutionary dynamics is critical for informing conservation decisions that enhance adaptability and persistence under environmental change. We review how emerging landscape genomic methods provide plant conservation programs with insights into evolutionary dynamics, including local adaptation and its environmental drivers. Landscape genomic approaches that explore relationships between genomic variation and environments complement rather than replace established population genomic and common garden approaches for assessing adaptive phenotypic variation, population structure, gene flow, and demography. Collectively, these approaches inform conservation actions, including genetic rescue, maladaptation prediction, and assisted gene flow. The greatest on-the-ground impacts from such studies will be realized when conservation practitioners are actively engaged in research and monitoring. Understanding the evolutionary dynamics shaping the genetic diversity of wild plant populations will inform plant conservation decisions that enhance the adaptability and persistence of species in an uncertain future.

C4 perennial bioenergy grasses are an economically and ecologically important group whose responses to climate change will be important to the future bioeconomy. These grasses are highly productive and frequently possess large geographic ranges and broad environmental tolerances, which may contribute to the evolution of ecotypes that differ in physiological acclimation capacity and the evolution of distinct functional strategies. C4 perennial bioenergy grasses are predicted to thrive under climate change—C4 photosynthesis likely evolved to enhance photosynthetic efficiency under stressful conditions of low [CO2], high temperature, and drought—although few studies have examined how these species will respond to combined stresses or to extremes of temperature and precipitation. Important targets for C4 perennial bioenergy production in a changing world, such as sustainability and resilience, can benefit from combining knowledge of C4 physiology with recent advances in crop improvement, especially genomic selection.

A major bottleneck in the crop improvement pipeline is our ability to phenotype crops quickly and efficiently. Image-based, high-throughput phenotyping has a number of advantages because it is nondestructive and reduces human labor, but a new challenge arises in extracting meaningful information from large quantities of image data. Deep learning, a type of artificial intelligence, is an approach used to analyze image data and make predictions on unseen images that ultimately reduces the need for human input in computation. Here, we review the basics of deep learning, assessments of deep learning success, examples of applications of deep learning in plant phenomics, best practices, and open challenges.

Progressive loss of plant diversity requires the protection of wild and agri-/horticultural species. For species whose seeds are extremely short-lived, or rarely or never produce seeds, or whose genetic makeup must be preserved, cryopreservation offers the only possibility for long-term conservation. At temperatures below freezing, most vegetative plant tissues suffer severe damage from ice crystal formation and require protection. In this review, we describe how increasing the concentration of cellular solutes by air drying or adding cryoprotectants, together with rapid cooling, results in a vitrified, highly viscous state in which cells can remain viable and be stored. On this basis, a range of dormant bud–freezing, slow-cooling, and (droplet-)vitrification protocols have been developed, but few are used to cryobank important agricultural/horticultural/timber and threatened species. To improve cryopreservation efficiency, the effects of cryoprotectants and molecular processes need to be understood and the costs for cryobanking reduced. However, overall, the long-term costs of cryopreservation are low, while the benefits are huge.