Annual Review of Plant Biology - Early Publication

RNA orchestrates intricate structures that influence gene expression and protein production in all living organisms, with implications for fundamental biology, medicine, and agriculture. Although extensive research has been conducted on RNA biology, many regulatory mechanisms remain elusive due to the complex and dynamic nature of RNA structures and past technological limitations. Recent advancements in RNA structure technology have revolutionized plant RNA biology research. Here, we review cutting-edge technologies for studying RNA structures in plants and their functional significance in diverse biological processes. Additionally, we highlight the pivotal role of RNA structure in influencing plant growth, development, and responses to environmental stresses. We also discuss the potential evolutionary significance of RNA structure in natural adaptation and crop domestication. Finally, we propose leveraging RNA structure–mediated gene regulation as an innovative strategy to bolster plant resilience against climate change.

Plant roots play myriad roles that include foraging for resources in complex soil environments. Within this highly dynamic soil environment roots must sense, interact with, and acclimate to factors such as water availability, microbiota, and heterogeneous distribution of nutrients. To aid their acclimation, roots alter their growth and development to optimize their architecture and actively regulate the physical, chemical, and biological properties of their rhizosphere. Understanding the complex interactions between roots and rhizosphere is critical for designing future crops with improved root traits better adapted to diverse and challenging soil conditions. However, studying roots and their interactions with soil under real-world conditions presents significant challenges. Addressing these challenges demands developing realistic laboratory-based model systems and innovative field-based root imaging techniques. Our review surveys the current knowledge and recent advances in understanding root–environment interactions while proposing future solutions to study roots under more “real-life” soil conditions.

Root exudation is the process by which plants release organic and inorganic metabolites from their roots into the surrounding soil. Root exudation is a dynamic process and shapes plant–environment interactions at the root–soil interface. Little is known about the biological and environmental factors that shape the exuded metabolome, hereafter referred to as the exudome, despite its importance in structuring soil processes. Here, we emphasize plant physiological and morphological traits that modulate the exudome in a species- and developmental stage–specific manner. We further discuss how environmental factors drive exudation processes. We highlight evidence of a potential circadian exudation rhythm and further illustrate how the physical (temperature, structure), chemical (moisture, pH, nutrients, pollutants), and biological (micro- and macrofauna) properties of soil alter the root exudome composition and release patterns. Exploring the factors that directly or indirectly modulate exudation will enhance our understanding of how this dynamic process mediates plant–environment interactions.

Immune system incompatibilities between naturally occurring genomic variants underlie many hybrid defects in plants and present a barrier for crop improvement. In this review, we approach immune system incompatibilities from pan-genomic and network perspectives. Pan-genomes offer insights into how natural variation shapes the evolutionary landscape of immune system incompatibilities, and through it, selection, polymorphisms, and recombination resistance emerge as common features that synergistically drive these incompatibilities. By contextualizing incompatibilities within the immune network, immune receptor promiscuity, complex dysregulation, and single-point failure appear to be recurrent themes of immune system defects. As geneticists break genes to investigate their function, so can we investigate broken immune systems to enrich our understanding of plant immune systems and work toward improving them.

The genetics model system Arabidopsis thaliana (L.) Heynh. lives across a vast geographic range with contrasting climates, in response to which it has evolved diverse life histories and phenotypic adaptations. In the last decade, the cataloging of worldwide populations, DNA sequencing of whole genomes, and conducting of outdoor field experiments have transformed it into a powerful evolutionary ecology system to understand the genomic basis of adaptation. Here, we summarize new insights on Arabidopsis following the coordinated efforts of the 1001 Genomes Project, the latest reconstruction of biogeographic and demographic history, and the systematic genomic mapping of trait natural variation through 15 years of genome-wide association studies. We then put this in the context of local adaptation across climates by summarizing insights from 73 Arabidopsis outdoor common garden experiments conducted to date. We conclude by highlighting how molecular and genomic knowledge of adaptation can help us to understand species’ (mal)adaptation under ongoing climate change.

Histones are far more than just the basic units of chromatin. Posttranslational modifications of histone tails have emerged as important regulatory mechanisms for diverse biological processes, including genome organization, gene expression, transposable element suppression, development, and environmental responses. This field is expanding rapidly with the development of new technologies and growing interest from both the basic and translational research communities. The past two decades have witnessed tremendous progress in our understanding of the complex, multilayered regulation and actions of histone modifications in plants. This review summarizes the characteristics, localization, and molecular functions of histone modifications with an emphasis on the well-studied marks in Arabidopsis. We further discuss their functions in developmental transitions and environmental responses as well as their contributions to epigenomic diversity and plasticity. By highlighting the functions and fundamental mechanisms of epigenetic modifications in model plants, this review underscores the potential to harness epigenetic regulation for agricultural improvement.

The centromeres of eukaryotic chromosomes are required to load CENH3/CENP-A variant nucleosomes and the kinetochore complex, which connects to spindle microtubules during cell division. Despite their conserved function, plant centromeres show rapid sequence evolution within and between species and a range of monocentric, holocentric, and polymetacentric architectures, which vary in kinetochore numbers and spacing. Plant centromeres are commonly composed of tandem satellite repeat arrays, which are invaded by specific families of centrophilic retrotransposons, whereas in some species the entire centromere is composed of such retrotransposons. We review the diversity of plant centrophilic retrotransposons and their mechanisms of integration, together with how epigenetic information and small RNAs control their proliferation. We discuss models for rapid centromere sequence evolution and speculate on the roles that centrophilic retrotransposons may play in centromere dynamics. We focus on plants but draw comparisons with animal and fungal centromeric transposons to highlight conserved and divergent themes across the eukaryotes.

Modern agricultural practices rely on high-input, intensive cultivation of a few crop varieties with limited diversity, increasing the vulnerability of our agricultural systems to biotic and abiotic stresses and the effects of climate changes. This necessitates a paradigm shift toward a more sustainable agricultural model to ensure a stable and dependable food supply for the burgeoning global population. Leveraging knowledge from crop biology, genetics, and genomics, alongside state-of-the-art biotechnologies, rational redomestication has emerged as a targeted and knowledge-driven approach to crop innovation. This strategy aims to broaden the range of species available for agriculture, restore lost genetic diversity, and further improve existing domesticated crops. We summarize how diverse plants can be exploited in rational redomestication endeavors, including wild species, underutilized plants, and domesticated crops. Equipped with rational redomestication approaches, we propose different strategies to empower the fast and slow breeding systems distinguished by plant reproduction systems.

Pectins underpin the assembly, molecular architecture, and physical properties of plant cell walls and through their effects on cell growth and adhesion influence many aspects of plant development. They are some of the most dynamic components of plant cell walls, and pectin remodeling and degradation by pectin-modifying enzymes can drive developmental programming via physical effects on the cell wall and the generation of oligosaccharides that can act as signaling ligands. Here, we introduce pectin structure and synthesis and discuss pectin functions in plants. We highlight recent advances in understanding the structure–function relationships of pectin-modifying enzymes and their products and how these advances point toward new approaches to bridging key knowledge gaps and manipulating pectin dynamics to control plant development. Finally, we discuss how a deeper understanding of pectin dynamics might enable innovations in agronomy and biotechnology, unlocking new benefits from these ubiquitous but complex polysaccharides.

Plant cells are defined by their walls, which, in addition to providing structural support and shape, are an integral component of the nonliving extracellular space called the apoplast. Cell wall thickenings are present in many different root cell types. They come in a variety of simple and more complex structures with varying composition of lignin and suberin and can change in response to environmental stressors. The majority of these root cell wall thickenings and cell types that contain them are absent in the model plant Arabidopsis thaliana despite being present in most plant species. As a result, we know very little regarding their developmental control and function. Increasing evidence suggests that these structures are critical for responding to and facilitating adaptation to a wide array of stresses that a plant root experiences. These structures function in blocking apoplastic transport, oxygen, and water loss and enhancing root penetrative strength. In this review, we describe the most common types of cell wall thickenings in the outer cell types of plant roots—the velamen, exodermal thickenings, the sclerenchyma, and phi thickenings. Their cell-type dependency, morphology, composition, environmental responsiveness, and genetic control in vascular plants are discussed, as well as their potential to generate more stress-resilient roots in the face of a changing climate.