Replicated Evolution in Plants

Similar traits and functions commonly evolve in nature. Here, we explore patterns of replicated evolution across the plant kingdom and discuss the processes responsible for such patterns. We begin this review by defining replicated evolution and the theoretical, genetic, and ecological concepts that help explain it. We then focus our attention on empirical cases of replicated evolution at the phenotypic and genotypic levels. We find that replication at the ecotype level is common, but evidence for repeated ecological speciation is surprisingly sparse. On the other hand, the replicated evolution of ecological strategies and physiological mechanisms across similar biomes appears to be pervasive. We conclude by highlighting where future efforts can help us bridge the understanding of replicated evolution across different levels of biological organization. Earth's landscape is diverse but also repeats itself. Organisms seem to have followed suit.

Temperature Sensing in Plants

Temperature is a key environmental cue that influences the distribution and behavior of plants globally. Understanding how plants sense temperature and integrate this information into their development is important to determine how plants adapt to climate change and to apply this knowledge to the breeding of climate-resilient crops. The mechanisms of temperature perception in eukaryotes are only just beginning to be understood, with multiple molecular phenomena with inherent temperature dependencies, such as RNA melting, phytochrome dark reversion, and protein phase change, being exploited by nature to create thermosensory signaling networks. Here, we review recent progress in understanding how temperature sensing in four major pathways in occurs: vernalization, cold stress, thermomorphogenesis, and heat stress. We discuss outstanding questions in the field and the importance of these mechanisms in the context of breeding climate-resilient crops.

Why Are Invasive Plants Successful?

Plant invasions, a byproduct of globalization, are increasing worldwide. Because of their ecological and economic impacts, considerable efforts have been made to understand and predict the success of non-native plants. Numerous frameworks, hypotheses, and theories have been advanced to conceptualize the interactions of multiple drivers and context dependence of invasion success with the aim of achieving robust explanations with predictive power. We review these efforts from a community-level perspective rather than a biogeographical one, focusing on terrestrial systems, and explore the roles of intrinsic plant properties in determining species invasiveness, as well as the effects of biotic and abiotic conditions in mediating ecosystem invasibility (or resistance) and ecological and evolutionary processes. We also consider the fundamental influences of human-induced changes at scales ranging from local to global in triggering, promoting, and sustaining plant invasions and discuss how these changes could alter future invasion trajectories.

Optogenetic Methods in Plant Biology

Optogenetics is a technique employing natural or genetically engineered photoreceptors in transgene organisms to manipulate biological activities with light. Light can be turned on or off, and adjusting its intensity and duration allows optogenetic fine-tuning of cellular processes in a noninvasive and spatiotemporally resolved manner. Since the introduction of Channelrhodopsin-2 and phytochrome-based switches nearly 20 years ago, optogenetic tools have been applied in a variety of model organisms with enormous success, but rarely in plants. For a long time, the dependence of plant growth on light and the absence of retinal, the rhodopsin chromophore, prevented the establishment of plant optogenetics until recent progress overcame these difficulties. We summarize the recent results of work in the field to control plant growth and cellular motion via green light–gated ion channels and present successful applications to light-control gene expression with single or combined photoswitches in plants. Furthermore, we highlight the technical requirements and options for future plant optogenetic research.

Mycorrhizal Symbiosis in Plant Growth and Stress Adaptation: From Genes to Ecosystems

Plant roots associate with diverse microbes (including bacteria, fungi, archaea, protists, and viruses) collectively called the root-associated microbiome. Among them, mycorrhizal fungi colonize host roots and improve their access to nutrients, usually phosphorus and nitrogen. In exchange, plants deliver photosynthetic carbon to the colonizing fungi. This nutrient exchange affects key soil processes, the carbon cycle, and plant health and therefore has a strong influence on the plant and microbe ecosystems. The framework of nutrient exchange and regulation between host plant and arbuscular mycorrhizal fungi has recently been established. The local and systemic regulation of mycorrhizal symbiosis by plant nutrient status and the autoregulation of mycorrhizae are strategies by which plants maintain a stabilizing free-market symbiosis. A better understanding of the synergistic effects between mycorrhizal fungi and mycorrhizosphere microorganisms is an essential precondition for their use as biofertilizers and bioprotectors for sustainable agriculture and forestry management.

Proximity Labeling in Plants

Proteins are workhorses in the cell; they form stable and more often dynamic, transient protein–protein interactions, assemblies, and networks and have an intimate interplay with DNA and RNA. These network interactions underlie fundamental biological processes and play essential roles in cellular function. The proximity-dependent biotinylation labeling approach combined with mass spectrometry (PL-MS) has recently emerged as a powerful technique to dissect the complex cellular network at the molecular level. In PL-MS, by fusing a genetically encoded proximity-labeling (PL) enzyme to a protein or a localization signal peptide, the enzyme is targeted to a protein complex of interest or to an organelle, allowing labeling of proximity proteins within a zoom radius. These biotinylated proteins can then be captured by streptavidin beads and identified and quantified by mass spectrometry. Recently engineered PL enzymes such as TurboID have a much-improved enzymatic activity, enabling spatiotemporal mapping with a dramatically increased signal-to-noise ratio. PL-MS has revolutionized the way we perform proteomics by overcoming several hurdles imposed by traditional technology, such as biochemical fractionation and affinity purification mass spectrometry. In this review, we focus on biotin ligase–based PL-MS applications that have been, or are likely to be, adopted by the plant field. We discuss the experimental designs and review the different choices for engineered biotin ligases, enrichment, and quantification strategies. Lastly, we review the validation and discuss future perspectives.

The Game of Timing: Circadian Rhythms Intersect with Changing Environments

Recurring patterns are an integral part of life on Earth. Through evolution or breeding, plants have acquired systems that coordinate with the cyclic patterns driven by Earth's movement through space. The biosystem responses to these physical rhythms result in biological cycles of daily and seasonal activity that feed back into the physical cycles. Signaling networks to coordinate growth and molecular activities with these persistent cycles have been integrated into plant biochemistry. The plant circadian clock is the coordinator of this complex, multiscale, temporal schedule. However, we have detailed knowledge of the circadian clock components and functions in only a few species under controlled conditions. We are just beginning to understand how the clock functions in real-world conditions. This review examines what we know about the circadian clock in diverse plant species, the challenges with extrapolating data from controlled environments, and the need to anticipate how plants will respond to climate change.

Chloroplast Proteostasis: Import, Sorting, Ubiquitination, and Proteolysis

Chloroplasts are the defining plant organelles with responsibility for photosynthesis and other vital functions. To deliver these functions, they possess a complex proteome comprising thousands of largely nucleus-encoded proteins. Composition of the proteome is controlled by diverse processes affecting protein translocation and degradation—our focus here. Most chloroplast proteins are imported from the cytosol via multiprotein translocons in the outer and inner envelope membranes (the TOC and TIC complexes, respectively), or via one of several noncanonical pathways, and then sorted by different systems to organellar subcompartments. Chloroplast proteolysis is equally complex, involving the concerted action of internal proteases of prokaryotic origin and the nucleocytosolic ubiquitin–proteasome system (UPS). The UPS degrades unimported proteins in the cytosol and chloroplast-resident proteins via chloroplast-associated protein degradation (CHLORAD). The latter targets the TOC apparatus to regulate protein import, as well as numerous internal proteins directly, to reconfigure chloroplast functions in response to developmental and environmental signals.

Plant Hormone Transport and Localization: Signaling Molecules on the Move

Plant hormones are a group of small signaling molecules produced by plants at very low concentrations that have the ability to move and function at distal sites. Hormone homeostasis is critical to balance plant growth and development and is regulated at multiple levels, including hormone biosynthesis, catabolism, perception, and transduction. In addition, plants move hormones over short and long distances to regulate various developmental processes and responses to environmental factors. Transporters coordinate these movements, resulting in hormone maxima, gradients, and cellular and subcellular sinks. Here, we summarize the current knowledge of most of the characterized plant hormone transporters with respect to biochemical, physiological, and developmental activities. We further discuss the subcellular localizations of transporters, their substrate specificities, and the need for multiple transporters for the same hormone in the context of plant growth and development.

The Evolution and Evolvability of Photosystem II

Photosystem II is the water-oxidizing and O-evolving enzyme of photosynthesis. How and when this remarkable enzyme arose are fundamental questions in the history of life that have remained difficult to answer. Here, recent advances in our understanding of the origin and evolution of photosystem II are reviewed and discussed in detail. The evolution of photosystem II indicates that water oxidation originated early in the history of life, long before the diversification of cyanobacteria and other major groups of prokaryotes, challenging and transforming current paradigms on the evolution of photosynthesis. We show that photosystem II has remained virtually unchanged for billions of years, and yet the nonstop duplication process of the D1 subunit of photosystem II, which controls photochemistry and catalysis, has enabled the enzyme to become adaptable to variable environmental conditions and even to innovate enzymatic functions beyond water oxidation. We suggest that this evolvability can be harnessed to develop novel light-powered enzymes with the capacity to carry out complex multistep oxidative transformations for sustainable biocatalysis.