Annual Review of Plant Biology - Volume 70, 2019

When first asked to write a review of my life as a scientist, I doubted anyone would be interested in reading it. In addition, I did not really want to compose my own memorial. However, after discussing the idea with other scientists who have written autobiographies, I realized that it might be fun to dig into my past and to reflect on what has been important for me, my life, my family, my friends and colleagues, and my career. My life and research has taken me from bacteriophage to Agrobacterium tumefaciens–mediated DNA transfer to plants to the plant genome and its environmentally induced changes. I went from being a naïve, young student to a postdoc and married mother of two to the leader of an ever-changing group of fantastic coworkers—a journey made rich by many interesting scientific milestones, fascinating exploration of all corners of the world, and marvelous friendships.

Plant mitochondria play a major role during respiration by producing the ATP required for metabolism and growth. ATP is produced during oxidative phosphorylation (OXPHOS), a metabolic pathway coupling electron transfer with ADP phosphorylation via the formation and release of a proton gradient across the inner mitochondrial membrane. The OXPHOS system is composed of large, multiprotein complexes coordinating metal-containing cofactors for the transfer of electrons. In this review, we summarize the current state of knowledge about assembly of the OXPHOS complexes in land plants. We present the different steps involved in the formation of functional complexes and the regulatory mechanisms controlling the assembly pathways. Because several assembly steps have been found to be ancestral in plants—compared with those described in fungal and animal models—we discuss the evolutionary dynamics that lead to the conservation of ancestral pathways in land plant mitochondria.

Chloroplasts contain high amounts of monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) and low levels of the anionic lipids sulfoquinovosyldiacylglycerol (SQDG), phosphatidylglycerol (PG), and glucuronosyldiacylglycerol (GlcADG). The mostly extraplastidial lipid phosphatidylcholine is found only in the outer envelope. Chloroplasts are the major site for fatty acid synthesis. In Arabidopsis, a certain proportion of glycerolipids is entirely synthesized in the chloroplast (prokaryotic lipids). Fatty acids are also exported to the endoplasmic reticulum and incorporated into lipids that are redistributed to the chloroplast (eukaryotic lipids). MGDG, DGDG, SQDG, and PG establish the thylakoid membranes and are integral constituents of the photosynthetic complexes. Phosphate deprivation induces phospholipid degradation accompanied by the increase in DGDG, SQDG, and GlcADG. During freezing and drought stress, envelope membranes are stabilized by the conversion of MGDG into oligogalactolipids. Senescence and chlorotic stress lead to lipid and chlorophyll degradation and the deposition of acyl and phytyl moieties as fatty acid phytyl esters.

The N-degron pathway, formerly the N-end rule pathway, regulates functions of regulatory proteins. It impacts protein half-life and therefore directs the actual presence of target proteins in the cell. The current concept holds that the N-degron pathway depends on the identity of the amino (N)-terminal amino acid and many other factors, such as the follow-up sequence at the N terminus, conformation, flexibility, and protein localization. It is evolutionarily conserved throughout the kingdoms. One possible entry point for substrates of the N-degron pathway is oxidation of N-terminal Cys residues. Oxidation of N-terminal Cys is decisive for further enzymatic modification of various neo–N termini by arginylation that generates potentially neofunctionalized or instable proteoforms. Here, I focus on the posttranslational modifications that are encompassed by protein degradation via the Cys/Arg branch of the N-degron pathway—part of the PROTEOLYSIS 6 (PRT6)/N-degron pathway—as well as the underlying physiological principles of this branch and its biological significance in stress response.

Assessing posttranslational modification (PTM) patterns within protein molecules and reading their functional implications present grand challenges for plant biology. We combine four perspectives on PTMs and their roles by considering five classes of PTMs as examples of the broader context of PTMs. These include modifications of the N terminus, glycosylation, phosphorylation, oxidation, and N-terminal and protein modifiers linked to protein degradation. We consider the spatial distribution of PTMs, the subcellular distribution of modifying enzymes, and their targets throughout the cell, and we outline the complexity of compartmentation in understanding of PTM function. We also consider PTMs temporally in the context of the lifetime of a protein molecule and the need for different PTMs for assembly, localization, function, and degradation. Finally, we consider the combined action of PTMs on the same proteins, their interactions, and the challenge ahead of integrating PTMs into an understanding of protein function in plants.

During the past decade, a flurry of research focusing on the role of peptides as short- and long-distance signaling molecules in plant cell communication has been undertaken. Here, we focus on peptides derived from nonfunctional precursors, and we address several key questions regarding peptide signaling. We provide an overview of the regulatory steps involved in producing a biologically active peptide ligand that can bind its corresponding receptor(s) and discuss how this binding and subsequent activation lead to specific cellular outputs. We discuss different experimental approaches that can be used to match peptide ligands with their receptors. Lastly, we explore how peptides evolved from basic signaling units regulating essential processes in plants to more complex signaling systems as new adaptive traits developed and how nonplant organisms exploit this signaling machinery by producing peptide mimics.

Although flavor is an essential element for consumer acceptance of food, breeding programs have focused primarily on yield, leading to significant declines in flavor for many vegetables. The deterioration of flavor quality has concerned breeders; however, the complexity of this trait has hindered efforts to improve or even maintain it. Recently, the integration of flavor-associated metabolic profiling with other omics methodologies derived from big data has become a prominent trend in this research field. Here, we provide an overview of known metabolites contributing to flavor in the major vegetables as well as genetic analyses of the relevant metabolic pathways based on different approaches, especially multi-omics. We present examples demonstrating how omics analyses can help us to understand the accomplishments of historical flavor breeding practices and implement further improvements. The integration of genetics, cultivation, and postharvest practices with genome-scale data analyses will create enormous potential for further flavor quality improvements.

Heterotrimeric GTP-binding proteins are key regulators of a multitude of signaling pathways in all eukaryotes. Although the core G-protein components and their basic biochemistries are broadly conserved throughout evolution, the regulatory mechanisms of G proteins seem to have been rewired in plants to meet specific needs. These proteins are currently the focus of intense research in plants due to their involvement in many agronomically important traits, such as seed yield, organ size regulation, biotic and abiotic stress responses, symbiosis, and nitrogen use efficiency. The availability of massive sequence information from a variety of plant species, extensive biochemical data generated over decades, and impressive genetic resources for plant G proteins have made it possible to examine their role, unique properties, and novel regulation. This review focuses on some recent advances in our understanding of the mechanistic details of this critical signaling pathway to enable the precise manipulation and generation of plants to meet future needs.

Plant cells divide their cytoplasmic content by forming a new membrane compartment, the cell plate, via a rerouting of the secretory pathway toward the division plane aided by a dynamic cytoskeletal apparatus known as the phragmoplast. The phragmoplast expands centrifugally and directs the cell plate to the preselected division site at the plasma membrane to fuse with the parental wall. The division site is transiently decorated by the cytoskeletal preprophase band in preprophase and prophase, whereas a number of proteins discovered over the last decade reside continuously at the division site and provide a lasting spatial reference for phragmoplast guidance. Recent studies of membrane fusion at the cell plate have revealed the contribution of functionally conserved eukaryotic proteins to distinct stages of cell plate biogenesis and emphasize the coupling of cell plate formation with phragmoplast expansion. Together with novel findings concerning preprophase band function and the setup of the division site, cytokinesis and its spatial control remain an open-ended field with outstanding and challenging questions to resolve.

A fascinating feature of plant growth and development is that plants initiate organs continually throughout their lifespan. The ability to do this relies on specialized groups of pluripotent stem cells termed meristems, which allow for the elaboration of the shoot, root, and vascular systems. We now have a deep understanding of the genetic networks that control meristem initiation and stem cell maintenance, including the roles of receptors and their ligands, transcription factors, and integrated hormonal and chromatin control. This review describes these networks and discusses how this knowledge is being applied to improve crop productivity by increasing fruit size and seed number.

Stem cell populations in meristematic tissues at distinct locations in the plant body provide the potency of continuous plant growth. Primary meristems, at the apices of the plant body, contribute mainly to the elongation of the main plant axes, whereas secondary meristems in lateral positions are responsible for the thickening of these axes. The stem cells of the vascular cambium—a secondary lateral meristem—produce the secondary phloem (bast) and secondary xylem (wood). The sites of primary and secondary growth are spatially separated, and mobile signals are expected to coordinate growth rates between apical and lateral stem cell populations. Although the underlying mechanisms have not yet been uncovered, it seems likely that hormones, peptides, and mechanical cues orchestrate primary and secondary growth. In this review, we highlight the current knowledge and recent discoveries of how cambial stem cell activity is regulated, with a focus on mobile signals and the response of cambial activity to environmental and stress factors.

When exposed to warmer, nonstressful average temperatures, some plant organs grow and develop at a faster rate without affecting their final dimensions. Other plant organs show specific changes in morphology or development in a response termed thermomorphogenesis. Selected coding and noncoding RNA, chromatin features, alternative splicing variants, and signaling proteins change their abundance, localization, and/or intrinsic activity to mediate thermomorphogenesis. Temperature, light, and circadian clock cues are integrated to impinge on the level or signaling of hormones such as auxin, brassinosteroids, and gibberellins. The light receptor phytochrome B (phyB) is a temperature sensor, and the phyB–PHYTOCHROME-INTERACTING FACTOR 4 (PIF4)–auxin module is only one thread in a complex network that governs temperature sensitivity. Thermomorphogenesis offers an avenue to search for climate-smart plants to sustain crop and pasture productivity in the context of global climate change.

Leaf senescence is an important developmental process involving orderly disassembly of macromolecules for relocating nutrients from leaves to other organs and is critical for plants’ fitness. Leaf senescence is the response of an intricate integration of various environmental signals and leaf age information and involves a complex and highly regulated process with the coordinated actions of multiple pathways. Impressive progress has been made in understanding how senescence signals are perceived and processed, how the orderly degeneration process is regulated, how the senescence program interacts with environmental signals, and how senescence regulatory genes contribute to plant productivity and fitness. Employment of systems approaches using omics-based technologies and characterization of key regulators have been fruitful in providing newly emerging regulatory mechanisms. This review mainly discusses recent advances in systems understanding of leaf senescence from a molecular network dynamics perspective. Genetic strategies for improving the productivity and quality of crops are also described.

Plants reprogram somatic cells following injury and regenerate new tissues and organs. Upon perception of inductive cues, somatic cells often dedifferentiate, proliferate, and acquire new fates to repair damaged tissues or develop new organs from wound sites. Wound stress activates transcriptional cascades to promote cell fate reprogramming and initiate new developmental programs. Wounding also modulates endogenous hormonal responses by triggering their biosynthesis and/or directional transport. Auxin and cytokinin play pivotal roles in determining cell fates in regenerating tissues and organs. Exogenous application of these plant hormones enhances regenerative responses in vitro by facilitating the activation of specific developmental programs. Many reprogramming regulators are epigenetically silenced during normal development but are activated by wound stress and/or hormonal cues.

Water transport in vascular plants represents a critical component of terrestrial water cycles and supplies the water needed for the exchange of CO2 in the atmosphere for photosynthesis. Yet, many fundamental principles of water transport are difficult to assess given the scale and location of plant xylem. Here we review the mechanistic principles that underpin long-distance water transport in vascular plants, with a focus on woody species. We also discuss the recent development of noninvasive tools to study the functional status of xylem networks in planta. Limitations of current methods to detect drought-induced xylem blockages (e.g., embolisms) and quantify corresponding declines in sap flow, and the coordination of hydraulic dysfunction with other physiological processes are assessed. Future avenues of research focused on cross-validation of plant hydraulics methods are discussed, as well as a proposed fundamental shift in the theory and methodology used to characterize and measure plant water use.

The size of seeds affects not only evolutionary fitness but also grain yield of crops. Understanding the mechanisms controlling seed size has become an important research field in plant science. Seed size is determined by the integrated signals of maternal and zygotic tissues, which control the coordinated growth of the embryo, endosperm, and seed coat. Recent advances have identified several signaling pathways that control seed size through maternal tissues, including or involving the ubiquitin-proteasome pathway, G-protein signaling, mitogen-activated protein kinase (MAPK) signaling, phytohormone perception and homeostasis, and some transcriptional regulators. Meanwhile, growth of the zygotic tissues is regulated in part by the HAIKU (IKU) pathway and phytohormones. This review provides a general overview of current findings in seed size control and discusses the emerging molecular mechanisms and regulatory networks found to be involved.

In order to optimally establish their root systems, plants are endowed with several mechanisms to use at distinct steps during their development. In this review, we zoom in on the major processes involved in root development and detail important new insights that have been generated in recent studies, mainly using the Arabidopsis root as a model. First, we discuss new insights in primary root development with the characterization of tissue-specific transcription factor complexes and the identification of non-cell-autonomous control mechanisms in the root apical meristem. Next, root branching is discussed by focusing on the earliest steps in the development of a new lateral root and control of its postemergence growth. Finally, we discuss the impact of phosphate, nitrogen, and water availability on root development and summarize current knowledge about the major molecular mechanisms involved.

MicroRNAs (miRNAs) are 20–24 nucleotide noncoding RNAs abundant in plants and animals. The biogenesis of plant miRNAs involves transcription of miRNA genes, processing of primary miRNA transcripts by DICER-LIKE proteins into mature miRNAs, and loading of mature miRNAs into ARGONAUTE proteins to form miRNA-induced silencing complex (miRISC). By targeting complementary sequences, miRISC negatively regulates gene expression, thereby coordinating plant development and plant–environment interactions. In this review, we present and discuss recent updates on the mechanisms and regulation of miRNA biogenesis, miRISC assembly and actions as well as the regulatory roles of miRNAs in plant developmental plasticity, abiotic/biotic responses, and symbiotic/parasitic interactions. Finally, we suggest future directions for plant miRNA research.

Diverse molecular processes regulate the interactions between plants and insect herbivores. Here, we review genes and proteins that are involved in plant–herbivore interactions and discuss how their discovery has structured the current standard model of plant–herbivore interactions. Plants perceive damage-associated and, possibly, herbivore-associated molecular patterns via receptors that activate early signaling components such as Ca²⁺, reactive oxygen species, and MAP kinases. Specific defense reprogramming proceeds via signaling networks that include phytohormones, secondary metabolites, and transcription factors. Local and systemic regulation of toxins, defense proteins, physical barriers, and tolerance traits protect plants against herbivores. Herbivores counteract plant defenses through biochemical defense deactivation, effector-mediated suppression of defense signaling, and chemically controlled behavioral changes. The molecular basis of plant–herbivore interactions is now well established for model systems. Expanding molecular approaches to unexplored dimensions of plant–insect interactions should be a future priority.

Ecological specialization in plants occurs primarily through local adaptation to different environments. Local adaptation is widely thought to result in costly fitness trade-offs that result in maladaptation to alternative environments. However, recent studies suggest that such trade-offs are not universal. Further, there is currently a limited understanding of the molecular mechanisms responsible for fitness trade-offs associated with adaptation. Here, we review the literature on stress responses in plants to identify potential mechanisms underlying local adaptation and ecological specialization. We focus on drought, high and low temperature, flooding, herbivore, and pathogen stresses. We then synthesize our findings with recent advances in the local adaptation and plant molecular biology literature. In the process, we identify mechanisms that could cause fitness trade-offs and outline scenarios where trade-offs are not a necessary consequence of adaptation. Future studies should aim to explicitly integrate molecular mechanisms into studies of local adaptation.