Annual Review of Plant Biology - Volume 71, 2020

Zhi-Hong Xu is a plant physiologist who studied botany at Peking University (1959–1965). He joined the Shanghai Institute of Plant Physiology (SIPP), Chinese Academy of Sciences (CAS), as a graduate student in 1965. He recalls what has happened for the institute, during the Cultural Revolution, and he witnessed the spring of science eventually coming to China. Xu was a visiting scholar at the John Innes Institute and in the Department of Botany at Nottingham University in the United Kingdom (1979–1981). He became deputy director of SIPP in 1983 and director in 1991; he also chaired the State Key Laboratory of Plant Molecular Genetics SIPP (1988–1996). He worked as a visiting scientist in the Institute of Molecular and Cell Biology, National University of Singapore, for three months each year (1989–1992). He served as vice president of CAS (1992–2002) and as president of Peking University (1999–2008). Over these periods he was heavily involved in the design and implementation of major scientific projects in life sciences and agriculture in China. He is an academician of CAS and member of the Academy of Sciences for the Developing World. His scientific contributions mainly cover plant tissue culture, hormone mechanism in development, as well as plant developmental response to environment. Xu, as a scientist and leader who has made an impact in the community, called up a lot of excellent young scientists returning to China. His efforts have promoted the fast development of China's plant and agricultural sciences.

Plant cell walls are dynamic structures that are synthesized by plants to provide durable coverings for the delicate cells they encase. They are made of polysaccharides, proteins, and other biomolecules and have evolved to withstand large amounts of physical force and to resist external attack by herbivores and pathogens but can in many cases expand, contract, and undergo controlled degradation and reconstruction to facilitate developmental transitions and regulate plant physiology and reproduction. Recent advances in genetics, microscopy, biochemistry, structural biology, and physical characterization methods have revealed a diverse set of mechanisms by which plant cells dynamically monitor and regulate the composition and architecture of their cell walls, but much remains to be discovered about how the nanoscale assembly of these remarkable structures underpins the majestic forms and vital ecological functions achieved by plants.

Anionic phospholipids, which include phosphatidic acid, phosphatidylserine, and phosphoinositides, represent a small percentage of membrane lipids. They are able to modulate the physical properties of membranes, such as their surface charges, curvature, or clustering of proteins. Moreover, by mediating interactions with numerous membrane-associated proteins, they are key components in the establishment of organelle identity and dynamics. Finally, anionic lipids also act as signaling molecules, as they are rapidly produced or interconverted by a set of dedicated enzymes. As such, anionic lipids are major regulators of many fundamental cellular processes, including cell signaling, cell division, membrane trafficking, cell growth, and gene expression. In this review, we describe the functions of anionic lipids from a cellular perspective. Using the localization of each anionic lipid and its related metabolic enzymes as starting points, we summarize their roles within the different compartments of the endomembrane system and address their associated developmental and physiological consequences.

Cryptochromes are blue-light receptors that mediate photoresponses in plants. The genomes of most land plants encode two clades of cryptochromes, CRY1 and CRY2, which mediate distinct and overlapping photoresponses within the same species and between different plant species. Photoresponsive protein–protein interaction is the primary mode of signal transduction of cryptochromes. Cryptochromes exist as physiologically inactive monomers in the dark; the absorption of photons leads to conformational change and cryptochrome homooligomerization, which alters the affinity of cryptochromes interacting with cryptochrome-interacting proteins to form various cryptochrome complexes. These cryptochrome complexes, collectively referred to as the cryptochrome complexome, regulate transcription or stability of photoresponsive proteins to modulate plant growth and development. The activity of cryptochromes is regulated by photooligomerization; dark monomerization; cryptochrome regulatory proteins; and cryptochrome phosphorylation, ubiquitination, and degradation. Most of the more than 30 presently known cryptochrome-interacting proteins are either regulated by other photoreceptors or physically interactingwith the protein complexes of other photoreceptors. Some cryptochrome-interacting proteins are also hormonal signaling or regulatory proteins. These two mechanisms enable cryptochromes to integrate blue-light signals with other internal and external signals to optimize plant growth and development.

Because of their high level of diversity and complex evolutionary histories, most studies on plant receptor-like kinase subfamilies have focused on their kinase domains. With the large amount of genome sequence data available today, particularly on basal land plants and Charophyta, more attention should be paid to primary events that shaped the diversity of the RLK gene family. We thus focus on the motifs and domains found in association with kinase domains to illustrate their origin, organization, and evolutionary dynamics. We discuss when these different domain associations first occurred and how they evolved, based on a literature review complemented by some of our unpublished results.

Rising CO2 concentrations and their effects on plant productivity present challenging issues. Effects on the photosynthesis/photorespiration balance and changes in primary metabolism are known, caused by the competitive interaction of CO2 and O2 at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase. However, impacts on stress resistance are less clear. Reactive oxygen species are key players in biotic and abiotic stress responses, but there is no consensus on whether elevated CO2 constitutes a stress. Although high CO2 increases yield in C3 plants, it can also increase cellular oxidation and activate phytohormone defense pathways. Reduction-oxidation processes play key roles in acclimation to high CO2, with specific enzymes acting in compartment-specific signaling. Traditionally, acclimation to high CO2 has been considered in terms of altered carbon gain, but emerging evidence suggests that CO2 is a signal as well as a substrate. Some CO2 effects on defense are likely mediated independently of primary metabolism. Nonetheless, primary photosynthetic metabolism is highly integrated with defense and stress signaling pathways, meaning that plants will be able to acclimate to the changing environment over the coming decades.

C4 photosynthesis evolved multiple times independently from ancestral C3 photosynthesis in a broad range of flowering land plant families and in both monocots and dicots. The evolution of C4 photosynthesis entails the recruitment of enzyme activities that are not involved in photosynthetic carbon fixation in C3 plants to photosynthesis. This requires a different regulation of gene expression as well as a different regulation of enzyme activities in comparison to the C3 context. Further, C4 photosynthesis relies on a distinct leaf anatomy that differs from that of C3, requiring a differential regulation of leaf development in C4. We summarize recent progress in the understanding of C4-specific features in evolution and metabolic regulation in the context of C4 photosynthesis.

Research in the past decade has uncovered new and surprising information about the pathways of starch synthesis and degradation. This includes the discovery of previously unsuspected protein families required both for processes and for the long-sought mechanism of initiation of starch granules. There is also growing recognition of the central role of leaf starch turnover in making carbon available for growth across the day-night cycle. Sophisticated systems-level control mechanisms involving the circadian clock set rates of nighttime starch mobilization that maintain a steady supply of carbon until dawn and modulate partitioning of photosynthate into starch in the light, optimizing the fraction of assimilated carbon that can be used for growth. These discoveries also uncover complexities: Results from experiments with Arabidopsis leaves in conventional controlled environments are not necessarily applicable to other organs or species or to growth in natural, fluctuating environments.

Small GTP-binding proteins represent a highly conserved signaling module in eukaryotes that regulates diverse cellular processes such as signal transduction, cytoskeletal organization and cell polarity, cell proliferation and differentiation, intracellular membrane trafficking and transport vesicle formation, and nucleocytoplasmic transport. These proteins function as molecular switches that cycle between active and inactive states, and this cycle is linked to GTP binding and hydrolysis. In this review, the roles of the plant complement of small GTP-binding proteins in these cellular processes are described, as well as accessory proteins that control their activity, and current understanding of the functions of individual members of these families in plants—with a focus on the model organism Arabidopsis—is presented. Some potential novel roles of these GTPases in plants, relative to their established roles in yeast and/or animal systems, are also discussed.

The control of gaseous exchange between the leaf and external atmosphere is governed by stomatal conductance (gs); therefore, stomata play a critical role in photosynthesis and transpiration and overall plant productivity. Stomatal conductance is determined by both anatomical features and behavioral characteristics. Here we review some of the osmoregulatory pathways in guard cell metabolism, genes and signals that determine stomatal function and patterning, and the recent work that explores coordination between gs and carbon assimilation (A) and the influence of spatial distribution of functional stomata on underlying mesophyll anatomy. We also evaluate the current literature on mesophyll-driven signals that may coordinate stomatal behavior with mesophyll carbon assimilation and explore stomatal kinetics as a possible target to improve A and water use efficiency. By understanding these processes, we can start to provide insight into manipulation of these regulatory pathways to improve stomatal behavior and identify novel unexploited targets for altering stomatal behavior and improving crop plant productivity.

Mathematical modeling of plant metabolism enables the plant science community to understand the organization of plant metabolism, obtain quantitative insights into metabolic functions, and derive engineering strategies for manipulation of metabolism. Among the various modeling approaches, metabolic pathway analysis can dissect the basic functional modes of subsections of core metabolism, such as photorespiration, and reveal how classical definitions of metabolic pathways have overlapping functionality. In the many studies using constraint-based modeling in plants, numerous computational tools are currently available to analyze large-scale and genome-scale metabolic networks. For ¹³C-metabolic flux analysis, principles of isotopic steady state have been used to study heterotrophic plant tissues, while nonstationary isotope labeling approaches are amenable to the study of photoautotrophic and secondary metabolism. Enzyme kinetic models explore pathways in mechanistic detail, and we discuss different approaches to determine or estimate kinetic parameters. In this review, we describe recent advances and challenges in modeling plant metabolism.

This review focuses on the evolution of plant hormone signaling pathways. Like the chemical nature of the hormones themselves, the signaling pathways are diverse. Therefore, we focus on a group of hormones whose primary perception mechanism involves an Skp1/Cullin/F-box-type ubiquitin ligase: auxin, jasmonic acid, gibberellic acid, and strigolactone. We begin with a comparison of the core signaling pathways of these four hormones, which have been established through studies conducted in model organisms in the Angiosperms. With the advent of next-generation sequencing and advanced tools for genetic manipulation, the door to understanding the origins of hormone signaling mechanisms in plants beyond these few model systems has opened. For example, in-depth phylogenetic analyses of hormone signaling components are now being complemented by genetic studies in early diverging land plants. Here we discuss recent investigations of how basal land plants make and sense hormones. Finally, we propose connections between the emergence of hormone signaling complexity and major developmental transitions in plant evolution.

Nucleotide-binding leucine-rich repeat receptors (NLRs) monitor the plant intracellular environment for signs of pathogen infection. Several mechanisms of NLR-mediated immunity arose independently across multiple species. These include the functional specialization of NLRs into sensors and helpers, the independent emergence of direct and indirect recognition within NLR subfamilies, the regulation of NLRs by small RNAs, and the formation of NLR networks. Understanding the evolutionary history of NLRs can shed light on both the origin of pathogen recognition and the common constraints on the plant immune system. Attempts to engineer disease resistance have been sparse and rarely informed by evolutionary knowledge. In this review, we discuss the evolution of NLRs, give an overview of previous engineering attempts, and propose how to use evolutionary knowledge to advance future research in the generation of novel disease-recognition capabilities.

The promotive effect of auxin on shoot cell expansion provided the bioassay used to isolate this central plant hormone nearly a century ago. While the mechanisms underlying auxin perception and signaling to regulate transcription have largely been elucidated, how auxin controls cell expansion is only now attaining molecular-level definition. The good news is that the decades-old acid growth theory invoking plasma membrane H⁺-ATPase activation is still useful. The better news is that a mechanistic framework has emerged, wherein Small Auxin Up RNA (SAUR) proteins regulate protein phosphatases to control H⁺-ATPase activity. In this review, we focus on rapid auxin effects, their relationship to H⁺-ATPase activation and other transporters, and dependence on TIR1/AFB signaling. We also discuss how some observations, such as near-instantaneous effects on ion transport and root growth, do not fit into a single, comprehensive explanation of how auxin controls cell expansion, and where more research is warranted.

Crop loss due to soil salinization is an increasing threat to agriculture worldwide. This review provides an overview of cellular and physiological mechanisms in plant responses to salt. We place cellular responses in a time- and tissue-dependent context in order to link them to observed phases in growth rate that occur in response to stress. Recent advances in phenotyping can now functionally or genetically link cellular signaling responses, ion transport, water management, and gene expression to growth, development, and survival. Halophytes, which are naturally salt-tolerant plants, are highlighted as success stories to learn from. We emphasize that (a) filling the major knowledge gaps in salt-induced signaling pathways, (b) increasing the spatial and temporal resolution of our knowledge of salt stress responses, (c) discovering and considering crop-specific responses, and (d) including halophytes in our comparative studies are all essential in order to take our approaches to increasing crop yields in saline soils to the next level.

Desiccation of plants is often lethal but is tolerated by the majority of seeds and by vegetative tissues of only a small number of land plants. Desiccation tolerance is an ancient trait, lost from vegetative tissues following the appearance of tracheids but reappearing in several lineages when selection pressures favored its evolution. Cells of all desiccation-tolerant plants and seeds must possess a core set of mechanisms to protect them from desiccation- and rehydration-induced damage. This review explores how desiccation generates cell damage and how tolerant cells assuage the complex array of mechanical, structural, metabolic, and chemical stresses and survive.Likewise, the stress of rehydration requires appropriate mitigating cellular responses. We also explore what comparative genomics, both structural and responsive, have added to our understanding of cellular protection mechanisms induced by desiccation, and how vegetative desiccation tolerance circumvents destructive, stress-induced cell senescence.

Although cyanobacteria and algae represent a small fraction of the biomass of all primary producers, their photosynthetic activity accounts for roughly half of the daily CO2 fixation that occurs on Earth. These microorganisms are able to accomplish this feat by enhancing the activity of the CO2-fixing enzyme Rubisco using biophysical CO2 concentrating mechanisms (CCMs). Biophysical CCMs operate by concentrating bicarbonate and converting it into CO2 in a compartment that houses Rubisco (in contrast with other CCMs that concentrate CO2 via an organic intermediate, such as malate in the case of C4 CCMs). This activity provides Rubisco with a high concentration of its substrate, thereby increasing its reaction rate. The genetic engineering of a biophysical CCM into land plants is being pursued as a strategy to increase crop yields. This review focuses on the progress toward understanding the molecular components of cyanobacterial and algal CCMs, as well as recent advances toward engineering these components into land plants.

Pollination is the transfer of pollen grains from the stamens to the stigma, an essential requirement of sexual reproduction in flowering plants. Cross-pollination increases genetic diversity and is favored by selection in the majority of situations. Flowering plants have evolved a wide variety of traits that influence pollination success, including those involved in optimization of self-pollination, attraction of animal pollinators, and the effective use of wind pollination. In this review we discuss our current understanding of the molecular basis of the development and production of these various traits. We conclude that recent integration of molecular developmental studies with population genetic approaches is improving our understanding of how selection acts on key floral traits in taxonomically diverse species, and that further work in nonmodel systems promises to provide exciting insights in the years to come.

Fertilization of flowering plants requires the organization of complex tasks, many of which become integrated by the female gametophyte (FG). The FG is a few-celled haploid structure that orchestrates division of labor to coordinate successful interaction with the sperm cells and their transport vehicle, the pollen tube. As reproductive outcome is directly coupled to evolutionary success, the underlying mechanisms are under robust molecular control, including integrity check and repair mechanisms. Here, we review progress on understanding the development and function of the FG, starting with the functional megaspore, which represents the haploid founder cell of the FG. We highlight recent achievements that have greatly advanced our understanding of pollen tube attraction strategies and the mechanisms that regulate plant hybridization and gamete fusion. In addition, we discuss novel insights into plant polyploidization strategies that expand current concepts on the evolution of flowering plants.

Rosaceae (the rose family) is an economically important family that includes species prized for high-value fruits and ornamentals. The family also exhibits diverse fruit types, including drupe (peach), pome (apple), drupetum (raspberry), and achenetum (strawberry). Phylogenetic analysis and ancestral fruit-type reconstruction suggest independent evolutionary paths of multiple fleshy fruit types from dry fruits. A recent whole genome duplication in the Maleae/Pyreae tribe (with apple, pear, hawthorn, and close relatives; referred to as Maleae here) may have contributed to the evolution of pome fruit. MADS-box genes, known to regulate floral organ identity, are emerging as important regulators of fruit development. The differential competence of floral organs to respond to fertilization signals may explain the different abilities of floral organs to form fleshy fruit. Future comparative genomics and functional studies in closely related Rosaceae species with distinct fruit types will test hypotheses and provide insights into mechanisms of fleshy fruit diversity. These efforts will be facilitated by the wealth of genome data and resources in Rosaceae.