The ”hourglass” model of embryogenesis extends to brown algae

The hourglass model of embryogenesis was proposed in the 1990s, and extended to green plants and fungi in the 2010s. During animal embryogenesis, the very earliest stages (post fertilization) are morphologically quite different from each other, and the later stages are quite different, but in the middle of embryogenesis there is a period, called the phylotypic period, at which the appearance of animal embryos converge and look quite similar. This pattern of morphological diversity resembles the shape of an hourglass, broad at the top and bottom and narrow in the middle. The phylotypic period is the period during which the basic body plan of the organism is established. Interestingly, during the phylotypic period, there is also a narrowing of patterns of gene expression, and a shift toward the expression of evolutionarily older, more highly conserved genes. In a new paper, Lotharukpong et al. found evidence for this hourglass model of development in another type of multicellular organism, the brown algae, which became multicellular independently of plants, fungi and animals. The study found that during the phylotypic period when the algal body plan was being established, younger genes were expressed less, rather than older genes being expressed more, and the more ancient genes expressed during this stage are also more pleiotropically expressed than younger genes, consistent with findings from animals and plants. (Summary by Mary Williams @PlantTeaching) Nature 10.1038/s41586-024-08059-8

Single-plant omics provides transcriptional insights into the transition from the vegetative to reproductive phases

Plants undergo a series of physiological processes when transitioning from the juvenile to the vegetative phase, and then vegetative to the reproductive phase. RNA-Seq offers substantial potential for uncovering the transcriptional landscape underlying these developmental transitions. However, developmental asynchrony among individual plants within a population creates variations in the spatiotemporal expression of genes. Redmond et al. performed a single-plant-omics study on a large population of Arabidopsis thaliana and their investigation revealed the detailed sequence of transcriptional events that occur before and after the bolting transition. Using single-plant-omics allowed the researchers to order individual plants by their intrinsic biological age, providing a high-resolution transcriptional landscape. They trained different models to test whether these models are more or less informative compared to gene expression data. Results revealed that most of the differentially expressed genes were closely linked with the traits of biomass and leaf area. Implication of the pseudotime inference algorithm revealed certain senescence-related traits e.g., transcriptional repression of ribosome biosynthesis followed by photosynthesis shutdown is a major event that serves as a landmark when a bolting plant changes from vegetative to reproductive phase. Their study highlights the role of environmental asynchrony and opens new avenues to use single-plant-omics in synthetic biology and molecular breeding programs. (Summary by Asif Ali @pbgasifkalas) Plant Cell. 10.1093/plcell/koae226

Phloem loading and subcellular transport drive carbon storage in cassava roots

Cassava (Manihot esculenta) is a vital starchy crop essential for food security in Sub-Saharan Africa, South America, and Southeast Asia. A recent study on cassava by Rüscher et al. provides important insights into the plant’s sugar control mechanisms as the roots expand, produce large amounts of storage parenchyma, and accumulate sugars and starch, a process known as root bulking. The authors examined how carbohydrates are transported into the roots and found that both the absence of upregulation of specific transporters and the presence of branched plasmodesmata support a model of passive symplastic phloem loading. They also found evidence of subcellular compartmentalization of sugars in the storage root during bulking. As sugar levels build in the cytosol, monosaccharide transporter genes that import sugars into the vacuole were more highly expressed, leading to vacuoles in storage roots containing up to 7.5% sucrose by dry weight. The accumulation of sugars establishes an osmotic gradient that attracts water into the vacuoles, resulting in the enlargement of root cells and potentially affecting the plant’s ability to regulate internal water resources. By understanding the dynamics of sugar compartmentation, gene expression, and transport patterns, the study highlights an immense opportunity for cassava breeding projects. (Summary by Tuyelee Das @das_tuyelee) Plant Phys. 10.1093/plphys/kiae298

Plant Science Research Weekly: November 1, 2024

Spotlight: The role of fossils for reconstructing the evolution of plant development

I suspect if we asked someone to describe a fossil we’d hear a lot about dinosaur bones. Certainly, science museums are full of fossilized animal remains, which have greatly informed our understanding of animal evolution. Plant fossils similarly are rich sources of information about plant evolution and evolutionary development (evo-devo), as highlighted here by Hetherington. The author starts with an observation that reconstructing evolution using only extant species misses out on all the stages that have become extinct, so can miss key forms and events (imagine trying to understand where birds came from without knowing about dinosaurs). He notes that piecing together plant evo-devo is challenging because most of the major innovations in plant form occurred 350 million years ago, well before the time when most terrestrial animals were around. He also makes the important point that if we only studied living plants, we would assume that leaves and roots each arise a single time, yet when we add in information from the fossil record it is apparent that the arose at least twice. This is a fascinating Spotlight article certainly worth sharing with students. (Summary by Mary Williams @PlantTeaching) Development 10.1242/dev.204322

Perspective: Enzymatic routes to designer hemicelluloses for use in biobased materials

This article poses the interesting question of whether we can use our knowledge of plant cell wall-modifying, carbohydrate-active enzymes to produce biobased materials. Specifically, the authors point out that much of the hemicellulose contained in agricultural and wood fiber could provide a starting point for making useful products such as aerogels, films, and coatings. Compared to common chemical processes, enzymes can be both more specific about what is produced, and greener in terms of waste. This Perspective article gives a comprehensive review of the substrates and products of many different characterized enzymes (a good review for those interested) and also proposes steps to overcome some of the challenges inherent in creating designer hemicelluloses. For example, the authors propose screening enzymes for application rather than function, e.g., by measuring changes in sample viscosity or light-scattering, and they call for more collaboration between enzymologists and materials scientists. (Summary by Mary Williams @PlantTeaching) JACS Au 10.1021/jacsau.4c00469

Review: Cracking the plant VOC sensing code and its practical applications

Many studies have demonstrated the importance of volatile organic compounds (VOCs) in communication between plants. VOCs emitted by a plant damaged by herbivory promote defenses in nearby plants. It is thought that these compounds may have originated as intra-plant signals, capable of moving long-distances faster than signals through the plant vascular system, with the inter-plant signaling function a fortuitous consequence. Notably, plants respond to signals produced by both conspecific and heterospecific individuals. A new review by Arimura and Uemura looks at these signals, reviewing their diverse functions but also highlighting what is known and not known about how they are perceived and elicit responses. Whether VOCs interact with specific plasma membrane-localized receptors (by analogy to animal olfactory system) remains an open question, and there is also some evidence that certain VOCs interact with proteins intracellularly. Some VOCs interact with the TOPLESS corepressor which may lead to changed in transcription and also chromatin remodeling. The review concludes with a discussion about how these insights might be used for protection of crop and horticultural plants, for example by the use of VOC-producing companion plants or synthetic VOCs. (Summary by Mary Williams @PlantTeaching) Trends Plant Sci 10.1016/j.tplants.2024.09.005

Review. Decoding resilience: Ecology, regulation, and evolution of biosynthetic gene clusters

Although clusters of functionally related genes are common in prokaryotes, until recently it was thought that they were not a feature of eukaryotic genomes. However, several studies have identified biosynthetic gene clusters (BGCs) in plants. Many of these gene clusters include sets of enzymes that act sequentially in the production of specialized metabolites, such as defense or signaling molecules, enabling rapid and cost-effective production of the compound. A new review by Cawood and Ton discusses the function and regulation of these BGCs and speculates on how they are formed. Unlike prokaryotes, which have polycistronic BGCs (with many proteins encoded by a single mRNA), BGCs in eukaryotes are monocistronic, yet closely co-regulated, raising the question of how.  Many studies suggest a role for histone modifications and histone variants (e.g., H2A.Z) in BGC co-regulation. There is also evidence for 3D chromatin topology and the formation of topologically associated domains (TADs) in BGC regulation. For example, in one case a chromatin loop structure leads to five BGC promoters simultaneously interacting with transcription factors and coactivators. Finally, the review turns to the question of how these BGCs were formed. It is generally assumed that they are derived from gene duplication and neofunctionalization, but the details of how this took place are not known. The authors describe a model in which stress induces activation of transposable elements, leading to gene duplication, exon shuffling, and gene fusion, providing opportunities for neofunctionalization. The authors also postulate that topologically associated domains could lead to related genes repositioning into BGCs. Finally, they note that in addition to positive selection of functional BGCs, there can be negative selection against incomplete BGCs due to the accumulation of potentially harmful metabolites.  (Summary by Mary Williams @PlantTeaching) Trends Plant Sci 10.1016/j.tplants.2024.09.008

PCMD: an interactive library for comparative metabolomics studies

Albert Einstein once said, “The only thing that you absolutely have to know is the location of the library.” Libraries house vast troves of information for readers to explore, analyze, and use. With the exponential increase in data, libraries have also evolved into digital databases and online platforms. For example, large-scale omics studies yield tremendous amounts of data on genes, proteins, and metabolites that can help us understand plant development, provided they are accessible to researchers. In a recent issue of Plant Communications, Hu and colleagues introduced the Plant Comparative Metabolome Database (PCMD; https://yanglab.hzau.edu.cn/PCMD) for comparative metabolomics. Built on genome-based predictions of metabolites and associated metabolic pathways, along with supporting experimental data, PCMD provides metabolic profiles for 530 plant species. It offers unique features such as metabolite enrichment determination for cross-species comparative analysis, setting it apart from other databases. Each metabolite entry also includes data on associated proteins, metabolic reactions, and relevant literature, and links to databases like PubChem and MetaCyc. Future updates include tools for uploading experimental data and visualizing metabolic networks to deepen studies of gene-metabolite relationships. In conclusion, like a library, PCMD provides researchers interested in comparative metabolomics with a robust starting point for exploring metabolites, metabolic profiles, and the evolution of metabolic networks and can even support biotechnological research focused on plant-derived compounds for pharmaceutical or therapeutic applications. (Summary by Thomas Depaepe @thdpaepe) Plant Communications 10.1016/j.xplc.2024.101038.

The ”hourglass” model of embryogenesis extends to brown algae

The hourglass model of embryogenesis was proposed in the 1990s, and extended to green plants and fungi in the 2010s. During animal embryogenesis, the very earliest stages (post fertilization) are morphologically quite different from each other, and the later stages are quite different, but in the middle of embryogenesis there is a period, called the phylotypic period, at which the appearance of animal embryos converge and look quite similar. This pattern of morphological diversity resembles the shape of an hourglass, broad at the top and bottom and narrow in the middle. The phylotypic period is the period during which the basic body plan of the organism is established. Interestingly, during the phylotypic period, there is also a narrowing of patterns of gene expression, and a shift toward the expression of evolutionarily older, more highly conserved genes. In a new paper, Lotharukpong et al. found evidence for this hourglass model of development in another type of multicellular organism, the brown algae, which became multicellular independently of plants, fungi and animals. The study found that during the phylotypic period when the algal body plan was being established, younger genes were expressed less, rather than older genes being expressed more, and the more ancient genes expressed during this stage are also more pleiotropically expressed than younger genes, consistent with findings from animals and plants. (Summary by Mary Williams @PlantTeaching) Nature 10.1038/s41586-024-08059-8

Single-plant omics provides transcriptional insights into the transition from the vegetative to reproductive phases

Plants undergo a series of physiological processes when transitioning from the juvenile to the vegetative phase, and then vegetative to the reproductive phase. RNA-Seq offers substantial potential for uncovering the transcriptional landscape underlying these developmental transitions. However, developmental asynchrony among individual plants within a population creates variations in the spatiotemporal expression of genes. Redmond et al. performed a single-plant-omics study on a large population of Arabidopsis thaliana and their investigation revealed the detailed sequence of transcriptional events that occur before and after the bolting transition. Using single-plant-omics allowed the researchers to order individual plants by their intrinsic biological age, providing a high-resolution transcriptional landscape. They trained different models to test whether these models are more or less informative compared to gene expression data. Results revealed that most of the differentially expressed genes were closely linked with the traits of biomass and leaf area. Implication of the pseudotime inference algorithm revealed certain senescence-related traits e.g., transcriptional repression of ribosome biosynthesis followed by photosynthesis shutdown is a major event that serves as a landmark when a bolting plant changes from vegetative to reproductive phase. Their study highlights the role of environmental asynchrony and opens new avenues to use single-plant-omics in synthetic biology and molecular breeding programs. (Summary by Asif Ali @pbgasifkalas) Plant Cell. 10.1093/plcell/koae226

Phloem loading and subcellular transport drive carbon storage in cassava roots

Cassava (Manihot esculenta) is a vital starchy crop essential for food security in Sub-Saharan Africa, South America, and Southeast Asia. A recent study on cassava by Rüscher et al. provides important insights into the plant’s sugar control mechanisms as the roots expand, produce large amounts of storage parenchyma, and accumulate sugars and starch, a process known as root bulking. The authors examined how carbohydrates are transported into the roots and found that both the absence of upregulation of specific transporters and the presence of branched plasmodesmata support a model of passive symplastic phloem loading. They also found evidence of subcellular compartmentalization of sugars in the storage root during bulking. As sugar levels build in the cytosol, monosaccharide transporter genes that import sugars into the vacuole were more highly expressed, leading to vacuoles in storage roots containing up to 7.5% sucrose by dry weight. The accumulation of sugars establishes an osmotic gradient that attracts water into the vacuoles, resulting in the enlargement of root cells and potentially affecting the plant’s ability to regulate internal water resources. By understanding the dynamics of sugar compartmentation, gene expression, and transport patterns, the study highlights an immense opportunity for cassava breeding projects. (Summary by Tuyelee Das @das_tuyelee) Plant Physiol. 10.1093/plphys/kiae298

Virtual issue: The chemical language of plant–microbe–microbe associations

Don’t miss this exciting Virtual Issue from New Phytologist on “plant-microbe-microbe” interactions. That’s not a typo – many of the articles address the signals that coordinate such multi-factorial interactions, as there is a growing recognition that interrelations between microbes influence how they interaction with plants (see also the review below by Mesny et al.). This Virtual issue centers the role of chemical signals, including hormones, metabolites, peptides, and volatile organic compounds (VOCs), in shaping plant-microbe-microbe outcomes. The editorial beautifully summarizes this exciting topic and introduces some of the key questions still being addressed. One of the articles I found particularly intriguing is “Listening to plant’s Esperanto via root exudates.” Esperanto is a constructed international language that was developed to foster communication between people of diverse origins, and I love thinking of plant exudates as a universal language that can be understood by all microbes. I also enjoyed the article exploring how “Microbial terroir” affects the flavor chemistry of mustard seed. Terroir is a term commonly used in winemaking that refers to how the environment in which a plant is grown influences its chemical composition and flavor. The potential applications of a better understanding plant-microbe-microbe interactions are vast, from optimizing or customizing flavor, to harnessing beneficial microbes in order to suppress disease-causing microbes, and beyond. (Summary by Mary Williams @PlantTeaching) New Phytologist. Editorial  10.1111/nph.20124.

Review. Microbial tug-of-war: How plants and pathogens manipulate microbiomes

The composition of plant-associated microbes is influenced by plant genetics, immune responses, environmental factors, and interactions between microbes. During disease development, the microbial community at infection sites changes due to tissue damage, altered immune responses, and manipulation via pathogen effector proteins. Mesny et al. argue that host-pathogen co-evolution involves not just the direct interaction between the two, but also the dynamics within the host’s microbiota. For example, effectors produced by fungal pathogens can have antimicrobial properties that suppress protective microbes, enhancing fungal pathogenicity.  On the other hand, foliar infections by fungal pathogens like Botrytis cinerea have been shown to stimulate beneficial microbes like Trichoderma harzianum at plant roots. This recruitment of beneficial microbes, termed the “cry-for-help” response, can have long-lasting effects on the soil microbiota, potentially leading to disease-suppressive soils that protect future crops. However, disease suppressiveness takes years to build up, possibly due to antimicrobial effector proteins secreted by pathogens, which slow down the recruitment of beneficial microbes. Future research should focus on understanding these mechanisms and their long- and short-term effects, leading to new approaches for sustainable disease management. (Summary by Kumanan N Govaichelvan, @NGKumanan) Curr. Opin. Plant Biol. 10.1016/j.pbi.2024.102622

PIN auxin transporters also transport auxin-like herbicides (and more?)

Auxin is an extremely important plant hormone that must be precisely controlled. Auxin-like herbicides have been developed that are often more stable than the natural auxins, thus their application can damage the plant. Here, Schulz, Ung et al. investigated how these auxin herbicides move in plant tissues. The authors investigated the interactions of the well-known PIN auxin transporters and various auxin herbicides, using several methods. Solid supported membrane (SSM) electrophysiology using liposomes as well as expression in oocytes allowed them to measure transport rate and binding affinities of the herbicides. They corroborated these results using cryo-EM, which allowed them to image direct interactions between the herbicides and the transporter proteins. They next generated a set of single residue variants and examined how these affected transport of the herbicides. Their results show that PIN proteins transport auxin herbicides in vivo and in vitro, shed light into the mechanisms of action of the PIN transporters, and open the door to the development of more-efficient herbicides and / or herbicide resistant plants. (Summary by Mary Williams @PlantTeaching) bioRxiv https://doi.org/10.1101/2024.08.29.610046. (Note that recently a human G-protein-coupled receptor was shown to have structural similarities to plant PIN transporters – maybe like auxin, PINs are everywhere  10.1038/s41586-024-08012-9).

Unveiling vacuole biogenesis: Tubular networks are present in plant meristem cells

A recent paper by Scheuring and colleagues investigates vacuole biogenesis in meristematic cells of Arabidopsis thaliana, challenging earlier models of vacuole formation. Vacuoles are crucial organelles responsible for various cellular functions, yet their formation has remained puzzling for quite some time. Historically, models have proposed that vacuoles are formed either by contributions from the endoplasmic reticulum (ER) or through homotypic fusion of multivesicular bodies (MVBs). However, recent evidence suggests a more complex process involving multiple membrane sources. The authors use advanced imaging techniques, such as super-resolution stimulated emission depletion (STED) microscopy and fluorescence recovery after photobleaching (FRAP), to confirm the presence of a tubular vacuolar network in meristematic plant cells. The authors introduced a RUBY vacuole reporter line (using betalain fluorescence) to image deeper into tissues, where conventional dyes might not penetrate. This tubular network, observed in young cells near the quiescent center of the root, appears interconnected, which contradicts the theory that MVBs alone are sufficient to form vacuoles. Their findings suggest instead that vacuolar membranes originate from various cellular sources, including the ER. The study further introduces a customized FRAP assay, termed vacuole-connectivity FRAP (vaccFRAP), to analyze vacuolar dynamics. This assay beautifully highlights different connectivity levels within the vacuolar network, providing insights into how vacuoles function as interconnected compartments even in early developmental stages. This research advances our understanding of vacuole formation and its role in plant cell development. (Summary by Ann-Kathrin Rößling @AK_Roessling) Plant Cell 10.1093/plcell/koae243

Decoding the signaling precision of receptor-MAPK pathways

Have you ever wondered how cells distinguish between the diverse array of external signals traveling through similar pathways? To understand the intricacies of plant signaling mechanisms, Ma et al. used single endodermal cells of Arabidopsis roots as a model to compare two receptor pathways. One pathway uses the immune receptor FLAGELLIN SENSING2 (FLS2) to detect microbial signals, while the other involves the SCHENGEN3 (SGN3) receptor, a key regulator of Casparian strip (CS) development in root endodermal cells. The authors used a combination of genetic, molecular, and biochemical approaches to demonstrate that the SGN3 pathway and the FLS2 pathway activate distinct groups of  mitogen-activated protein kinase kinases (MKKs). The study further showed that SGN3 stimulation enables CS domain fusion in endodermal cells through MYB36-mediated transcriptional responses, while MYB36 is not activated by the FLS2 pathway. Instead MKK4/5 is activated by FLS2 to facilitate enhanced lignin and suberin deposition. Moreover, FLS2 activates MKK7/9 which are negative regulators of CS development, thus suppressing SGN3-specific responses when this pathway is triggered. Thus, this study sheds light on the intricate complexities of plant signaling mechanisms through single cell analyses. (Summary by Abira Sahu @AbiraSahu) Nature Plants 10.1038/s41477-024-01768-y