The Plant Cell Focus Issue: Biomolecular Condensates

The September issue of The Plant Cell includes a focus on biomolecular condensates. Although the term “biomolecular condensates” is relatively new, it actually reflects a convergence and synthesis of several distinct threads of research. Biomolecular condensates span from “classic” membraneless organelles (e.g., nucleolus, pyrenoid) to small, transient functional condensates, some of which are only recently recognized. A lot of the advancements in our understanding come from new tools and imaging techniques that reveal condensate structures and functions, many of which are reviewed here. The collection provides a great overview of this coalescing discipline. Start with the editorial overview by Gutierrez-Beltran et al. (Summary by Mary Williams @PlantTeaching) Plant Cell 10.1093/plcell/koad182 Furthermore, there’s a not-to-miss webinar on September 13 featuring three authors whose work appears in the Focus Issue; register at https://plantae.org/plant-cell-webinar-biomolecular-condensates/.

Immature leaves are the dominant volatile-sensing organs of maize

It’s well established that damaged plant tissues emit volatile compounds that bolster defense responses in nearby plants, but how those neighbors sense these compounds has remained obscure. This new work by Wang et al. reveals some important clues. First, as the title indicates, immature leaves are much more responsive to damage-associated volatiles (the authors specifically use (Z)-3-hexenyl acetate, HAC, as a proxy in many of their studies).  This is a volatile-specific developmental effect; older leaves remain sensitive and responsive to non-volatile defense cues such as the peptide ZmPep3. The authors also investigated factors that might affect volatile perception, looking at both stomatal aperture and the epidermal cuticle as possible variables. Interestingly, changing neither appears to affect volatile perception.  The authors speculate that factors involved in HAC perception or early stages of the signal transduction pathway might be preferentially expressed in young leaves, and suggest that, as young leaves are present at the outer periphery, the plant might benefit from focusing its perception in these regions (an analogy is drawn to the heightened environmental sensitivity of the root tip). Or, the plant might preferentially protect its young leaves by providing them with heightened sensitivity. Finally, the authors observe that knowing about this developmental pattern of sensitivity can provide an opportunity to finally identify the specific receptors for these volatiles. (Summary by Mary Williams @PlantTeaching) Curr. Biol. 10.1016/j.cub.2023.07.045

Genetic architecture of heterostyly and domestication history of common buckwheat

Common buckwheat (Fagopyrum esculentum) is a self-incompatible orphan crop which is gaining interest as it can be grown worldwide and grows well in low fertility soil. However, there are limited genomic resources available for common buckwheat. Here Fawcett et al. combined Illumnia short-read data with PacBio HiFi long-read data to produce a 1.27 Gb chromosome-level assembly of common buckwheat with over 30,000 annotated gene models. Surprisingly, 76% (960 Mb) of the genome was transposable elements, with the majority being Gypsy-type retrotransposons. Fluorescence in situ hybridization showed many Gypsy– retrotransposons at the centromeres, likely to have evolved after common buckwheat diverged from the closely related orphan crop tartary buckwheat (F. tataricum). The reference genome revealed many other interesting loci. The authors highlight a hemizygous gene S-ELF which is involved in heterostyly, a phenomenon where common buckwheat has two flower morphs each of which is self-incompatible, so both are required for reproduction. Knocking out S-ELF led to self-compatible flowers, suggesting a role for S-ELF in female compatibility and determining style length. The authors also used their reference genome to identify two endosperm-expressed copies of the starch synthesis gene Granule-Bound Starch Synthase (GBSS), most likely generated due to whole genome duplication during common buckwheat evolution. EMS-mutagenesis was used to knock out both GBSS paralogs and the double homozygous mutant had a waxy phenotype, which is the first example of waxy common buckwheat. These knockout gbss alleles are currently being introduced into elite common buckwheat varieties, demonstrating how the reference genome produced here can aid breeding. (Summary by Rose McNully @Rose_McN) Nature Plants 10.1038/s41477-023-01474-1

Water fluxes contribute to growth patterning in shoot meristems

The shoot apical meristem (SAM) is a wonderous thing. How this tiny clump of cells generates the entire above-ground organ system regularly, predictably, and dynamically is a question that has been investigated for decades, with models incorporating cascades regulatory genes, diffusible peptides, hormone fluxes, cell wall properties, cytoskeletal patterns, and more. In this new preprint by Alonso-Serra et al., water fluxes are introduced as contributors to growth patterning. The authors used timelapse imaging to create a 3D cell volume map of the growing meristem, followed by imaging of a fluorescent dye that mimics water movement. They found that cells in the boundary layer (the fold between the meristem and the emerging primordium) actually shrink in the absence of cell division, while adjacent cells expand, consistent with water movement between cells. Their model predicts that the rapid expansion of the growing cells leads to a decrease in their hydrostatic pressure, creating a sink that draws water from neighboring cells. As the authors conclude, these findings “make water a patterning factor at the shoot apex acting in synergy with mechanical and biochemical cues.” (Summary by Mary Williams @PlantTeaching) bioRiv 10.1101/2023.08.27.554993

LysM-mediated signaling in Marchantia polymorpha and conservation of PTI in land plants

Marchantia polymorpha, the common (but adorable) liverwort, has earned its spot in the ranks of very important plant model systems, joining Physcomitrium patens as representatives of the bryophyte clade. Many systems first characterized in Arabidopsis and other angiosperms are now being studied in these plants, providing much-needed insights into their evolutionary origins and trajectories. Here, Yotsui and colleagues show evidence for functional LysM (Lysin-motif) receptors in M. polymorpha. LysM receptors recognize peptidoglycans and chitins, cell wall components of bacteria and fungi, and can recognize both pathogens and symbiotic organisms. Previous studies showed that M. polymorpha recognized bacterial and fungal cell wall extracts; this new work demonstrates that it does this through LysM receptors. Furthermore, disruption mutants of some LysM-encoding genes showed decreased responses to chitin and peptidoglycans. The authors also identified signaling components downstream of LysM through phosphoproteomic approaches. Interestingly, the found that the blue-light receptor phototropin appears to be a negative regulator of LysM-mediated defenses.  (Summary by Mary Williams @PlantTeaching) Curr. Biol. 10.1016/j.cub.2023.07.068

Plant Science Research Weekly: Sept. 8, 2023

Review: Red macroalgae in the genomic era

I highly recommend this excellent and accessible article by Borg et al. that provides an overview of the red macroalgae, which “may have been the first eukaryotic lineage to have evolved complex multicellularity”. It’s full of fascinating information: although 97% of red algal species are marine, one lives in sloth hairs, and nori (sushi seaweed) is made from red algae (Porphyra and Pyropia genera). This article also gives an excellent and fascinating overview of red algal cell biology; from their unique cell wall polysaccharides that provide them with strength and elasticity (and us with agarose) to their unusual and highly efficient light-harvesting antennae (phycobilisomes) and their lack of plasmodesmata. There’s a tremendous diversity and variation in the reproductive biology of the red algae spanning from triphasic life cycles to the presence of trichogynes that receive the male nucleus for fertilization; interestingly, the authors point out that this great diversity offers the opportunity to explore questions about the evolutionary and ecological importance of sex. As the title suggests, genomic tools and the emergence of some model species are now shedding further light on these fascinating and important organisms. Summary by Mary Williams @PlantTeaching) New Phytol. https://doi.org/10.1111/nph.19211

Review: How plant roots respond to waterlogging

As the hottest year on record, 2023 has truly been a global annus horribilis during which humans, other animals, and domesticated and wild plants have faced unprecedented environmental challenges. In the past month alone, torrential rainfalls have wreaked havoc in Asia, the Middle East, and many parts of Africa, Europe, and the Americas. Frightenedly, disruptive flooding is expected to get worse, adding to food security concerns. Therefore, it’s timely to read about how plants respond to waterlogging in the new review by Daniel and Hartman. The main challenge in waterlogging is hypoxia, oxygen deprivation. The plant senses its waterlogged state through both hypoxia and an accumulation of ethylene, which is not able to diffuse away under water. Some plants have adaptations that enable them to tolerate at least some waterlogging, such as aerenchyma (air channels in roots), the ability to enter a quiescent state, or rapid elongation to reach above the water level. However, for non-adapted plants, even short periods can be lethal. The review covers plant responses from sensing, metabolic changes, and growth responses including changes to root system architecture and gravitropic setpoints (plants are amazing). It also discusses the very important question of translating from simple experimental systems (e.g., Arabidopsis on Petri plates) to real-world conditions, and makes the plea for moving towards “less artificial” experimental conditions. (Summary by Mary Williams @PlantTeaching) J. Exp. Bot. 10.1093/jxb/erad332

Plant Physiology Focus Issue: Plant Cell Polarity

The September issue of Plant Physiology has a focus on plant cell polarity, which plays a pivotal role in the fundamental processes that dictate plant growth, development, and adaptation. By establishing distinct regions within cells, plant cell polarity is crucial for regulating asymmetric cell divisions, guiding the direction of cell expansion, and determining the spatial distribution of essential cellular components. Understanding the mechanisms and regulatory pathways involved in plant cell polarity holds immense promise for enhancing crop productivity, optimizing plant responses to changing environments, and ultimately contributing to sustainable agriculture and ecological resilience. Don’t miss the editorial overview by Dong et al., and keep your eyes open for the registration link for a Focus Issue webinar to be held Sept. 25.  (Summary by Mary Williams @PlantTeaching) Plant Physiol. 10.1093/plphys/kiad436.

The Plant Cell Focus Issue: Biomolecular Condensates

The September issue of The Plant Cell includes a focus on biomolecular condensates. Although the term “biomolecular condensates” is relatively new, it actually reflects a convergence and synthesis of several distinct threads of research. Biomolecular condensates span from “classic” membraneless organelles (e.g., nucleolus, pyrenoid) to small, transient functional condensates, some of which are only recently recognized. A lot of the advancements in our understanding come from new tools and imaging techniques that reveal condensate structures and functions, many of which are reviewed here. The collection provides a great overview of this coalescing discipline. Start with the editorial overview by Gutierrez-Beltran et al. (Summary by Mary Williams @PlantTeaching) Plant Cell 10.1093/plcell/koad182 Furthermore, there’s a not-to-miss webinar on September 13 featuring three authors whose work appears in the Focus Issue; register at https://plantae.org/plant-cell-webinar-biomolecular-condensates/.

Immature leaves are the dominant volatile-sensing organs of maize

It’s well established that damaged plant tissues emit volatile compounds that bolster defense responses in nearby plants, but how those neighbors sense these compounds has remained obscure. This new work by Wang et al. reveals some important clues. First, as the title indicates, immature leaves are much more responsive to damage-associated volatiles (the authors specifically use (Z)-3-hexenyl acetate, HAC, as a proxy in many of their studies).  This is a volatile-specific developmental effect; older leaves remain sensitive and responsive to non-volatile defense cues such as the peptide ZmPep3. The authors also investigated factors that might affect volatile perception, looking at both stomatal aperture and the epidermal cuticle as possible variables. Interestingly, changing neither appears to affect volatile perception.  The authors speculate that factors involved in HAC perception or early stages of the signal transduction pathway might be preferentially expressed in young leaves, and suggest that, as young leaves are present at the outer periphery, the plant might benefit from focusing its perception in these regions (an analogy is drawn to the heightened environmental sensitivity of the root tip). Or, the plant might preferentially protect its young leaves by providing them with heightened sensitivity. Finally, the authors observe that knowing about this developmental pattern of sensitivity can provide an opportunity to finally identify the specific receptors for these volatiles. (Summary by Mary Williams @PlantTeaching) Curr. Biol. 10.1016/j.cub.2023.07.045

Genome sequencing reveals the genetic architecture of heterostyly and domestication history of common buckwheat

Common buckwheat (Fagopyrum esculentum) is a self-incompatible orphan crop which is gaining interest as it can be grown worldwide and grows well in low fertility soil. However, there are limited genomic resources available for common buckwheat. Here Fawcett et al. combined Illumnia short-read data with PacBio HiFi long-read data to produce a 1.27 Gb chromosome-level assembly of common buckwheat with over 30,000 annotated gene models. Surprisingly, 76% (960 Mb) of the genome was transposable elements, with the majority being Gypsy-type retrotransposons. Fluorescence in situ hybridization showed many Gypsy– retrotransposons at the centromeres, likely to have evolved after common buckwheat diverged from the closely related orphan crop tartary buckwheat (F. tataricum). The reference genome revealed many other interesting loci. The authors highlight a hemizygous gene S-ELF which is involved in heterostyly, a phenomenon where common buckwheat has two flower morphs each of which is self-incompatible, so both are required for reproduction. Knocking out S-ELF led to self-compatible flowers, suggesting a role for S-ELF in female compatibility and determining style length. The authors also used their reference genome to identify two endosperm-expressed copies of the starch synthesis gene Granule-Bound Starch Synthase (GBSS), most likely generated due to whole genome duplication during common buckwheat evolution. EMS-mutagenesis was used to knock out both GBSS paralogs and the double homozygous mutant had a waxy phenotype, which is the first example of waxy common buckwheat. These knockout gbss alleles are currently being introduced into elite common buckwheat varieties, demonstrating how the reference genome produced here can aid breeding. (Summary by Rose McNully @Rose_McN) Nature Plants 10.1038/s41477-023-01474-1

Water fluxes contribute to growth patterning in shoot meristems

The shoot apical meristem (SAM) is a wonderous thing. How this tiny clump of cells generates the entire above-ground organ system regularly, predictably, and dynamically is a question that has been investigated for decades, with models incorporating cascades regulatory genes, diffusible peptides, hormone fluxes, cell wall properties, cytoskeletal patterns, and more. In this new preprint by Alonso-Serra et al., water fluxes are introduced as contributors to growth patterning. The authors used timelapse imaging to create a 3D cell volume map of the growing meristem, followed by imaging of a fluorescent dye that mimics water movement. They found that cells in the boundary layer (the fold between the meristem and the emerging primordium) actually shrink in the absence of cell division, while adjacent cells expand, consistent with water movement between cells. Their model predicts that the rapid expansion of the growing cells leads to a decrease in their hydrostatic pressure, creating a sink that draws water from neighboring cells. As the authors conclude, these findings “make water a patterning factor at the shoot apex acting in synergy with mechanical and biochemical cues.” (Summary by Mary Williams @PlantTeaching) bioRiv 10.1101/2023.08.27.554993

LysM-mediated signaling in Marchantia polymorpha highlights the conservation of pattern-triggered immunity in land plants

Marchantia polymorpha, the common (but adorable) liverwort, has earned its spot in the ranks of very important plant model systems, joining Physcomitrium patens as representatives of the bryophyte clade. Many systems first characterized in Arabidopsis and other angiosperms are now being studied in these plants, providing much-needed insights into their evolutionary origins and trajectories. Here, Yotsui and colleagues show evidence for functional LysM (Lysin-motif) receptors in M. polymorpha. LysM receptors recognize peptidoglycans and chitins, cell wall components of bacteria and fungi, and can recognize both pathogens and symbiotic organisms. Previous studies showed that M. polymorpha recognized bacterial and fungal cell wall extracts; this new work demonstrates that it does this through LysM receptors. Furthermore, disruption mutants of some LysM-encoding genes showed decreased responses to chitin and peptidoglycans. The authors also identified signaling components downstream of LysM through phosphoproteomic approaches. Interestingly, the found that the blue-light receptor phototropin appears to be a negative regulator of LysM-mediated defenses.  (Summary by Mary Williams @PlantTeaching) Curr. Biol. 10.1016/j.cub.2023.07.068

Blue light, PAS/LOV photoreceptor and GDP-L-galactose phosphorylase (GGP): the Triumvirate controlling ascorbic acid biosynthesis in plants

Bournonville et al. explore which factors control ascorbic acid biosynthesis in plants and its accumulation in fruits.

https://doi.org/10.1093/plcell/koad108

Céline Bournonville, Bayer SAS, 1050 Route de Pardies, 40300 Peyrehorade, France

Kentaro Mori, Université Bordeaux, INRAE, UMR Biologie du Fruit et Pathologie, 33883 Villenave d’Ornon, France.

Pierre Baldet, Université Bordeaux, INRAE, UMR Biologie du Fruit et Pathologie, 33883 Villenave d’Ornon, France.

Background: Ascorbic acid, also known as vitamin C, is an essential antioxidant with key roles in several stress responses in living organisms. Since humans are not able to produce this molecule, we must obtain it through our diet, with plant products being the main source. Although the plant biosynthetic pathway of ascorbic acid is well known, the molecular mechanisms that regulate it are not yet understood. Among these regulatory factors, light occupies an important place, since it is vital for plants and it is well established that the more light there is, the more ascorbic acid plants produce and vice versa. However, the underlying mechanisms remain totally unknown.

Question: What are the factors that control ascorbic acid biosynthesis in plants and more particularly its accumulation in fruits?

Findings: Our work uncovers the mechanism by which plants use blue light to modulate ascorbate biosynthesis. From a tomato mutant, we identified a photoreceptor named PAS/LOV (PLP) and revealed that it functions as a negative regulator in vivo and in vitro by interacting with the GDP-galactose phosphorylase (GGP), which is known to be the most controlling enzyme of the pathway. We also demonstrated that blue light counteracts the inhibition of the GDP-galactose phosphorylase by the PAS/LOV photoreceptor. This is a major finding because it finally explains how plants protect themselves from too much light by synthesizing more of their main antioxidant.

Next steps: Future research should study the turnover of GGP in relation to PLP, particularly to better understand the adaptive role of PLP. Such research would open up new ways for developing plants that are more resistant to stress, fruits with prolonged “shelf-life”, and even plants with enhanced nutritional profiles.

Reference:

Céline Bournonville, Kentaro Mori, Paul Deslous, Guillaume Decros, Tim Blomeier, Jean-Philippe Mauxion, Joana Jorly, Stéphanie Gadin, Cédric Cassan, Mickael Maucourt, Daniel Just, Cécile Brès, Christophe Rothan, Carine Ferrand, Lucie Fernandez-Lochu, Laure Bataille, Kenji Miura, Laure Beven, Matias D. Zurbriggen, Pierre Pétriacq, Yves Gibon and Pierre Baldet. (2023). Blue light promotes ascorbate synthesis by deactivating the PAS/LOV photoreceptor that inhibits GDP-L-galactose phosphorylase. https://doi.org/10.1093/plcell/koad108

PRC1 shapes local and long-range interactions in the Arabidopsis genome

Yin, Romero-Campero, Yang, et al. identify CDs in the Arabidopsis genome and investigate the role of PRC1 in 3D structure.

Xiaochang Yin1, Francisco J. Romero-Campero2 3, Minqi Yang1, Myriam Calonje2, Yue Zhou1

1State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking University, 100871, Beijing, China.

2Institute of Plant Biochemistry and Photosynthesis (IBVF-CSIC), Avenida Américo Vespucio 49, 41092, Seville, Spain.

3Department of Computer Science and Artificial Intelligence (University of Sevilla), Avenida Reina Mercedes s/n 41012, Seville, Spain.

Background: How chromatin is organized in three dimensions (3D) within the nucleus has been proposed to be important for controlling biological processes. Post-translational histone modifications within chromatin, such as those mediated by the Polycomb Group machinery, seem to be involved in shaping this 3D organization, but their exact role is not clear. Recent studies have shown that the genome of animals and many plant species is partitioned into blocks of chromatin that self-interact. These topologically associating domains (TADs) or compartment domains (CDs) are usually enriched in specific histone modifications. Although Arabidopsis (Arabidopsis thaliana) chromatin is also decorated with histone modifications such as histone H2A monoubiquitination on lysine 121 (H2AK121ub), TADs or CDs have not been detected.

Question: What is the role of Polycomb Repressive complex 1 (PRC1)–mediated H2AK121ub in Arabidopsis 3D chromatin organization? Are TADs or CDs really absent in Arabidopsis?

Findings: Our results showed that TADs or CDs are present in the Arabidopsis genome. We identified CDs dominated by specific histone marks, like trimethylation of histone H3 on lysine 27 (H3K27me3), which is mediated by Polycomb Repressive Complex 2 (PRC2), H3K27me1 or H3K4me3. Interestingly, PRC1 mediated H2AK121ub could be found in combination with other modifications, displaying different roles. We found that H2AK121ub acting together with H3K27me3 is required to maintain the interactions inside H3K27me3 enriched CDs. In addition, PRC1 and H2AK121ub when acting independently of PRC2 prevent the formation of chromatin loops marked with H3K4me3. Likewise, we found that PRC1 affects interactions between distant CDs, participating in a higher order of chromatin organization. Our results reveal a versatile role of PRC1 activity in shaping 3D chromatin configuration in Arabidopsis.

Next steps: An interesting path to continue our findings would be to explore whether the 3D interactions observed to be dependent on PRC1 are key in defining the 3D structure genome associated with developmental phase transitions and environmental responses.

Reference:

Xiaochang Yin, Francisco J. Romero-Campero, Minqi Yang, Fernando Baile, Yuxin Cao, Jiayue Shu, Lingxiao Luo, Dingyue Wang, Shang Sun, Peng Yan, Zhiyun Gong, Xiaorong Mo, Genji Qin, Myriam Calonje, Yue Zhou. (2023). Binding by the Polycomb complex component BMI1 and H2A monoubiquitination shape local and long-range interactions in the Arabidopsis genome. https://doi.org/10.1093/plcell/koad112

Perspective: How flower development genes were identified using forward genetic screens in Arabidopsis

If you weren’t around in the ’80s, you missed some great times; the music, the fashion, the flower genetics! This historical perspective article by David Smythe nicely sums up those heady days with an account of how Arabidopsis thaliana blasted into the ranks of a top model organism, in part through the uncovering of genes controlling flower development. The article describes the steps that occurred in order for these genes to be found and the models of floral development revealed, from chemical mutagenesis of dry seeds, phenotypic screening, backcrossing, and double-mutant analysis. Beyond floral organ identity, these approaches also revealed now-familiar genes involved in auxin transport and meristem maintenance and identity. (Summary by Mary Williams @PlantTeaching) Genetics 10.1093/genetics/iyad102