Unforeseen plant diversity in global dryland

Earth’s terrestrial ecosystems harbor remarkable plant diversity. Some of this diversity can be quantified as functional traits, which provide a measure for diversity in different environments. In this new work, Gross et al. used a functional trait analysis to examine how plants respond to increasing aridity and animal grazing in global drylands, which are highly vulnerable to drivers of global change. The study analyzed 133,769 traits from 301 perennial plants across 98 sites in 25 countries. The findings break the widely accepted belief that extreme climatic conditions lead to a decline in the diversity of plant traits. On the contrary, it suggests that plants in arid regions use a wide variety of adaptation strategies, and this diversity increases with the degree of aridity. The authors describe this response to aridity as the “plant loneliness syndrome”.  Heavily grazed drylands also correspond to greater diversity in traits. The findings emphasize that factors like soil fertility and plant cover contribute to trait diversity in challenging environments. This study underscores the significance of drylands as a global reservoir of plant diversity and shows how plants can adapt to increasing environmental pressures and climate change through diverse strategies. (Summary by Maneesh Lingwan @LingwanManeesh) Nature 10.1038/s41586-024-07731-3

Plant memories: How people build lasting connections with plants

People often fail to recognize and appreciate the importance of plants, a phenomenon known as Plant Awareness Disparity (PAD), also known as plant blindness. This lack of awareness has a negative impact on botanical knowledge and skill acquisitions, consequently affecting biodiversity conservation efforts. McGinn et al. investigated the relationship between art and plant awareness through an exhibition, “In Memory of Plants,” at the Alternative Kilkenny Arts Festival 2022, using art as a tool to address PAD phenomenon. The study revealed the importance of art as a tool for reflection and emotional engagement to connect people to plants. Visitors at the exhibition were encouraged to share their personal plant-related memories, and plants were seen to link people to significant experiences and relationships. The analysis demonstrated the importance of sensory experiences in relating to plants, giving a deeper understanding of human-plant connections and buttressing art-based research as an effective tool to enhance plant awareness and stimulate collaboration among artists, botanists and science communicators. This study, therefore advocates for art as a vital instrument in addressing biodiversity loss and supporting plant conservation efforts. (Summary by Idowu Arinola Obisesan, @IdowuAobisesan) Plants People Planet 10.1002/ppp3.10555

Plant Science Research Weekly: August 23, 2024

Review. Chilling out: How plants remodel membranes to survive the cold

Low temperatures disrupt cellular processes and require metabolic adaptation. Cold-induced lipid remodeling helps maintain membrane permeability and prevents phase separations that can lead to cellular damage. In this review, Shomo, Li and colleagues provide an overview of the mechanisms by which plants remodel their membrane lipids to adapt to low temperatures and cold stress. They focus on glycerolipids, sphingolipids, and phytosterols. Additionally, they examine how cold stress affects membrane composition and functionality at the subcellular level, presenting current glycerolipidomic data from Arabidopsis thaliana, maize, and sorghum. This data highlights the consistency as well as the variability of lipid responses across species. The authors delve into the three main ways of lipid alteration. First is acyl editing and headgroup exchange, where plants modify their membrane lipids to maintain membrane integrity and function. The second way is regulating lipase activity, which plays a crucial role in lipid remodeling during cold stress. The third is changes in phytosterol abundance, where altering phytosterol levels help to stabilize membranes under cold conditions. The review points out recent advances and accomplishments in the field with an informative overview of observed lipid changes, and highlights gaps in current the knowledge and areas needing further investigation to fully understand and manipulate plant cold tolerance. Summary by Ann-Kathrin Rößling (@AK_Roessling) 10.1093/plphys/kiae382

Review: Defining and rewiring of gene regulatory networks for plant improvement

Much of the focus of functional genomics studies in plants is to improve yield, disease resistance, abiotic stress tolerance and nutritional quality. Many desirable traits are controlled by sets of genes that are coordinated in a complex network, called a gene regulatory network (GRN). A transcription factor (TF) binds to the promoter region of one or more genes and promotes or represses gene expression. In this review, Borowsky and Bailey-Serres discuss how defining the GRNs underlying desired traits can be used to fine-tune and further adjust them to meet the demands of climate change and food supply. Next-generation sequencing technologies coupled with omics studies made it possible to explore the gene circuitry and interacting proteins controlling favorable traits. The functions of most major genes are conserved among different species with much diversity attributed to TFs and cis-regulatory elements, which drive or alter the expression of target genes. For example, the function of the root TF SHORTROOT  is conserved, but its redeployment results in the addition of more cortical cells in maize compared to Arabidopsis. Similarly, the function of the bundle sheath TF DNA BINDING WITH ONE FINGER is conserved in photosynthesis, however, its downstream deployment regulates C3 genes in rice and C4 genes in sorghum. The authors present a set of examples of how synthetic biology and genome editing can be used to engineer desirable phenotypes in plants through rewiring gene circuitry. (Summary by Asif Ali @pbgasifkalas) Nat. Genet. 10.1038/s41588-024-01806-7

Review: Stem-borne roots as a framework to study trans-organogenesis

Plants develop new organs and tissues throughout their lifespan as they grow new leaves, roots and reproductive structures. Many of these tissues arise from similar tissues, such as lateral roots arising from primary roots, and the mechanisms guiding their formation are well understood. But what about ‘trans-organogenesis’: where structures arise from completely different tissue types? The development of roots from stems – also known as adventitious roots – is one such example. And while stem-borne roots have been described for many species, the mechanisms controlling their development remain elusive. In this review, Rasmussen et al. summarise the current knowledge on development of stem-borne roots, including their occurrence throughout the plant kingdom and diversity of form and function. They consider open questions of whether stem-borne roots share an evolutionary history, or have arisen multiple times, possibly through rewiring of ancient developmental pathways. The authors provide a framework to better classify types of stem-borne roots based on their form, function and tissue of origin – and propose stem-borne roots as a model for understanding trans-organogenesis, plasticity and adaptation in plants. (Summary by Alicia Quinn @AliciaQuinnSci). Curr. Opin. Plant Biol. 10.1016/j.pbi.2024.102604

Cytokinin signalling regulates auxin availability and wounding-induced adventitious rooting competency

Adventitious roots, i.e. those derived from non-root tissues, are key elements of the plastic architecture of root systems. Auxins and cytokinins are known to induce and inhibit (respectively) adventitious root formation, though the exact mechanism remains to be fully explained. Here, Damodaran and Strader investigated the role of local conversion of indole-3-butyric acid (IBA) into indole-3-acetic acid (IAA) – both forms of auxin – in adventitious rooting competency. Following wounding of the hypocotyl, adventitious roots form mainly near the excision site, indicating that not all hypocotyl cells are competent to make roots. IAA can be obtained locally from IBA via peroxisomal beta-oxidation, and mutants unable to make this conversion produce fewer adventitious roots than the wildtype. TRANSPORTER OF IBA 1 (TOB1) can limit the supply of IBA by sequestering it into the vacuole, and tob1 plants produced more adventitious roots than wildtype, further evidencing the role of IBA-to-IAA conversion in adventitious rooting competency. Additionally, tob1 hypocotyls were insensitive to the known inhibitory effects of cytokinin on adventitious rooting, possibly due to cytokinin control of TOB1 expression. These results contribute to a more mechanistic understanding of the long-established auxin-cytokinin interplay in adventitious rooting, which will be invaluable in the development of improved protocols for clonal propagation by cuttings. (Summary by John Vilasboa @vilasjohn) Dev. Cell.  10.1016/j.devcel.2024.06.019

Convergent evolution of plant prickles

Contrary to common belief, roses do not have thorns: instead, they have prickles. Thorns (as in hawthorns) are modified stems, spines (as in cactus spines) are modified leaves, and prickles (as in roses) are modified epidermal tissues. Prickles occur in a wide range of plants. Satterlee et al. set out to investigate the genetic basis for prickle formation, starting with a comparison between a prickleless cultivated eggplant (Solanum melongena) and its prickled wild relative (Solanum insanum). Interestingly, they identified a gene known to be involved in cytokinin biosynthesis, LONELY GUY (LOG), as critical for prickle formation. The authors looked across the Solanum genus and beyond and found that mutations in LOG are widely correlated with prickle loss. Furthermore, homologous prickle-like structures known as barbs in grasses are also dependent on a functional LOG gene, indicating that loss of prickles has occurred convergently. Finally, the authors used gene editing techniques to produce prickleless varieties without additional pleiotropic effects. (Summary by Mary Williams @PlantTeaching) Science 10.1126/science.ado1663

A kinase fusion protein from Aegilops longissima confers resistance to wheat powdery mildew

The obligate biotrophic pathogen Blumeria graminis f. sp. tritici (Bgt) is the cause of wheat powdery mildew, a foliar disease that results in significant yield loss in most wheat-growing regions across the globe. This research focuses on the identification and functional analysis of the powdery mildew resistance gene Pm13, which was introgressed into wheat from Aegilops longissima. The gene was identified through a comprehensive approach that revealed its critical role in conferring resistance to wheat powdery mildew. Pm13 encodes a unique fusion protein that combines elements typically associated with the regulation and signaling of cell death. The validation of Pm13 function, confirmed through various genetic assays, underscores its importance in enhancing disease resistance. Notably, a specific segment of the protein was shown to initiate cell death, highlighting the gene’s potential impact on improving wheat resilience through targeted breeding or genetic engineering. This discovery adds a valuable tool to the arsenal for combating powdery mildew in wheat. The findings also highlight the potential of wild relatives, such as Aegilops longissima, to enhance disease resistance in cultivated wheat. (Summary by Muhammad Aamir Khan @MAKNature1998) Nature 10.1038/s41467-024-50909-6

New kid on the plant block: Single-cell proteomics

While single-cell omics technologies, particularly transcriptomics, are already becoming widely adopted in plant science, quantifying proteins at single cell resolution is less established. Fortunately, important technological strides have been made that improve sample preparation, separation techniques, and overall sensitivity and resolution to make single cell proteomics (SCP) possible. Montes et al. have recently developed a multiplexed methodology for SCP specifically adapted to plant tissue, overcoming typical challenges associated with handling such samples. As a proof-of-concept, the authors compared proteins from two adjacent root cell layers, the endodermis and cortex, and observed their distinct proteomic signatures. The optimized SCP can successfully detect proteins associated with both low and high abundance transcripts, and even detects low abundant proteins like transcription factors, opening up tremendous possibilities to study plant signaling networks in neighboring cell types. As expected however, the varying cell sizes along the root led to considerable variation in protein quantification, an important consideration for improvement in future studies. In conclusion, this methodology offers a clear, comprehensive, and practical tool for scientists looking to explore the world of single-cell proteomics in plants. (Summary by Thomas Depaepe @thdpaepe). New Phytologist 10.1111/nph.19923

Unforeseen plant diversity in global dryland

Earth’s terrestrial ecosystems harbor remarkable plant diversity. Some of this diversity can be quantified as functional traits, which provide a measure for diversity in different environments. In this new work, Gross et al. used a functional trait analysis to examine how plants respond to increasing aridity and animal grazing in global drylands, which are highly vulnerable to drivers of global change. The study analyzed 133,769 traits from 301 perennial plants across 98 sites in 25 countries. The findings break the widely accepted belief that extreme climatic conditions lead to a decline in the diversity of plant traits. On the contrary, it suggests that plants in arid regions use a wide variety of adaptation strategies, and this diversity increases with the degree of aridity. The authors describe this response to aridity as the “plant loneliness syndrome”.  Heavily grazed drylands also correspond to greater diversity in traits. The findings emphasize that factors like soil fertility and plant cover contribute to trait diversity in challenging environments. This study underscores the significance of drylands as a global reservoir of plant diversity and shows how plants can adapt to increasing environmental pressures and climate change through diverse strategies. (Summary by Maneesh Lingwan @LingwanManeesh) Nature 10.1038/s41586-024-07731-3

Plant memories: How people build lasting connections with plants

People often fail to recognize and appreciate the importance of plants, a phenomenon known as Plant Awareness Disparity (PAD), also known as plant blindness. This lack of awareness has a negative impact on botanical knowledge and skill acquisitions, consequently affecting biodiversity conservation efforts. McGinn et al. investigated the relationship between art and plant awareness through an exhibition, “In Memory of Plants,” at the Alternative Kilkenny Arts Festival 2022, using art as a tool to address PAD phenomenon. The study revealed the importance of art as a tool for reflection and emotional engagement to connect people to plants. Visitors at the exhibition were encouraged to share their personal plant-related memories, and plants were seen to link people to significant experiences and relationships. The analysis demonstrated the importance of sensory experiences in relating to plants, giving a deeper understanding of human-plant connections and buttressing art-based research as an effective tool to enhance plant awareness and stimulate collaboration among artists, botanists and science communicators. This study, therefore advocates for art as a vital instrument in addressing biodiversity loss and supporting plant conservation efforts. (Summary by Idowu Arinola Obisesan, @IdowuAobisesan) Plants People Planet 10.1002/ppp3.10555

 

Review. Lighting the way: Compelling open questions in photosynthesis research

Photosynthesis is fundamental to life on Earth and a topic that all plant biologists should have a good understanding of, but it is also an incredibly complex set of processes, reactions and structures spanning great temporal and spatial distances. In this new Commentary by Eckardt et al., several experts summarize some of the fundamental unknowns being investigated in photosynthesis research. The questions focus largely on the light harvesting reactions, including the reaction center and the antenna complexes and their dynamic responses to the light and chemical environment. The authors also step beyond land plants by looking at other photosynthetic organisms, and consider unresolved questions about the evolution of photosynthesis. Open questions on stomatal regulation and the C4 pathway are also addressed. This is an engaging and compelling “must read”, and one severl in the upcoming Plant Cell Focus Issue on Photosynthesis, to be published in October, 2024. (Summary by Mary Williams @PlantTeaching) Plant Cell 10.1093/plcell/koae203

Review: Unlocking plant genetics with telomere-to-telomere genome assemblies

The era of complete telomere-to-telomere (T2T) plant genomes is finally here! Recent advances in long-read sequencing technologies have revolutionized genome assembly, giving rise to gapless T2T assemblies and offering unprecedented insights into genome organization and function. Why are T2T genomes so important? These assemblies provide a comprehensive, end-to-end view of a genome, covering all coding and non-coding regions. However, constructing T2T assemblies, especially for complex crop genomes with challenges like repeats, polyploidy, and heterozygosity, is a difficult task. This review by Garg et al. highlights such challenges and delves into the strategies and technological advancements necessary to overcome them. High-quality DNA extraction, improved sequencing accuracy, and the use of long-range scaffolding techniques like high-throughput chromosome conformation capture (Hi-C) and optical mapping are critical. Combining long-read sequencing and assembly algorithms, followed by manual curation, has resulted in complete T2T assemblies for crops such as rice and maize. The review also describes the current status of T2T plant genomes and their applications, including pangenomics, functional gene discovery, QTL cloning, and breeding strategies.  Complete T2T assemblies promise to resolve genetic complexities in important traits like yield, disease resistance, and climate adaptation and open up new research possibilities, including developing new crop varieties for future needs. However, achieving these assemblies requires collaboration among geneticists, bioinformaticians, breeders, and other experts, along with continued investment in sequencing technologies and data integration. (Summary by Ileana Tossolini @IleanaDrt)  Nature Genetics 10.1038/s41588-024-01830-7

Control of chloroplast biogenesis by MYB-related transcription factors

In this study, Frangedakis et al. identified MYB-related transcription factors as critical regulators of chloroplast development in land plants. Focusing on the liverwort Marchantia polymorpha and the angiosperm Arabidopsis thaliana, the team discovered that mutations in some MYB-related genes lead to pale plant phenotypes with significantly smaller chloroplasts, indicating their pivotal role in chloroplast biogenesis. Through genetic analysis and gene editing, the study revealed that these transcription factors target a broad array of genes involved in various aspects of chloroplast function, including chlorophyll biosynthesis, carbon fixation, photorespiration, and the assembly and repair of photosystems.  The research also revealed that these MYB-related transcription factors work redundantly and synergistically with other known regulators, such as the GOLDEN2-LIKE (GLK) family of transcription factors, to control chloroplast development. This discovery not only reveals the regulatory mechanisms governing chloroplast development but also opens new avenues for enhancing crop productivity by manipulating these master regulators. (Summary by Amarachi Ezeoke) Cell 10.1016/j.cell.2024.06.039

Plant rheostat BAP2 determines the direction of ER stress tolerance mechanisms

When protein folding is disrupted by abiotic or biotic stresses, cells can experience ER stress. Sensors like inositol-requiring enzyme 1 (IRE1) detect this stress, triggering the unfolded protein response (UPR) pathway. UPR signaling activates genes that restore proteostasis and maintain cellular vitality. However, under chronic ER stress, a pro-death strategy is initiated, leading to programmed cell death. But which route is taken and how this is controlled at the molecular level has been a long-standing question in ER stress research. Recently, Pastor-Cantizano and colleagues made a significant discovery in this area. They utilized the natural genetic variation in Arabidopsis to perform ER stress sensitivity assays, coupled with quantitative trait locus analyses, identifying BON-ASSOCIATED PROTEIN2 (BAP2) as a key player. Their analysis of bap2 mutants, combined with other UPR pathway components, revealed that BAP2 directs the UPR away from pro-death strategies when the stress is manageable. Conversely, under chronic stress, when the UPR can no longer sustain a pro-life response, BAP2 activates programmed cell death. This novel function of BAP2 as a rheostat, acting as a decision-maker depending on stress strength and duration, is just the beginning of unraveling the regulatory mechanisms controlling ER stress in plants. (Summary by Thomas Depaepe @thdpaepe). Nature Comms 10.1038/s41467-024-50105-6

SAM-seq: A novel approach for unraveling plant epigenetic complexity

The complex interplay between nucleosome positioning, DNA methylation, and chromatin accessibility is crucial for genome regulation in eukaryotic organisms. However, current chromatin profiling methods, which rely on short-read sequencing, fail to characterize highly repetitive genomic regions and cannot detect multiple chromatin features simultaneously. In a recent study, Leduque et al. addressed these challenges by introducing a novel approach called SAM-seq (Simultaneous Accessibility and DNA Methylation sequencing). They adapted the m6A-tagged chromatin accessibility assay, SMAC-seq, for use in purified plant nuclei and employed long-read nanopore sequencing technology to assess both chromatin accessibility and DNA methylation simultaneously. SAM-seq proved effective not only in the model organism Arabidopsis but also in a complex plant genome such as maize. SAM-seq allowed for a detailed examination of accessibility and DNA methylation, particularly in subnucleosomal regions associated with genes, transposable elements, and centromeric repeats. Notably, the power and sensitivity of SAM-seq facilitated the detection of short-scale changes in accessibility and the identification of cis-regulatory regions occupied by transcription factors in vivo. Additionally, the study revealed cellular heterogeneity within chromatin domains with opposing chromatin marks, suggesting that bivalency reflects cell-specific regulatory mechanisms rather than a uniform chromatin state. SAM-seq also offers an all-in-one tool to generate de novo genome assemblies together with detailed epigenome information. Its technical simplicity, reproducibility, scalability, and cost-effectiveness make it a valuable tool for studying chromatin regulation in both model and non-model plant species. (Summary by Ileana Tossolini @IleanaDrt) Nucleic Acids Res. 10.1093/nar/gkae306

Altering cold-regulated gene expression decouples the salicylic acid–growth trade-off

Enhancing plant defense against pathogens and pests often incurs a cost to essential physiological functions such as growth and reproduction, creating a trade-off. This phenomenon is evident in genetic studies across various plant models and agricultural breeding programs. Salicylic acid (SA) is a well-known phytohormone essential for basal immunity and systemic acquired resistance; however, its overaccumulation penalizes growth. Ortega and colleagues established a panel of Arabidopsis transgenic lines expressing a broad range of SA levels to study the effects of SA on growth, disease resistance, and abiotic stress tolerance. Interestingly, they observed that cold-regulated (COR) genes are repressed by increasing SA levels in a dose-dependent manner. Consequently, high-SA (hiSA) lines, which are smaller under unstressed conditions, grow even less when the temperature is lowered. However, strikingly, if COR genes are constitutively overexpressed in the hiSA lines, the growth defect can be rescued without compromising defense. This breakthrough suggests that the low-temperature response in plant can decouple the SA-mediated growth-defense trade-off, which potentially serving as an important strategy for balancing plant growth and immunity, thereby improving agricultural productivity. (Summary by Ching Chan @ntnuchanlab) Plant Cell 10.1093/plcell/koae210