Hidden influence: How microbial stress responses shape plant natural selection

Soil microbial communities respond rapidly to stress, potentially leading to altered compositions in stressful environments and consequently impacting plant natural selection. Bolin and Lau investigated the influence of microbial responses to stress and persistent microbial legacy effects on plant selection. Chamaecrista fasciculata (partridge pea) plants were cultivated under stressful (salt, herbicide, or herbivory) or non-stressful conditions with microbes previously exposed to these environments. Microbial responses to stress counteracted the direct effects of stress on plant selection, thereby attenuating stress’s role as a selective agent. Additionally, microbial legacy effects of stress altered plant selection in non-stressful environments, indicating a prolonged impact beyond the stress period. These findings suggest that soil microbes may alter plant adaptation to stress, potentially reshaping the evolutionary trajectory of plant populations by reducing stress’s selective pressure. (Summary by Yueh Cho @YuehCho1984) New Phytologist. 10.1111/nph.19707.

Unintended consequences of planting native and non- native trees in treeless ecosystems to mitigate climate change

Afforestation initiatives are globally underway to replace naturally treeless ecosystems with native and non-native trees. The primary objective is to enhance atmospheric carbon capture as a means to combat climate change. This review seeks to illuminate the diverse impacts of afforestation, both positive and negative, while also proposing mitigation strategies. Notably, the replacement of grasslands and shrublands during afforestation can adversely affect biodiversity. Negative consequences may include water yield reduction, soil salinization, soil carbon depletion, heightened wildfire risk, and increased soil temperatures. Additionally, the proliferation of woody plants presents a health hazard by facilitating the spread of vector-borne diseases. Given the complexity of afforestation efforts, it is crucial to consider various factors such as tree species selection, location suitability, and the duration of tree growth. Special care is warranted when introducing non-native trees to prevent them from replacing native species. Furthermore, prioritizing conservation and restoration initiatives over afforestation may offer greater potential for carbon sequestration. (Summary by Villő Bernád @BernadVillo) J. Ecol. 10.1111/1365-2745.14300

Plant Science Research Weekly: April 19, 2024

Review: Chloroplast ion homeostasis

Healthy plants require access to several mineral nutrients, which are usually taken up in ionic form. The details of nutrient uptake, distribution, and function have been painstakingly revealed over several decades. In this excellent new Tansley Review, Kunz et al. provide an overview of ion homeostasis with a focus on the chloroplast and the roles of these mineral ions in photosynthesis. Moving charged ions across membranes requires transport proteins, and plastids have three sets of membranes (outer, inner, and thylakoid) so there is a lot of information about the many transporters involved. Functionally, plastid mineral ions have diverse roles. Several, such as Cu2+, Fe2+, Mn2+, and Zn2+, are necessary as cofactors for the light harvesting and electron transport proteins, and the mechanisms that ensure their homeostasis (right place, right time, right amount) are described. The authors also look at how changing light conditions affect activities of some of the key transporters such as KEA3. They also present the phylogenetic distribution of orthologues across the photosynthetic lineages, noting that cyanobacteria, ancestral plastids, show little overlap with the eukaryotic transportome. The review concludes with a discussion of future research areas, noting that plastid ion homeostasis provides an untapped approach to engineer improved photosynthesis in plants. (Summary Mary Williams @PlantTeaching) New Phytol. 10.1111/nph.19661

Unraveling the role of tRNA thiolation in translation control for plant immunity

Thiolation of tRNA adds a sulfur-containing nucleotide modification at the tRNA wobble position, which is necessary for efficient translation. Zheng et al. investigated the role of tRNA thiolation in plant immunity, revealing its necessity for robust defense responses in Arabidopsis. They identified a pathogen hyper-susceptible mutant, cgb, that encodes ROL5, an enyme required for tRNA thiolation.  They showed that, as in yeast, ROL5 interacts with CTU2, which also displays a hyper-susceptible phenotype when function is lost. Using these mutants and proteins, the authors elucidated the molecular mechanisms of tRNA thiolation underlying plant defense. Inhibiting tRNA thiolation causes disruptions in transcriptome and proteome dynamics, particularly impacting NPR1 translation, which highlights the regulatory function of tRNA thiolation in defense signaling pathways. Overall, this research advances our understanding of plant immunity and unveils a novel biological function of tRNA thiolation. (Summary by Yueh Cho @YuehCho1984) eLife. 10.7554/eLife.93517.

How do plants export brassinosteroids?

If you’ve ever wondered how plants grow, survive, and adapt to their dynamic environment, the secret lies in their vast array of chemical messengers, also called phytohormones. Brassinosteroids are important hormones that are crucial for plant development and defense against environmental stresses. Like other hormones, brassinosteroids also require specific proteins and other helpers for their perception and signaling inside the cell. Although many of the proteins involved in brassinosteroid signaling have been well-characterized, until now its export mechanism was unknown. In this study, Ying et al. identified ABCB19, an ABC transporter, as an exporter of this hormone. The authors  demonstrated the stimulation of ATPase activity of the ABCB19 protein in presence of brassinolides (BL), which confirmed that these proteins interact with BL. Interestingly, this effect was specific to BL. The role of ABCB19 as a brassinosteroid transporter was further established by studying accumulation of BL over time in proteoliposomes containing ABCB19 and Arabidopsis protoplasts incubated with castasterone, a transport substrate for ABCB19. Additionally, in silico studies revealed that the ABCB19 consists of two transmembrane domains, one of which is important for binding with the brassinosteroid molecule. Furthermore, ABCB19 was shown to regulate brassinosteroid signaling together with ABCB1 by using plants with defective ABCB1 and ABCB19 genes. Thus, this study sheds light on an important player involved in transporting brassinosteroids across the cell membrane. (Summary by Abira Sahu @AbiraSahu) Science  10.1126/science.adj4591

Methyltransferase TaSAMT1 mediates wheat freezing tolerance by integrating brassinosteroid and salicylic acid signaling

Temperature extremes, such as cold stress, severely affect wheat (Triticum aestivum) productivity and quality by impairing its vegetative and reproductive growth. Several phytohormones have roles in cold stress, such as brassinosteroids (BRs) and salicylic acid (SA). However, how BR interacts with SA in response to cold stress remains unknown. In this work, Chu et al. describe the role of an SA methyltransferase named TaSAMT1 and its function in conferring freezing tolerance in wheat. They demonstrated that TaSAMT1 converts SA to methyl SA (MeSA), a volatile form of SA that acts as a signal molecule in plant responses to abiotic stress.  Through various experiments, including use of Arabidopsis thaliana knock-out and overexpressing mutant lines, they established a role of MeSA in the response to freezing tolerance in wheat. In addition, they elucidated how SA and BRs pathways interact in the regulation of freezing tolerance. Specifically, they found that BRASSINAZOLE-RESISTANT 1 (TaBZR1) directly interacts with the TaSAMT1 promoter, inducing its transcription.  Finally, TaBZR1 also interacts with TaHAG1, a histone acetyltransferase that enhances TaSAMT1 expression via histone acetylation but it also interacts with TaHAG1, a histone acetyltransferase that enhances TaSAMT1 expression via histone acetylation. This work suggests that TaSAMT1 might be a target for selection and breeding for improving wheat cold tolerance. (Summary by Eva Maria Gomez Alvarez @eva_ga96) Plant Cell 10.1093/plcell/koae100

A nitrogen-fixing algal organelleCoale et al. provide an exciting peek into the evolution of a nitrogen-fixing organelle (called a nitroplast) in their studies of a tiny marine alga, Braarudosphaera bigelowii and its endosymbiont cyanobacterium, Candidatus Atelocyanobacterium thalassa (UCYN-A). Plant biologists are familiar with other nitrogen-fixing endosymbionts, such as the rhizobia that reside in plant nodules. And of course, we are all familiar with the mitochondria and plastids, descendants of ancient endosymbionts that have lost their ability to live independently of the host cell. The interesting new findings presented by Coale et al. suggest that the UCYN-A, long-considered to be an endosymbiont, has evolved into an organelle. The authors used soft x-ray tomography to image the single-celled alga during division. They found that the single endosymbiont/nitroplast in each cell replicates alongside the other cellular compartments, and one each of the resulting structures is passed into each daughter cell. What cements this as an organelle is that many genes required for its viability and function (such as genes required to synthesize amino acids) are encoded in the host genome and imported into the nitroplast. Interestingly, these proteins are marked by a novel transit peptide that directs them to the nitroplast, analogous to how nuclear-encoded plastid or mitochondrial proteins are imported. Besides providing yet another example of how “life finds a way”, this study opens the door to the possibility of introducing nitroplasts into crop plants and alleviating a major agricultural challenge. (Summary by Mary Williams @PlantTeaching) Science 10.1126/science.adk1075

Altering root system architecture in barley without impacting above-ground traits

Roots are important for acquiring water and nutrients from the soil; however root system architecture is poorly understood in cereal crops. Here Aldiss et al. used CRISPR/Cas9 to generate barley mutants in the auxin transporter PIN-FORMED2 (PIN2). Seedlings were grown in chambers and after four days the chambers were rotated by 90o. Whilst the roots of wild type plants grew towards the gravity vector, the roots of mutant plants did not, suggesting they were agravitropic. To look at the root system architecture of more mature plants, the mutants were grown in wide rhizoboxes for 28 days. Analysis of the root system using the image analysis software RhizoVision Explorer showed that pin2 plants had a wider root system and more shallow roots, defined as having a root angle of less than 30o. Interestingly, pin2 plants had no significant difference in shoot biomass and no differences in either tiller number or time to flowering. Hence mutating PIN2 provides a way of generating a wide, shallow root system in barley without compromising above ground traits, which could be beneficial for capturing phosphorus or water from the topsoil. (Summary by Rose McNeilly @Rose_McN)  bioRxiv  10.1101/2024.03.28.587117v1

All fruit things come to an end: FRUITFULL controls end of flowering and seed yield in pea

The onset of flowering is a tightly regulated process, as is the end of the reproductive phase in plants. In Arabidopsis thaliana, FRUITFULL (FUL) contributes to ending the reproductive cycle, as do signals derived from developing seeds. Here, Martínez-Fernández et al. explored to which extent that role extends to other plant species, namely pea (Pisum sativum ‘Cameor’). The expression levels of pea FUL genes PsFULa and PsFULb are upregulated upon floral transition. As in Arabidopsis, loss-of-function mutant psfulb and double-mutant psfula/b lines have longer reproductive cycles and develop more pods and seeds per plant than WT. Fruit and seed morphology and composition, however, do not differ significantly between WT and mutant lines. As seed-derived signals also contribute to ending the reproductive phase, the authors investigated the interaction between the FUL genes and seed signals. When seed formation was inhibited, all plants had longer reproductive phases, with the extension in psfulb and psfula/b phases approximately 9- and 12-fold longer, respectively. This shows that the FUL genes and seed-derived signals synergistically determine the end of the reproductive phase. Field trials revealed that psfulb and psfula/b plants yield significantly higher seed production when compared to WT, showcasing the agricultural potential that might be harnessed by understanding end-of-flowering regulation. (Summary by John Vilasboa @vilasjohn) Proc Natl Acad Sci. USA  10.1073/pnas.2321975121

SWEET sugar transporters orchestrate distribution of microbiota along the longitudinal axis of Arabidopsis roots

Plant roots are functionally distinct along the longitudinal axis due to different cell types and diverse metabolic states. Root-secreted metabolites are involved in the assembly of complex microbial communities, yet the relationships between root-metabolites and organization of root microbiota at the spatial scale is poorly understood. This is partly because of a lack of suitable system to study such relationships by simultaneous profiling of metabolites and microbiota along the longitudinal axis of roots. Loo et al. developed two complementary plant growth systems, CD-rhizotron and ArtSoil, to study such relationships. Through bacterial community profiling (root endospheric and rhizosphere fractions) and metabolomics analyses, they showed that differential microbial community structure coincided with a differential metabolite accumulation along the longitudinal axis, suggesting spatial metabolite profiles could be implicated for orchestrating the microbial community. Further, applying bioinformatics, GUS histochemical analyses, and Arabidopsis mutant lines, they discovered a relationship between SWEET transporters (sugar transporters) and microbial communities along the longitudinal root axes. Specifically, several SWEET uniporters were induced by microbiota along the longitudinal root axis, and they contributed to microbial community assembly. This study established the spatial coordination between sugar transporters and microbial community assembly in roots. (Summary by Arijit Mukherjee @ArijitM61745830) Cell Host Microbe 10.1016/j.chom.2024.02.014

Unlocking nature’s arsenal: Engineering grasses for insect defense and livestock palatability

The defensive alkaloid gramine, present in barley and other grass species, plays an important role in protecting the plant from insect damage but poses challenges for ruminant palatability. Breeding strategies balance these factors by maintaining the protective function and making the grain palatable for grazing animals. In this study, Dias et al. used pan-genome sequencing to identify a gramine biosynthesis gene cluster in barley. They further characterized an enzyme responsible for the intricate oxidative rearrangement of tryptophan. Through the adjustment of gramine levels in yeast and various plant species, the authors demonstrated that gramine-related traits could be optimized. This study represents a big step forward in understanding grass defenses for agricultural improvement. (Summary by Yueh Cho @YuehCho1984) Science. 10.1126/science.adk6112.

Hidden influence: How microbial stress responses shape plant natural selection

Soil microbial communities respond rapidly to stress, potentially leading to altered compositions in stressful environments and consequently impacting plant natural selection. Bolin and Lau investigated the influence of microbial responses to stress and persistent microbial legacy effects on plant selection. Chamaecrista fasciculata (partridge pea) plants were cultivated under stressful (salt, herbicide, or herbivory) or non-stressful conditions with microbes previously exposed to these environments. Microbial responses to stress counteracted the direct effects of stress on plant selection, thereby attenuating stress’s role as a selective agent. Additionally, microbial legacy effects of stress altered plant selection in non-stressful environments, indicating a prolonged impact beyond the stress period. These findings suggest that soil microbes may alter plant adaptation to stress, potentially reshaping the evolutionary trajectory of plant populations by reducing stress’s selective pressure. (Summary by Yueh Cho @YuehCho1984) New Phytologist. 10.1111/nph.19707.

Unintended consequences of planting native and non- native trees in treeless ecosystems to mitigate climate change

Afforestation initiatives are globally underway to replace naturally treeless ecosystems with native and non-native trees. The primary objective is to enhance atmospheric carbon capture as a means to combat climate change. This review seeks to illuminate the diverse impacts of afforestation, both positive and negative, while also proposing mitigation strategies. Notably, the replacement of grasslands and shrublands during afforestation can adversely affect biodiversity. Negative consequences may include water yield reduction, soil salinization, soil carbon depletion, heightened wildfire risk, and increased soil temperatures. Additionally, the proliferation of woody plants presents a health hazard by facilitating the spread of vector-borne diseases. Given the complexity of afforestation efforts, it is crucial to consider various factors such as tree species selection, location suitability, and the duration of tree growth. Special care is warranted when introducing non-native trees to prevent them from replacing native species. Furthermore, prioritizing conservation and restoration initiatives over afforestation may offer greater potential for carbon sequestration. (Summary by Villő Bernád @BernadVillo) J. Ecol. 10.1111/1365-2745.14300

A key player in glutamate export from Arabidopsis chloroplasts

The et al. identified a chloroplast glutamate exporter in Arabidopsis thaliana. The Plant Cell (2023).

By Samantha The and Mechthild Tegeder, School of Biological Sciences, Washington State University, Pullman, WA, 99164, USA

https://doi.org/10.1093/plcell/koad310

Background: Plants produce amino acids in chloroplasts, and membrane transporters are needed to move these amino acids to the cytosol. In the cytosol, the amino acids are used for protein production and other biochemical pathways within leaf cells and to supply nitrogen to growing sink organs, such as seeds. However, despite their importance, little is known about these plastidial exporters.

Questions: What is the role of chloroplast amino acid transporters in leaf metabolism and long-distance transport of nitrogen? What is their physiological importance?

Findings: We found that Arabidopsis thaliana USUALLY MULTIPLE ACIDS MOVE IN AND OUT TRANSPORTER 44 (UMAMIT44) localizes to the chloroplast envelope and regulates plastidial glutamate export and glutamate homeostasis within and outside of chloroplasts. Decreased export and subsequent cellular imbalances in umamit44 mutants impact the cellular redox state and affect both leaf nitrogen and carbon metabolism as well as the long-distance delivery of nitrogen and carbon to growing organs. Observed changes lead to decreased mutant growth and seed yield. Nevertheless, umamit44 plants adapt to some extent by accelerating alternative pathways for glutamate synthesis outside of chloroplasts and by producing other amino acids and antioxidants to alleviate oxidative stress. Overall, we demonstrate that UMAMIT44 is an essential player in plastidial glutamate export and vital for plant growth and development.

Next steps: Transcriptome, 13CO2 labeling and metabolic flux analyses are needed to determine the interrelationship between plastidial amino acid export, cellular metabolism and sink nitrogen supply. In addition, the identification of further chloroplast amino acid transport systems is a “must-do” as our understanding of the kind of transporters that mediate chloroplast efflux or influx of amino acids, and how they affect metabolic networks, metabolite levels and sink nitrogen nutrition, remains in its infancy.

Reference:

Samantha V. The, James P. Santiago, Clara Pappenberger, Ulrich Z. Hammes, and Mechthild Tegeder. (2023). UmamiT44 is a key player in glutamate export from Arabidopsis chloroplasts. https://doi.org/10.1093/plcell/koad310

MdBPC2 regulates apple growth

Zhao et al. discovered that MdYUC2a and MdYUC6b are targets of H3K27me3 modification mediated by MdBPC2-MdLHP1, which regulates auxin biosynthesis during apple growth.

https://doi.org/10.1093/plcell/koad297

Haiyan Zhao, Shuyuan Wan, Yanni Huang, Xiaoqiang Li, Tiantian Jiao, Zhijun Zhang, Baiquan Ma, Lingcheng Zhu, Fengwang Ma, Mingjun Li.

State Key Laboratory for Crop Stress Resistance and High-Efficiency/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Yangling 712100, Shaanxi, China.

Background: Plant height is an agronomic trait that markedly affects crop yield. It is controlled by the environment, plant hormone metabolism and signaling pathways. Transcription factors play a key role in these processes and have been proposed to be involved in the regulation of plant height. Although little is known about the underlying molecular mechanisms by which they regulate plant dwarfism, a BARLEY B RECOMBINANT/BASIC PENTACYSTEINE (BBR/BPC) transcription factor induces plant dwarfing in Arabidopsis and rice. In apple, the Class I BBR/BPC gene MdBPC2 is highly expressed in dwarfing rootstocks, and MdBPC2-overexpressing plants show a dwarf phenotype. However, the exact mechanism of how BPC transcription factors affect plant structure is not well understood.

Question: What is the role of MdBPC family members in regulating growth and development of apple plants, and how do they function?

Findings: We found that a BBR/BPC transcription factor gene, MdBPC2, was highly expressed in dwarfing rootstocks. When MdBPC2 was overexpressed, auxin content decreased, plant growth was inhibited, plant height decreased, and roots were underdeveloped. These growth defects were reversed by supplementation of exogenous auxin. MdBPC2 bound to the GAGA-Rich element of the MdYUC2a and MdYUC6b promoters, inhibiting their expression. We also found that MdBPC2 interacted with MdLHP1 and recruited it to MdYUC2a and MdYUC6b gene loci to mediate the catalysis and maintenance of H3K27me3 methylation, enhancing chromatin condensation. This process led to the inhibition of MdYUC2a and MdYUC6b transcription, which limited auxin synthesis and ultimately stimulated dwarfism of apple plants.

Next steps: In view of the significant decrease of MdGH3.1 in MdBPC2 overexpressing transgenic plants, we will next focus on the mechanism of MdBPC2 involved in maintaining auxin homeostasis, which will deepen our understanding of how plants promote or inhibit their development in response to environmental changes, thereby enhancing their environmental adaptability.

Reference:

Haiyan Zhao, Shuyuan Wan, Yanni Huang, Xiaoqiang Li, Tiantian Jiao, Zhijun Zhang, Baiquan Ma, Lingcheng Zhu, Fengwang Ma, Mingjun Li. (2024). The transcription factor MdBPC2 alters apple growth and promotes dwarfing by regulating auxin biosynthesis. https://doi.org/10.1093/plcell/koad297

Examination of the plant cytokinesis machinery reveals the rules of cellular asymmetry

Schmidt-Marcec, Parish and colleagues characterize members of the MACERATOR (MACET) family of proteins in the context of cell division.

 https://doi.org/10.1093/plcell/koad304

 By Sharol Schmidt-Marcec, Alyssa Parish, Tetyana Smertenko, Matthew Hickey, Bernard M.A.G. Piette, Andrei Smertenko

Institute of Biological Chemistry, Washington State University, Pullman, WA99164, USA; Department of Mathematics, Durham University, Durham UK

Background: The success of many cellular programs depends on asymmetry, resulting from a shift of cellular components from an even to an uneven distribution. Understanding the rules of cellular asymmetry requires information about structural blocks and their behavior in specific contexts. We use cell division as a model system to explore cellular asymmetry. Cells in land plants divide via the formation of a cell plate, a partition formed of membranes and oligosaccharides. The cell plate is constructed by an asymmetrical structure known as the phragmoplast, whose structure is maintained by microtubules, 25-nm thick tubes built from the protein tubulin. Microtubules govern phragmoplast asymmetry through three types of behavior: nucleation (birth of a new microtubule), growth, and shrinkage. The transition between these behaviors is controlled by tubulin availability: higher tubulin abundance promotes microtubule polymerization, whereas low tubulin abundance triggers depolymerization. Cells contain a fixed amount of tubulin, meaning that microtubule polymerization causes depletion of tubulin, leading to depolymerization and vice versa.

Question: What is the role of microtubule nucleation and geometry in phragmoplast asymmetry?

Findings: We analyzed the Arabidopsis thaliana MACERATOR (MACET) family comprising seven plant-specific microtubule-nucleating proteins. Mutants lacking MACET4 and MACET5 function (mce4-1 mce5) showed defective phragmoplast asymmetry and morphology caused by a greater angle of branched microtubule nucleation. MACET4 interacts with the plant-specific microtubule nucleation factor AUGMIN7. Simultaneous mutation of MACET4, MACET5, and AUGMIN7, causes plant lethality. A computational analysis revealed that microtubule nucleation by MACET depletes tubulin, leading to destabilization of phragmoplast microtubules. Hence, assembly factors contribute to cellular asymmetry directly by defining the architecture of cellular structures and indirectly by the controlling abundance of their building blocks.

Next steps: Identification and functional characterization of proteins that cooperate with MACET. Determining the rules of cellular asymmetry would advance understanding of life and enable engineering of living systems.

Reference:

Sharol Schmidt-Marcec, Alyssa Parish, Tetyana Smertenko, Matthew Hickey, Bernard M.A.G. Piette, Andrei Smertenko (2024). The microtubule nucleating factor MACERATOR tethers AUGMIN7 to microtubules and governs phragmoplast architecture. https://doi.org/10.1093/plcell/koad304

Mechanisms underlying transposable element load variation in Arabidopsis

Jiang et al. explore the mechanisms underlying transposable element load variation in the model plant Arabidopsis thaliana.

 https://doi.org/10.1093/plcell/koad296

By Juan Jiang (Institute of Botany, Chinese Academy of Sciences) and Ya-Long Guo (Institute of Botany, Chinese Academy of Sciences)

Background: Genetic load refers to accumulated deleterious mutations that could reduce organism fitness. Range expansion promotes adaptation but increases genetic load. Transposable elements (TEs) are a type of repetitive DNA sequence mobilizing across the genome; this mobilization could rapidly produce large-effect mutations. Understanding genetic load and its drivers during range expansion has important implications for human health, crop breeding, and conservation biology. However, the genetic load of TEs during range expansion remains unclear.

Question: How did the genetic load of TEs vary during Arabidopsis (Arabidopsis thaliana) range expansion? What are the driving forces of TE load variation?

Findings: By analyzing the genomes of 1,115 worldwide Arabidopsis accessions, we determined that the deleterious effect of TEs is between that of deleterious missense mutations and loss-of-function mutations. TE load accumulated along the expansion axis, particularly in the recently established Yangtze River basin population. Effective population size explained 62.0% of the variance in TE load. High transposition rates and selective sweeps also contributed to TE accumulation in the expanded populations. In addition, we genetically mapped the candidate causal genes or TEs and revealed the genetic architecture of TE load variation among natural populations.

Next steps: It is important to incorporate multiple genome assemblies or long-read sequencing data to capture the full landscape of TE variation. We must also clarify the relative contribution of each driving force to TE load variation and perform experimental validation of candidate genes or TEs associated with TE load variation in natural populations.

Reference:

Juan Jiang, Yong-Chao Xu, Zhi-Qin Zhang, Jia-Fu Chen, Xiao-Min Niu, Xing-Hui Hou, Xin-Tong Li, Li Wang, Yong Zhang, Song Ge, Ya-Long Guo. (2023). Forces driving transposable element load variation during Arabidopsis range expansion. https://doi.org/10.1093/plcell/koad296

Thermoprotection by a metacaspase

Zhou et al. examine the fundamental functions of metacaspases in the unicellular green alga Chlamydomonas reinhardtii.

https://doi.org/10.1093/plcell/koad289

By Yong Zou, Adrian N. Dauphinee, Simon Stael and Peter V. Bozhkov

Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden

Background: Metacaspases are a large class of proteases spanning kingdoms of life including bacteria but absent from animals; they are believed to represent an ancestral group from which animal-specific caspases evolved. In contrast to caspases, a textbook example of well-studied proteases, metacaspases remain poorly understood. Recent research just began to link metacaspases to the biology of land plants, which possess multiple metacaspase genes (e.g., nine in Arabidopsis thaliana) split into two major types (I and II), which substantially complicates their characterization. By contrast, green algae represent an ideal model for metacaspase research, as their genomes carry only one or two metacaspase genes.

Question: We wished to establish a toolbox of chemical probes and mutant strains for metacaspase research in a major unicellular green algal model, Chlamydomonas (Chlamydomonas reinhardtii). With such a toolbox in hand, we intended to investigate the fundamental functions of metacaspases in a unicellular plant lineage.

Findings: Knockout of the single type-II metacaspase gene of Chlamydomonas (named CrMCA-II) decreased algal fitness under heat stress (42°C), resulting in lower growth and increased cell death. Unlike other studied plant metacaspases, CrMCA-II was abundantly associated with the plasma membrane but partially translocated to the cytoplasm during heat treatment. Another peculiar feature of CrMCA-II was its oligomerization to form both catalytically active dimers and larger, megadalton-scale complexes comprising inactive pro-enzyme (zymogen). We discovered that the thermoprotective function of CrMCA-II is independent of its proteolytic activity but instead might be associated with an unknown mechanism by which CrMCA-II mediates fluidization of the plasma membrane.

Next steps: Understanding exactly how CrMCA-II works at the subcellular and molecular levels to confer thermoprotection to algal cells awaits further investigations. In this context, isolation and characterization of the megadalton-size CrMCA-II complex, including its structural analysis, represents a particular challenge.

Reference:

Yong Zou, Igor Sabljić, Natalia Horbach, Adrian N. Dauphinee, Anna Åsman, Lucia Sancho Temino, Elena A. Minina, Marcin Drag, Simon Stael, Marcin Poreba, Jerry Ståhlberg and Peter V. Bozhkov (2024). Thermoprotection by a cell membrane-localized metacaspase in a green alga. https://doi.org/10.1093/plcell/koad289

Things to do before you die: The bucket list of a plant cell

Wang, Bollier, Buono, et al. catalog the cellular processes that occur during programmed cell death in plants.

https://doi.org/10.1093/plcell/koad308

Jie Wang, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China

Moritz K. Nowack, VIB-UGent Center for Plant Systems Biology, Gent, Belgium

Background: Programmed cell death (PCD) is a genetically controlled process causing the targeted death of specific cells. Plants use PCD to fight pathogens, but also during development, growth and reproduction. Efficient water transport from the roots to the leaves for instance relies on PCD to produce a network of dead hollow xylem cells that function as water conduits. However, despite the importance of PCD for plant development, information on the cellular mechanisms that execute PCD in plants remains fragmentary.

Question: We set out to generate a detailed inventory of the cellular processes that occur during PCD execution in plants. We wanted to know which processes occur, and in which order they facilitate a controlled cessation of vital cellular functions.

Findings: Making use of the accessibility of the Arabidopsis thaliana root cap for live-cell confocal microscopy imaging, we followed the fate of different cellular compartments in a high spatial and temporal resolution. We identified a succession of ordered and stepwise events causing the breakdown of cellular compartmentalization that is necessary to keep cells alive. We found that an increase of intracellular calcium and proton levels, accompanied by mitochondrial breakup, are the earliest events in PCD execution. Only minutes later, the nucleus and the endoplasmic reticulum collapse, releasing their contents into the cytosol. Finally, the large central vacuole breaks up, and the plasma membrane becomes permeable to dyes that cannot normally enter the cell. Intriguingly however, the plasma membrane remains largely intact after cell death execution, effectively restricting the release of proteins from dead cells.

Next steps: We found that the order of cellular de-compartmentalization events is under genetic control. Hence we are now entering an exciting phase of research in which we will attempt to find molecular regulators for the individual PCD execution steps that jointly cause cellular death and breakdown.

Reference:

Jie Wang, Norbert Bollier, Rafael Andrade Buono, Hannah Vahldick, Zongcheng Lin, Qiangnan Feng, Roman Hudecek, Qihang Jiang, Evelien Mylle, Daniel Van Damme, and Moritz K. Nowack. (2024). A developmentally controlled cellular decompartmentalization process executes programmed cell death in the Arabidopsis root cap. https://doi.org/10.1093/plcell/koad308