Stavros Vraggalas

Goethe University Frankfurt

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Sotirios Fragkostefanakis

Goethe University Frankfurt

Remus R. E. Rosenkranz

Max Planck Institute of Biophysics

Mario Keller

Goethe University Frankfurt

Moussa Benhamed

Université Paris Cité

Stefan Simm

Universitätsmedizin Greifswald

Kathi Zarnack

Goethe University Frankfurt

Enrico Schleiff

Goethe University Frankfurt

Christos Bazakos

Max Planck Institute for Plant Breeding Research

Michael Feldbrügge

Heinrich Heine University Düsseldorf

Thomas Berberich

Senckenberg Biodiversity and Climate Research Centre

Cooperative Institutions

Goethe University Frankfurt

Centre National de la Recherche Scientifique

University of Vienna

Consejo Superior de Investigaciones Científicas

Max Planck Society

Ghent University

Vlaams Instituut voor Biotechnologie

Université Paris-Saclay

Magyar Agrár- és Élettudományi Egyetem

University of Naples Federico II

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Integrative approaches to enhance reproductive resilience of crops for climate-proof agriculture

Plant Stress (2024)

Collins Agho Adi Avni Ariola Bacu Ayat Bakery Salma Balazadeh

Resilience

Proof of concept

10.1016/j.stress.2024.100704

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Citations (2)

A plant-specific clade of serine/arginine-rich proteins regulates RNA splicing homeostasis and thermotolerance in tomato

bioRxiv (Cold Spring Harbor Laboratory) (2024)

Remus R. E. Rosenkranz Stavros Vraggalas Mario Keller Srimeenakshi Sankaranarayanan François McNicoll

Abstract High temperatures cause heat stress (HS), which has negative effects on plant growth and development and affects many cellular processes including pre-mRNA splicing. In tomato plants the splicing profile of many of genes is altered under HS, including that of HSFA2 , a central transcriptional regulator of thermotolerance. To identify the core splicing regulators of HS-sensitive alternative splicing, we used HSFA2 as bait and identified two plant-specific members of the serine/arginine-rich family of splicing factors, namely RS2Z35 and RS2Z36, that inhibit HSFA2 intron splicing. Single and double CRISPR mutants of these proteins show dysregulated splicing of many genes and exhibit lower basal and acquired thermotolerance. Individual-nucleotide resolution UV cross-linking and immunoprecipitation (iCLIP) of tomato leaves revealed that the majority of HS-sensitive alternatively spliced RNAs are bound by RS2Z35 and RS2Z36 and this interaction occurs at purine-rich RNA motifs. Phenotypic and transcriptome analyses revealed that RS2Z35 and RS2Z36 are important players in the stress response and thermotolerance in plants that mitigate the negative effects of HS on RNA splicing homeostasis.

SR protein

Splicing factor

Homeostasis

10.1101/2024.05.15.594399

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Citations (1)

Identification and Regulation of Tomato Serine/Arginine-Rich Proteins Under High Temperatures

Frontiers in Plant Science (2021)

Remus R. E. Rosenkranz Samia Bachiri Stavros Vraggalas Mario Keller Stefan Simm

Alternative splicing is an important mechanism for the regulation of gene expression in eukaryotes during development, cell differentiation or stress response. Alterations in the splicing profiles of genes under high temperatures that cause heat stress (HS) can impact the maintenance of cellular homeostasis and thermotolerance. Consequently, information on factors involved in HS-sensitive alternative splicing is required to formulate the principles of HS response. Serine/arginine-rich (SR) proteins have a central role in alternative splicing. We aimed for the identification and characterization of SR-coding genes in tomato ( Solanum lycopersicum ), a plant extensively used in HS studies. We identified 17 canonical SR and two SR-like genes. Several SR-coding genes show differential expression and altered splicing profiles in different organs as well as in response to HS. The transcriptional induction of five SR and one SR-like genes is partially dependent on the master regulator of HS response, HS transcription factor HsfA1a. Cis -elements in the promoters of these SR genes were predicted, which can be putatively recognized by HS-induced transcription factors. Further, transiently expressed SRs show reduced or steady-state protein levels in response to HS. Thus, the levels of SRs under HS are regulated by changes in transcription, alternative splicing and protein stability. We propose that the accumulation or reduction of SRs under HS can impact temperature-sensitive alternative splicing.

SR protein

Splicing factor

10.3389/fpls.2021.645689

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Citations (20)

Heat stress transcription factors as the central molecular rheostat to optimize plant survival and recovery from heat stress

New Phytologist (2024)

Ayat Bakery Stavros Vraggalas Boushra Shalha Harsh Chauhan Moussa Benhamed

Heat stress transcription factors (HSFs) are the core regulators of the heat stress (HS) response in plants. HSFs are considered as a molecular rheostat: their activities define the response intensity, incorporating information about the environmental temperature through a network of partner proteins. A prompted activation of HSFs is required for survival, for example the de novo synthesis of heat shock proteins. Furthermore, a timely attenuation of the stress response is necessary for the restoration of cellular functions and recovery from stress. In an ever-changing environment, the balance between thermotolerance and developmental processes such as reproductive fitness highlights the importance of a tightly tuned response. In many cases, the response is described as an ON/OFF mode, while in reality, it is very dynamic. This review compiles recent findings to update existing models about the HSF-regulated HS response and address two timely questions: How do plants adjust the intensity of cellular HS response corresponding to the temperature they experience? How does this adjustment contribute to the fine-tuning of the HS and developmental networks? Understanding these processes is crucial not only for enhancing our basic understanding of plant biology but also for developing strategies to improve crop resilience and productivity under stressful conditions.

Heat shock factor

10.1111/nph.20017

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Citations (5)

A plant-specific clade of serine/arginine-rich proteins regulates RNA splicing homeostasis and thermotolerance in tomato

Nucleic Acids Research (2024)

Remus R. E. Rosenkranz Stavros Vraggalas Mario Keller Srimeenakshi Sankaranarayanan François McNicoll

Abstract Global warming poses a threat for crops, therefore, the identification of thermotolerance mechanisms is a priority. In plants, the core factors that regulate transcription under heat stress (HS) are well described and include several HS transcription factors (HSFs). Despite the relevance of alternative splicing in HS response and thermotolerance, the core regulators of HS-sensitive alternative splicing have not been identified. In tomato, alternative splicing of HSFA2 is important for acclimation to HS. Here, we show that several members of the serine/arginine-rich family of splicing factors (SRSFs) suppress HSFA2 intron splicing. Individual-nucleotide resolution UV cross-linking and immunoprecipitation (iCLIP) combined with RNA-Seq revealed that RS2Z35 and RS2Z36, which make up a plant-specific clade of SR proteins, not only regulate HSFA2 but approximately 50% of RNAs that undergo HS-sensitive alternative splicing, with preferential binding to purine-rich RNA motifs. Single and double CRISPR rs2z mutant lines show a dysregulation of splicing and exhibit lower basal and acquired thermotolerance compared to wild type plants. Our results suggest that RS2Z35 and RS2Z36 have a central role in mitigation of the negative effects of HS on RNA splicing homeostasis, and their emergence might have contributed to the increased capacity of plants to acclimate to high temperatures.

SR protein

Splicing factor

10.1093/nar/gkae730

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Citations (2)

Regulation of early-stage tomato fruit growth by the splicing factor RS2Z36

bioRxiv (Cold Spring Harbor Laboratory) (2025)

Stavros Vraggalas Remus R. E. Rosenkranz Mario Keller Yolanda Pérez‐Pérez Samia Bachiri

Fruit size and shape are determined by cell division and expansion. In tomato, the model plant for fleshy fruit development, both processes are associated with changes in gene expression, including transcription and RNA processing. While several transcription factors have been identified as regulators of genes involved in fruit development, the contribution of splicing regulators remains unknown. Profiling of RNA splicing-related genes revealed stage-preferential expression of several factors, including RS2Z36, a serine/arginine-rich splicing factor highly expressed during the early stages of fruit development. Mutations in RS2Z36 lead to smaller ellipsoid fruits than the wild type, with histological analysis showing elongated pericarp cells in the ovaries along the longitudinal axis. RNA-seq analysis uncovered numerous alternatively spliced genes involved in different biological processes. Complementary proteome analysis identified proteins with altered abundance and peptides corresponding to novel RNA splice isoforms, underscoring the role of RS2Z36 in shaping both transcriptome and proteome diversity. Immunofluorescence screening of cell wall proteins further demonstrated an increased abundance of LM6-recognized arabinan epitopes of rhamnogalacturonan-I pectins and arabinogalactan protein (AGP) epitopes in rs2z36.1 pericarp cells compared to the wild type. These findings highlight RS2Z36 as a critical regulator of alternative splicing, impacting fruit development through diverse transcriptome and proteome changes.

Splicing factor

Factor (programming language)

10.1101/2025.01.31.635986

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