Claudia Martinho

Endogenous viral elements inserted in host genomes are often regarded as inert relics of past infections. Whether they can retain infective potential and contribute to active viral cycles has remained largely unresolved. Here we demonstrate that giant viral elements in the multicellular alga Ectocarpus can reactivate and drive productive viral infections. Using long-read sequencing and transcriptomics, we identify full-length, transcriptionally active phaeoviruses integrated within the host genome, and we use classical genetics and CRISPR–Cas to demonstrate that these elements are stably inherited through the germline, while their reactivation is precisely regulated by developmental and environmental cues including temperature. We resolve the genomic integration sites and propose a mechanism for phaeovirus integration and replication. Our work provides direct evidence and uncovers the mechanisms by which giant viral elements can reactivate, replicate and transmit both horizontally and vertically in a multicellular eukaryote, establishing a new model of latency, inheritance and evolutionary impact of giant dsDNA viruses.

ARGONAUTE (AGO) proteins are a highly conserved family of RNA-binding proteins that play central roles in gene regulation and developmental processes across eukaryotes. Although AGO family members have been extensively studied in animals and plants, where they are typically encoded by multiple genes, their function in brown algae, a diverse and complex group of multicellular algae, remains largely unknown. Here, we show that the genomes of several brown algae encode only a single AGO protein, containing the conserved functional domains characteristic of the family. Using the model brown alga Ectocarpus and a combination of cell biology, genetic, and transcriptomic approaches, we demonstrate that AGO is essential for the transition from vegetative growth to sexual reproductive development and for germline establishment. Our results further suggest that AGO functions in concert with microRNAs to regulate target genes primarily at the posttranscriptional level, likely through translational repression. Ectocarpus thus represents a rare example of a complex multicellular organism that relies on a single AGO protein to regulate key developmental processes, pointing to a minimalistic model of RNA-based regulation in brown algae.

Societal Impact Statement: Plants provide oxygen, food, shelter, medicines and environmental services, without which human society could not exist. Tackling pressing and global challenges requires well‐trained plant scientists and plant‐aware individuals. This manifesto provides a practical evidence‐based vision to strengthen plant science education, focused on five strategic priorities. It is relevant to all stakeholders within plant science and beyond: from frontline educators to institutional leaders; from commercial or charitable professionals to entrepreneurs and donors; from individual community members to their legislative representatives. Strengthening plant science education demands concrete actions from all stakeholders, ultimately to the benefit of us all. Summary: Plant science education needs urgent attention. Skilled plant scientists are needed to address major environmental and societal challenges, and global communities require plant‐aware professionals to drive impactful policy, research and environmental stewardship. This manifesto was collaboratively generated by a community of educators who gathered to reflect on the state of plant science education. The forward‐facing document provides a clear strategy for plant science education, complementing existing research strategies. Five themes were identified as essential for meeting the evolving needs of plant science, educators and learners: (i) plants must be at the centre of an education that addresses global challenges and societal values; (ii) plant science education must prepare students for their futures using bold and effective pedagogies; (iii) equity, diversity and inclusion must be robustly embedded in educational practices; (iv) local and strategic partnerships (with industry and beyond) are required to strengthen academic education; and (v) plant science educators need resources and opportunities to develop and connect. The manifesto is intended as a framework for change. Educators, funders, publishers, industry representatives, policymakers and all other members of our communities must commit to sustained investment in plant science education. By proactively and collectively embracing the recommendations provided, the sector has an opportunity to cultivate a new generation equipped with the knowledge, skills and passion to unlock the full potential of photosynthetic organisms.

In many eukaryotes, genetic sex determination is not governed by XX/XY or ZW/ZZ systems but by a specialized region on the poorly studied U (female) or V (male) sex chromosomes. Previous studies have hinted at the existence of a dominant male-sex factor on the V chromosome in brown algae, a group of multicellular eukaryotes distantly related to animals and plants. The nature of this factor has remained elusive. Here, we demonstrate that an HMG-box gene acts as the male-determining factor in brown algae, mirroring the role HMG-box genes play in sex determination in animals. Over a billion-year evolutionary timeline, these lineages have independently co-opted the HMG box for male determination, representing a paradigm for evolution’s ability to recurrently use the same genetic “toolkit” to accomplish similar tasks.

Significance: Paramutation involves the transfer of a repressive epigenetic mark between silent and active alleles. It is best known from exceptional non-Mendelian inheritance of conspicuous phenotypes in maize but also in other plants and animals. Recent genomic studies, however, indicate that paramutation may be less exceptional. It may be a consequence of wide-cross hybridization and may contribute to quantitative trait variation or unstable phenotypes in crops. Using the sulfurea ( sulf ) locus in tomato, we demonstrate that a self-reinforcing feedback loop involving DNA- and histone-methyl transferases CHROMOMETHYLTRANSFERASE3 (CMT3) and KRYPTONITE (KYP) is required for paramutation of sulf and that there is a change in chromatin organization. These findings advance the understanding of non-Mendelian inheritance in plants.

Paramutation involves the transfer of a repressive epigenetic mark from a silent allele to an active homologue and, consequently, non-Mendelian inheritance. In tomato the sulfurea ( sulf ) paramutation is associated with a high level of CHG hypermethylation in a region overlapping the transcription start site of the SlTAB2 gene that affects chlorophyll synthesis. The CCG sub-context hypermethylation is under-represented at this region relative to CTG or CAG implicating the CHROMOMETHYLTRANSFERASE3 (CMT3) in paramutation at this locus. Consistent with this interpretation, loss of CMT 3 function leads to loss of the sulf chlorosis, the associated CHG hypermethylation and paramutation. Loss of KRYPTONITE (KYP) histone methyl transferase function has a similar effect linked to reduced H3K9me2 at the promoter region of SlTAB2 and a shift in higher order chromatin structure at this locus. Mutation of the largest subunit of RNA polymerase V ( PolV ) in contrast does not affect sulf paramutation. These findings indicate the involvement of a CMT3/KYP dependent feedback rather than the PolV-dependent pathway leading to RNA directed DNA methylation (RdDM) in the maintenance of paramutation.

The decision of whether to grow and proliferate or to restrict growth and develop resilience to stress is a key biological trade-off. In plants, constitutive growth results in increased sensitivity to environmental stress^1,2. The underlying mechanisms controlling this decision are however not well understood. We used temperature as a cue to discover regulators of this process in plants, as it both enhances growth and development rates within a specific range and is also a stress at extremes. We found that the conserved chromatin-associated protein DEK plays a central role in balancing the response between growth and arrest in Arabidopsis, and it does this via H2A.Z-nucleosomes. DEK target genes show two distinct categories of chromatin architecture based on the distribution of H2A.Z in +1 nucleosome and gene body, and these predict induction or repression by DEK. We show that these chromatin signatures of DEK target genes are conserved in human cells, suggesting that DEK may act through an evolutionarily conserved mechanism to control the balance between growth and arrest in plants and animals.

Intron splicing increases proteome complexity, promotes RNA stability, and enhances transcription. However, introns and the concomitant need for splicing extend the time required for gene expression and can cause an undesirable delay in the activation of genes. Here, we show that the plant microRNA processing factor SERRATE (SE) plays an unexpected and pivotal role in the regulation of intronless genes. Arabidopsis SE associated with more than 1000, mainly intronless, genes in a transcription-dependent manner. Chromatin-bound SE liaised with paused and elongating polymerase II complexes and promoted their association with intronless target genes. Our results indicate that stress-responsive genes contain no or few introns, which negatively affects their expression strength, but that some genes circumvent this limitation via a novel SE-dependent transcriptional activation mechanism. Transcriptome analysis of a Drosophila mutant defective in ARS2, the metazoan homologue of SE, suggests that SE/ARS2 function in regulating intronless genes might be conserved across kingdoms.