Resistance breeding offers invaluable perspectives for environment-friendly crop protection, but its success may be limited by the breakdown of plant resistance by pathogen strains. With the breeding and use of varieties carrying multiple genetic resistances, grapevine (Vitis spp.) represents a distinctive model for perennials to investigate the agreement that pyramiding broadens and enhances the efficacy and durability of resistance. To this end, grapevine progenies segregating for four major resistance loci against Plasmopara viticola (Rpvs) were used to evaluate single and pyramided loci when confronted with naive and Rpv-breaking pathogen strains. In pyramiding, undefeated and defeated Rpvs provided either beneficial, neutral, or detrimental quantitative effects, depending on the loci combination and pathogen strain. In particular, the fact that defeated loci may compromise resistance highlighted important implications for the breeding of perennials. Thorough phenotypic investigations of pyramiding schemes emerge as a critical step for the effective and durable management of genetic resistances.

How selection and demography jointly shape the genomes of perennial crops remains an open question. Apple (M. domestica) is a compelling system because its domestication involved multiple wild progenitors and post-domestication admixture across Eurasia. We integrate 218 whole genomes (68 cultivated dessert/cider; 150 wild: M. sieversii, M. orientalis, M. sylvestris), RNA sequencing (RNA-seq), and a genome-wide association study of flowering time to resolve how these forces shaped the cultivated apple genome. Despite weak neutral differentiation and widespread admixture, dessert and cider apples form distinct gene pools that derive primarily from M. sieversii-M. orientalis rather than European M. sylvestris. We find no evidence of a domestication bottleneck, as expected in perennials. Demographic-aware selection scans reveal non-overlapping targets supported by RNA-seq; dessert shows more hard sweeps at fruit quality, disease resistance, and flowering genes, whereas cider shows proportionally more soft sweeps and balancing selection. Wild-to-crop introgression from M. sylvestris is extensive but heterogeneous; some introgressed tracts concentrate in hard-sweep regions and approach fixation (consistent with rapid, targeted uptake), whereas others persist at intermediate frequencies with soft-sweep signatures (consistent with diffuse, recurrent introgression of adaptive alleles). The lead chromosome 9 flowering-time association lies within an introgressed segment near a transposable element and is separated from sweep peaks, consistent with regulatory/polygenic control. Cultivated apples carry a lower deleterious load than wild relatives. These results provide a comprehensive genomic portrait of perennial fruit tree domestication, clarifying how selection and adaptive introgression shaped the cultivated apple genome and yielding actionable targets for breeding and conservation.

We focus on the evolution of behavioral sexual isolation through the empirical study of two marine isopod species. The males of Jaera albifrons and Jaera praehirsuta engage females in tactile courtship by brushing the female's back, but they do so with divergent sets of specialized setae, and female choice results in strong reproductive isolation. Using RADseq-derived genotypes of individuals from natural populations and controlled crosses, we found that secondary contacts between J. albifrons and J. praehirsuta resulted in different levels of heterospecific gene flow. Comparison of the genomic landscapes of differentiation in the two most contrasted situations (extremely low heterospecific gene flow in one geographic region, but strong introgressive hybridization in another) allowed us to conclude that genomic regions resistant to interspecies gene flow are primarily located on the sex chromosomes or on rearranged chromosomes (several fusion-scissions and one reciprocal translocation). These genomic regions show low recombination, and in two cases quantitative trait locus analyses found genetic variation associated with male courtship traits. These results suggest that a period of allopatry may have allowed the divergent coevolution of male traits and female preferences, with genetic bases located at least in part in nonrecombining regions on sex chromosomes and rearranged chromosomes.

In this study, we demonstrate that Vitis cryptic virus (VCV), one of the many viruses that infect grapevines, is transmitted by both gametes. Regardless of the infected parent being used as the male or female virus source in crosses, VCV was detected in all eight interspecific progenies tested. Interestingly, except for a single mutation, all VCV sequences obtained from the different hybrids display 100% identity to either RNA1 or RNA2 in the parental vines. In addition, we confirmed a close relationship between the virus and wild Vitis species from Asia or the Americas, where the virus has been originally characterized and reported by transcriptomic datamining. Following a phylogenetic analysis, we identified clustering of sequences underlining a potential co-evolution pattern between some VCV genotypes and specific Vitis subspecies.

Abstract The sugar kelp Saccharina latissima is a promising candidate for sustainable aquaculture in the North Atlantic and North-East Pacific but genetic improvement has been hindered by limited understanding of the genetic basis of economically important traits. We conducted the first genome-wide association study (GWAS) for this species using 202 self-fertilised pseudo-F1 individuals derived from 12 populations spanning northern and southern European genetic clusters. Individuals were genotyped with ddRAD-seq-derived SNP markers and phenotyped in a common garden experiment for four morphological traits (blade length, blade width, blade area, stipe length) and six metabolic traits related to nitrogen metabolism. We identified 26 significant marker-trait associations, with phenotypic variance explained (PVE) ranging from 0.65% to 52.44%. Major-effect loci were detected for blade width (52.44% PVE) and blade area (45.22% PVE) and a locus on chromosome 17 influenced both blade length and blade area. Marker-based heritability estimates ranged from 0.75 to 0.99 for morphological traits and from 0.00 to 0.99 for metabolic traits, though with large standard errors. Cross-validation of genomic selection models yielded predictive abilities of 0.21-0.59 across traits. Our findings reveal a mixed genetic architecture with major-effect loci suitable for marker-assisted selection and polygenic traits amenable to genomic selection, providing a foundation for genomics-assisted breeding programs in kelp aquaculture.

- Perennial crops can respond to climate change through phenotypic plasticity and genetic adaptation, yet how these processes interact and are shaped by domestication and population history remains poorly understood in long-lived species. - We combined controlled reciprocal climate experiments with phenotypic, transcriptomic, and genomic analyses in cultivated apple (Malus domestica) and its wild relatives. We grew 1,248 seedlings from four wild apple populations under four simulated European climates alongside M. domestica. Early survival and twelve phenotypic traits were quantified, and gene expression was analyzed in 96 individuals using RNA sequencing, together with DNA sequencing from a previous study. - Early seedling survival revealed strong population-specific responses to climate. Phenotypic and transcriptional responses to climate were widespread and largely conserved, with a core set of climate-responsive genes enriched for stress- and nutrient-related functions and evolving under strong purifying selection. Population-specific regulatory responses were limited and largely reflected genetic divergence. Domestication was associated with altered expression patterns and reduced deleterious mutation load. - These results show that climate responses in apple seedlings reflect a balance between conserved plastic responses and population-specific genetic constraints shaped by evolutionary history and domestication, with implications for predicting climate resilience in perennial crops. ### Competing Interest Statement The authors have declared no competing interest. European Agricultural Fund for Rural Development, RIDF190219CR0110026 New York University Abu Dhabi, Tamkeen, Grant AD 454 Agence Nationale de la Recherche, ANR-21-CE20-0005, ANR-10-EQPX-13-01, ANR-11-INBS-0001 Conseil Régional d'Île-de-France, I-05-098/R, 2011-11017735, 2015-1657 Ministère de l’Enseignement Supérieur et de la Recherche, https://ror.org/03sjk9a61, D23-ET006 Ministerul Cercetării și Inovării, 88-PHE, PN23020401/7N/03.01.2023, PN-IV-P8-8.1-PRE-HE-ORG-2024-0223 Centre National de la Recherche Scientifique, ATIP-Avenir 2019-2021

Climate change and intensifying disease pressure push viticulture beyond incremental adaptation, especially where grape production depends on repeated pesticide applications. Reducing chemical inputs requires an integrated strategy combining broader genetic diversity, conventional and genomic-assisted breeding, new genomic techniques, somaclonal and clonal variation, and cultivar-tailored IPM. The Horizon Europe projects Shield4Grape and GrapeBreed4IPM operationalize this vision across genetics, agronomy, socioeconomics, and policy, with success depending on governance, stewardship, and proportionate regulation.

Esca is the most destructive and predominant grapevine trunk disease. The chronic infections and vine mortality caused by esca syndrome lead to huge economic losses and threaten the sustainability of vineyards worldwide. Esca is caused by numerous wood-decay and wood-decay-associated fungi, but its full etiology remains unclear due to the grapevine trunk disease complex, making effective control methods challenging. As differences in esca susceptibility have already been observed among grapevine varieties, we investigated the presence of genetic factors that can explain these variations using a Riesling × Gewurztraminer progeny. Thanks to the destructive phenotyping of a 16-year-old vineyard plot, we discovered that the Gewurztraminer variety carries on chromosome 1 a locus linked to variations in trunk necrosis associated with esca, which we have named Esca Necrosis Susceptibility 1 (ENS1). Our study also suggests that there is a partial link between trunk vigor and necrosis due to esca. To our best knowledge, ENS1 is the first instance of the genetic factor identified as involved in the limitation of necrosis associated with grapevine esca. While the identification of ENS1 alone may not provide a complete resolution of the issue, this discovery nonetheless represents a first step toward a genetic solution and paves the way for broader genetic investigations in the future.

The current genetic model explaining berry skin color in Vitis vinifera is incomplete and fails to predict berry skin color phenotypes for one allele of VvMybA1, referred to as VvMybA1_SUB. Our study focuses on this specific allele, revealing that the haplotype containing VvMybA1_SUB (haplotype F) represents an ancient lineage of the berry color locus. Within haplotype F, we identified two functional subhaplotypes, HapF1 and HapF2, associated with black-skinned phenotype, and one non-functional subhaplotype, HapFDEL, responsible for white-skinned phenotype. HapF1 likely originated from wild populations domesticated in the Near East and subsequently spread globally with the expansion of viticulture. In contrast, HapF2 has a more restricted distribution and may have emerged from hybridization events between cultivated grapevines and local wild populations as viticulture migrated to the Italian peninsula. Furthermore, we found that in white-skinned berry cultivar, HapF has undergone a large deletion at the berry color locus, removing the majority of the VvMybA genes. Previous works suggested a single common origin for white-skinned varieties during grapevine domestication. Our results challenge this notion, instead proposing that white-skinned grape cultivars arose at least twice during grapevine domestication history. Alongside the major haplotype A, some white-skinned cultivars, such as cv. ‘Sultanina’ harbor HapFDEL. Since HapFDEL is present only in table grape varieties, we suggest that it likely arose from a recent mutational event and dispersed along the ancient Silk Road into East Asia. These findings enhance our understanding of the genetic diversity and evolutionary trajectory of grapevine cultivars, offering insights into their domestication and spread across different geographical regions.

### Competing Interest Statement The authors have declared no competing interest.

Resistance breeding offers invaluable perspectives for environment-friendly crop protection, but its success may be limited by the breakdown of plant resistance by pathogen strains. This threat is particularly acute for perennial crops, which may be cultivated for several decades. With the increasing use of new varieties carrying multiple major resistance loci, grapevine ( Vitis spp.) represents a distinctive model to investigate the broad agreement that combining several resistance genes (pyramiding) enhances both resistance efficacy and durability. To this end, grapevine progenies segregating for four resistance loci against Plasmopara viticola ( Rpvs ) were used to evaluate the efficiency of single and pyramided major loci when confronted to naive and Rpv -breaking pathogen strains. In the context of polygenic resistance, both undefeated and defeated Rpvs provided significant quantitative effects. However, interactions between pyramided Rpvs were either beneficial, neutral or detrimental to the level of resistance, depending on the loci combination and pathogen strain. In particular, the fact that the presence of defeated resistance loci may compromise the resistance provided by functional major loci has important implications for crops resistance breeding. Thorough phenotypic investigations of pyramiding breeding schemes emerge as a critical step for the effective and durable management of genetic resistances and plant diseases. ### Competing Interest Statement The authors have declared no competing interest. Agence Nationale de la RechercheAgence Nationale de la Recherche, https://ror.org/00rbzpz17, ANR-22-CE92-0005 Deutsche ForschungsgemeinschaftDeutsche Forschungsgemeinschaft, , 504993256

Saccharina latissima is an important species for the emerging seaweed aquaculture industry in the northern Atlantic. In this study, genotype and phenotype data for a segregating F2 family was used to generate a high-density genetic map for S. latissima and to identify temperature-stress-related quantitative trait loci (QTLs). A temperature stress experiment detected distinct phenotypic classes with different stress responses within the F2 family and these phenotypic classes were shown to exhibit different transcriptomic responses to heat stress. The existence of heat tolerant, resilient and sensitive individuals within this segregating family indicates that it should be possible to breed temperature tolerant strains of S. latissima. This conclusion was supported by the identification of three QTLs that influenced recovery after temperature stress. The results of this study and the resources generated, in particular the high-density genetic map, represent an important foundation for future S. latissima breeding programs.

European viticulture faces two critical challenges currently: climate change and its direct and indirect impacts in the one hand and the need to dramatically reduce pesticide use in the other hand. In response, breeding programs, such as the INRAE-ResDur program, have prioritized the development of grapevine varieties with disease resistance and improved adaptability to climate change. We took the opportunity of the important plant material produced during the INRAE-ResDur program over twenty years to dissect the genetic basis of key agronomic traits using a comprehensive approach. We conducted genome-wide association studies (GWAS) modeling both additive and non-additive genetic effects, alongside classical QTL mapping and a meta-GWAS that integrates data across multiple environments and pleiotropic effects. These analyses identified numerous loci associated with important traits related to yield, phenology, and stress tolerance. Notably, several loci showed significant genotype-by-environment (GxE) interactions, while others showed pleiotropic effects influencing multiple traits. Overall, 39 genomic regions were detected in QTL analysis in biparental populations, GWAS with additive and non-additive effects, and meta-GWAs analysis, accounting for the 13 agronomic traits. These results provide valuable molecular markers that can be applied in marker-assisted selection or knowledge-assisted genomic selection. This study highlights a complex polygenic architecture underlying agronomic traits in grapevine, involving multiple loci with both additive and interaction effects and underscores the need for integrative breeding strategies to achieve sustainable improvements in future viticulture. ### Competing Interest Statement The authors have declared no competing interest. INRAE BAP division, IB2022_SelGen-ResDur, IVD4 ResGrape CASDAR FranceAgriMer, ViRéVATE, INNOVRES OIV research grant, PhD thesis of Clémentine Borrelli CTNSP

The integration of genetic values in ecophysiological models for phenological stages allows us to predict the effect of loci in future conditions. Modern grapevine (Vitis vinifera L.) breeding programs aim to create new varieties resistant to biotic and abiotic stresses, simultaneously. Developmental stages may affect many physiological processes in grapevine, especially berry composition. The shifts of phenological stages observed in the context of climate change challenge the selection of new varieties. In this paper, we evaluate how genotypes derived from a breeding program aimed at developing disease-resistant varieties may adapt to future climatic conditions. Specifically, we examine the genetic variability of three key phenological periods (February 15 to budbreak, budbreak to flowering, and flowering to véraison) using an ecophysiological model based on thermal requirements. Using high-density genetic information, we identified more than 18 quantitative trait loci for three phenological periods. By combining relevant allelic effects, we virtually constructed both an early and late composite genotype and evaluated their potential adaptation to future climatic conditions, using the greenhouse gas IPCC emissions scenario RCP 8.5 and simulated meteorological data at a local scale. While the early composite genotype may not outperform V. vinifera cv. Chardonnay under these projected conditions, the late composite genotype appears to remain suitably adapted through at least 2060. Our approach enables the prediction of allele-specific advantages on phenological stages across a range of future climate scenarios.

Accelerating grapevine breeding for disease resistance and climate adaptation remains a major challenge due to long generation cycles. We conducted a comprehensive benchmarking of genomic (SNP), phenomic (FT-NIR), and metabolomic (untargeted LC-MS) prediction models across multiple traits in a biparental grapevine population phenotyped over three years. Seven statistical frameworks and four tissue x timepoint strategies (wood; vineyard leaves at budbreak and flowering; greenhouse leaves at flowering) were assessed for predictive performance. Cross-year and cross-population scenarios, involving two additional biparental populations, evaluated model robustness and transferability. Genomic prediction consistently yielded the highest accuracies (up to r = 0.80), with rrBLUP outperforming other models. Metabolomic models achieved intermediate accuracies and, in some cases matched genomic predictions, while phenomic models, though less accurate, provided a cost-effective option for early selection. Heritability analyses showed that metabolomic features were more genetically determined than NIR traits, which were highly sensitive to environmental variation. Integrating omic layers led to limited improvement, except in a few traits where genomic-metabolomic models provided modest gains. Prediction accuracy declined in across-population transfers, underscoring the importance of genetic relatedness. We propose a tiered selection strategy combining low-cost phenomic or metabolomic pre-screening under controlled conditions with genomic selection in advanced lines to accelerate the development of resilient grapevine cultivars. ### Competing Interest Statement The authors have declared no competing interest. INRAE BAP division, IB\_2023\_MetabOptimum, PhD thesis grant OIV research grant, PhD thesis of Clémentine Borrelli

Research on the biology and evolution of sex chromosomes has primarily focused on diploid XX/XY and ZW/ZZ systems. In contrast, the rise, evolution and demise of U/V systems has remained an enigma. Here we analyse genomes of nine brown algal species with different sexual systems to determine the history of their sex determination. U/V sex chromosomes emerged between 450 and 224 million years ago, when a region containing the pivotal male-determinant MIN ceased recombining. Seven ancestral genes within the sex-determining region show remarkable conservation over this vast evolutionary time, although nested inversions caused expansions of the sex locus, independently in each lineage. We evaluate whether these expansions are associated with increased morphological complexity and sexual differentiation, and show that taxonomically restricted genes evolve unexpectedly often in U and V chromosomes. We also investigate two situations in which U/V-linked regions have changed. First, we demonstrate that convergent evolution of two monoicous species occurred by ancestral males acquiring U-specific genes. Second, the Fucus dioecious system involves new sex-determining gene(s), acting upstream of formerly V-specific genes during development. Both situations have led to the demise of U and V chromosomes and erosion of their specific genomic characteristics.

Societal Impact Statement Widespread adoption of disease‐resistant grapevine varieties presents a significant opportunity to revolutionize viticulture and address pressing environmental concerns. By reducing reliance on chemical pesticides, these varieties align with the European Commission's Green Deal objectives, striving for sustainable agricultural practices. Despite initial hesitancy among winegrowers and consumers, shifting attitudes towards sustainability and environmental consciousness are fostering increased acceptance of these varieties. As the market evolves, coupled with supportive policy measures for adoption, disease‐resistant vines are poised to significantly expand their presence in European vineyards. This transition not only mitigates environmental impact but also ensures the long‐term viability and resilience of viticulture. Summary Sustainable agriculture and most prominently the reduction of pesticides is one of the main goals of the European Unions (EU) agricultural policy. As viticulture uses around 70% of the fungicides in the EU, there is substantial pressure on winemakers to reduce their pesticide input. On top of the political goal, winegrowers face increased pressure from the public demanding a more sustainable production of wine. Since the introduction of downy mildew, powdery mildew, and other pests and pathogens from North America to Europe in the 19th century, substantial breeding efforts were undertaken to develop disease‐resistant varieties and reduce the amount of plant protection products needed for harvesting healthy grapes. Today's winegrowers in Europe can choose from many new varieties, allowing them to reduce fungicide input by 50–80% and produce high‐quality wines on par with the valued traditional cultivars. This review will provide an overview on the current situation of disease‐resistant varieties in European viticulture. Selected breeding institutions and private breeders will be introduced, and their most important grapevine varieties presented. Many resistant varieties are available for winegrowers today, however, even the most robust new varieties will not lead to a more sustainable viticulture if the market does not accept them. The adoption and acceptance of new varieties by winegrowers and consumers is still rather low, but the interest in these varieties is rapidly growing. The production of grafted vines of disease‐resistant grapevine varieties allows the estimation that the area of disease‐resistant varieties will significantly grow in the next years.

How selection and demography shape genomes of long-lived crops remains largely unresolved. Using apple ( Malus domestica ) as a model, we integrate 218 whole genomes (68 cultivated dessert/cider; 150 wild: M. sieversii, M. orientalis, M. sylvestris ), RNA-seq, and a flowering-time GWAS to resolve how these forces forged the cultivated apple genome. Despite weak neutral differentiation and widespread admixture, dessert and cider apples form distinct gene pools that derive primarily from M. sieversii–M. orientalis rather than European M. sylvestris . We find no evidence of a strong domestication bottleneck, as expected in perennials. Demography-aware selection scans reveal largely non-overlapping targets: dessert shows more hard sweeps at genes linked to fruit quality, disease resistance, and flowering, whereas cider shows proportionally more soft sweeps and balancing selection; RNA-seq differential expression supports these candidates. Wild-to-crop introgression from M. sylvestris is extensive but heterogeneous by context: some introgressed tracts concentrate in hard-sweep regions and approach fixation (consistent with rapid, targeted uptake), whereas others persist at intermediate frequencies with soft-sweep signatures (consistent with diffuse, recurrent introgression of adaptive alleles). Extending to the phenotype, the lead chromosome 9 flowering-time association lies within an introgressed segment near a transposable element and is separated from sweep peaks, consistent with regulatory/polygenic control. Cultivated apples carry a lower predicted deleterious load than wild relatives. Together, these results provide one of the most comprehensive population genomic portraits of a perennial fruit tree domestication, clarifying how selection and adaptive introgression jointly shaped the cultivated apple genome architecture and yielding actionable targets for breeding and conservation. Significance statement Perennial crops are underexplored compared to annuals, leaving open the question of how selection, gene flow, and demography shape their genomes. Using the apple tree ( Malus domestica ), we analyzed 218 genomes, along with expression and trait data. Despite weak genome-wide differences, dessert and cider apples form distinct gene pools. Widespread gene flow from the European wild apple supplied adaptive alleles, with contrasting dynamics: in cider, a few introgressed DNA segments rose rapidly; in dessert, many variants shifted gradually. Cultivated apples also carry a lower predicted burden of harmful mutations than wild relatives. Together, these results redefine perennial domestication and pinpoint genomic targets to accelerate breeding and conservation. ### Competing Interest Statement The authors have declared no competing interest. Inserm, ATIP-CNRS IDEEV LabEx BASC Tamkeen, under the New York University, Abu Dhabi Research Institute grant AD, 454 European LEADER, 1.1.359 Proverbio PLEASURE, ANR-21-CE20-0005 Ministry of Research, Innovation and Digitization, CNCS/CCCDI-UEFISCDI, PN-IV-P8-8.1-PRE-HE-ORG-2024-0223, within PNCDI IV

Parallel clines in traits related to adaptation in a species can be due to independent selection on a pair of traits, or due to selection in one trait resulting in a parallel cline in a correlated trait. To distinguish between the mechanisms giving rise to parallel adaptive population divergence of multiple traits along an environmental gradient we need to study variation, correlations, and selective forces within individual populations along the gradient. In many tree species, budset timing (BST) forms a latitudinal cline, and parallel clinal variation is also found in other seedling traits, such as first-year height (FYH) and fall frost injury (FFI). In this study, we set up a common garden experiment with open pollinated progeny from natural populations of Scots pine (Pinus sylvestris), with one large sample from single population (500 families) and smaller samples from across a latitudinal gradient. BST, FYH and induced FFI were first measured in a greenhouse. The seedlings were then planted in the field, where survival and height were measured at the age of 9 years as fitness proxies. We compared between- and within-population variation and genetic correlations of these three seedling traits, and estimated selection gradients at the family level in our main population, taking into account the potential effects of seed weight. Between-population genetic correlations between seedling traits were high (0.76-0.95). Within-population genetic correlations in the main population were lower (0.14-0.35), as in other populations (0.10-0.39). Within population, extensive adaptive variation persists in the seedling traits, in line with rather weak selection gradients, yet maintaining the clines. Although our sampling does not cover the whole cline equally, the results suggest that the individual clines in these traits are maintained by largely independently acting selection, which results in fewer constraints in adaptation under changing climate.