1. More severe seasonal stresses resulting from climate change affect the survival of perennial plant species. The growth-survival trade-off exemplified in dormant species is a key issue to understand adaptation. As the validity of this trade-off has yet to be tested in non-dormant species, it was assessed by exploring the intraspecific variability of strategies to face drought and frost within perennial ryegrass. 2. Three common gardens compared 385 European perennial ryegrass populations along a latitudinal environmental gradient over 3-years. Persistence, productivity and physiological traits were recorded under contrasting seasonal environments. 3. Decoupling plant responses, that is, growth under favourable summers/winters and plant survival under harsh summers/winters, showed a general trade-off between growth potential and dehydration survival. Three groups of perennial ryegrass populations were identified according to their contrasting strategies: (a) year-round productive but stress sensitive populations from wet areas; (b) drought-tolerant populations with low summer growth potential from drought-prone areas and (c) frost-tolerant populations with low winter growth potential from frost-prone areas. Overall, the populations surviving drought best were more resource conservative, whereas populations of the other groups were more resource acquisitive. However, such overall functional patterns were less meaningful than seasonal variations of resource acquisition potentials. The predicted potential biogeographical distribution of these groups suggests shifts of areas of suitability under climate change over the next decades in Europe. Dehydration escape and dehydration tolerance through reduction of growth potential in summer may become the strategies best adapted to an increasingly large area of Europe. 4. The large intraspecific variability of phenological adaptations within perennial ryegrass reveals that the seasonal modulation of growth potential is crucial to plant adaptation under severe chronic abiotic stresses. The global plant economics spectrum cannot account for contrasting seasonal trade-offs, which points out the importance of integrating phenological traits as key components of plant strategies. The identification of the trade-off between growth potential and frost or drought stress survival in this non-dormant species provides key knowledge to understand the future regional distribution of this major species for grassland ecosystem services.

BACKGROUND AND AIMS:The persistence of a plant population under a specific local climatic regime requires phenotypic adaptation with underlying particular combinations of alleles at adaptive loci. The level of allele diversity at adaptive loci within a natural plant population conditions its potential to evolve, notably towards adaptation to a change in climate. Investigating the environmental factors that contribute to the maintenance of adaptive diversity in populations is thus worthwhile. Within-population allele diversity at adaptive loci can be partly driven by the mean climate at the population site but also by its temporal variability.METHODS:The effects of climate temporal mean and variability on within-population allele diversity at putatively adaptive quantitative trait loci (QTLs) were evaluated using 385 natural populations of Lolium perenne (perennial ryegrass) collected right across Europe. For seven adaptive traits related to reproductive phenology and vegetative potential growth seasonality, the average within-population allele diversity at major QTLs (HeA) was computed.KEY RESULTS:Significant relationships were found between HeA of these traits and the temporal mean and variability of the local climate. These relationships were consistent with functional ecology theory.CONCLUSIONS:Results indicated that temporal variability of local climate has likely led to fluctuating directional selection, which has contributed to the maintenance of allele diversity at adaptive loci and thus potential for further adaptation.

Climate change is leading to more intense and more frequent water stress. Since existing forage varieties tend to do best under favourable conditions, new forage varieties are needed. A better understanding of a) the natural diversity of forage species within their distribution ranges and b) the genetics underlying different adaptation strategies could facilitate the creation of a range of varieties that combine sufficient yield with different levels of water stress resistance (growth maintenance) or tolerance (arrested growth and survival). It appears especially important to select for phenological traits (and therefore seasonal growth rates) that better correspond to climatic constraints. In an increasingly changing environment, species mixtures often allow for greater production stability. The attributes of the varieties in the mixture play an essential role in maintaining the balance among species. That said, it is still early days for methods that improve plant varieties with a view to increasing blend performance while maintaining species balance.

Germplasm from perennial ryegrass (Lolium perenne L.) natural populations is useful for breeding because of its adaptation to a wide range of climates. Climate-adaptive genes can be detected from associations between genotype, phenotype and climate but an integrated framework for the analysis of these three sources of information is lacking. We used two approaches to identify adaptive loci in perennial ryegrass and their effect on phenotypic traits. First, we combined Genome-Environment Association (GEA) and GWAS analyses. Then, we implemented a new test based on a Canonical Correlation Analysis (CANCOR) to detect adaptive loci. Furthermore, we improved the previous perennial ryegrass gene set by de novo gene prediction and functional annotation of 39,967 genes. GEA-GWAS revealed eight outlier loci associated with both environmental variables and phenotypic traits. CANCOR retrieved 633 outlier loci associated with two climatic gradients, characterized by cold-dry winter versus mild-wet winter and long rainy season versus long summer, and pointed out traits putatively conferring adaptation at the extremes of these gradients. Our CANCOR test also revealed the presence of both polygenic and oligogenic climatic adaptations. Our gene annotation revealed that 374 of the CANCOR outlier loci were positioned within or close to a gene. Co-association networks of outlier loci revealed a potential utility of CANCOR for investigating the interaction of genes involved in polygenic adaptations. The CANCOR test provides an integrated framework to analyse adaptive genomic diversity and phenotypic responses to environmental selection pressures that could be used to facilitate the adaptation of plant species to climate change.

The natural genetic diversity of agricultural species is an essential genetic resource for breeding programs aiming to improve their ecosystem and production services. A large natural ecotype diversity is usually available for most grassland species. This could be used to recombine natural climatic adaptations and agronomic value to create improved populations of grassland species adapted to future regional climates. However describing natural genetic resources can be long and costly. Molecular markers may provide useful information to help this task. This opportunity was investigated for Lolium perenne L., using a set of 385 accessions from the natural diversity of this species collected right across Europe and provided by genebanks of several countries. For each of these populations, genotyping provided the allele frequencies of 189,781 SNP markers. GWAS were implemented for over 30 agronomic and/or putatively adaptive traits recorded in three climatically contrasted locations (France, Belgium, Germany). Significant associations were detected for hundreds of markers despite a strong confounding effect of the genetic background; most of them pertained to phenology traits. It is likely that genetic variability in these traits has had an important contribution to environmental adaptation and ecotype differentiation. Genomic prediction models calibrated using natural diversity were found to be highly effective to describe natural populations for almost all traits as well as commercial synthetic populations for some important traits such as disease resistance, spring growth or phenological traits. These results will certainly be valuable information to help the use of natural genetic resources of other species.