A hemizygous supergene controls homomorphic and heteromorphic self-incompatibility systems in Oleaceae.

Self-incompatibility (SI) has evolved independently multiple times and prevents self-fertilization in hermaphrodite angiosperms. Several groups of Oleaceae such as jasmines exhibit distylous flowers, with two compatibility groups each associated with a specific floral morph.1 Other Oleaceae species in the olive tribe have two compatibility groups without associated morphological variation.2,3,4,5 The genetic basis of both homomorphic and dimorphic SI systems in Oleaceae is unknown. By comparing genomic sequences of three olive subspecies (Olea europaea) belonging to the two compatibility groups, we first locate the genetic determinants of SI within a 700-kb hemizygous region present only in one compatibility group. We then demonstrate that the homologous hemizygous region also controls distyly in jasmine. Phylogenetic analyses support a common origin of both systems, following a segmental genomic duplication in a common ancestor. Examination of the gene content of the hemizygous region in different jasmine and olive species suggests that the mechanisms determining compatibility groups and floral phenotypes (whether homomorphic or dimorphic) in Oleaceae rely on the presence/absence of two genes involved in gibberellin and brassinosteroid regulation.

Contrasting Genetic Footprints among Saharan Olive Populations: Potential Causes and Conservation Implications.

The Laperrine's olive is endemic to the Saharan Mountains. Adapted to arid environments, it may constitute a valuable genetic resource to improve water-stress tolerance in the cultivated olive. However, limited natural regeneration coupled with human pressures make it locally endangered in Central Sahara. Understanding past population dynamics is thus crucial to define management strategies. Nucleotide sequence diversity was first investigated on five nuclear genes and compared to the Mediterranean and African olives. These data confirm that the Laperrine's olive has a strong affinity with the Mediterranean olive, but it shows lower nucleotide diversity than other continental taxa. To investigate gene flows mediated by seeds and pollen, polymorphisms from nuclear and plastid microsatellites from 383 individuals from four Saharan massifs were analyzed. A higher genetic diversity in Ahaggar (Hoggar, Algeria) suggests that this population has maintained over the long term a larger number of individuals than other massifs. High-to-moderate genetic differentiation between massifs confirms the role of desert barriers in limiting gene flow. Yet contrasting patterns of isolation by distance were observed within massifs, and also between plastid and nuclear markers, stressing the role of local factors (e.g., habitat fragmentation, historical range shift) in seed and pollen dispersal. Implications of these results in the management of the Laperrine's olive genetic resources are discussed.

Paternity tests support a diallelic self-incompatibility system in a wild olive (Olea europaea subsp. laperrinei, Oleaceae).

Self-incompatibility (SI) is the main mechanism that favors outcrossing in plants. By limiting compatible matings, SI interferes in fruit production and breeding of new cultivars. In the Oleeae tribe (Oleaceae), an unusual diallelic SI system (DSI) has been proposed for three distantly related species including the olive (Olea europaea), but empirical evidence has remained controversial for this latter. The olive domestication is a complex process with multiple origins. As a consequence, the mixing of S-alleles from two distinct taxa, the possible artificial selection of self-compatible mutants and the large phenological variation of blooming may constitute obstacles for deciphering SI in olive. Here, we investigate cross-genotype compatibilities in the Saharan wild olive (O. e. subsp. laperrinei). As this taxon was geographically isolated for thousands of years, SI should not be affected by human selection. A population of 37 mature individuals maintained in a collection was investigated. Several embryos per mother were genotyped with microsatellites in order to identify compatible fathers that contributed to fertilization. While the pollination was limited by distance inside the collection, our results strongly support the DSI hypothesis, and all individuals were assigned to two incompatibility groups (G1 and G2). No self-fertilization was observed in our conditions. In contrast, crosses between full or half siblings were frequent (ca. 45%), which is likely due to a nonrandom assortment of related trees in the collection. Finally, implications of our results for orchard management and the conservation of olive genetic resources are discussed.

Coexistence of diploids and triploids in a Saharan relict olive: evidence from nuclear microsatellite and flow cytometry analyses.

Polyploidy was recently reported in two endangered olive subspecies from North-West Africa. The origin of this phenomenon remains unclear. In the present study, 106 genotypes of a relict Laperrine's olive population form Hoggar (Algeria) were analysed using eight nuclear microsatellites. Diploid and triploid genetic profiles were observed. A flow cytometry analysis confirmed that trees displaying three alleles at several loci are effectively triploid. This report constitutes the first evidence for the coexistence of two ploidy types in an olive population. The triploid genotypes, probably in mean more vigorous than diploid trees, may be positively selected in the absence of sexual regeneration since a very long time, explaining their relative high frequency in the investigated population.

Pollen-mediated gene flow in a highly fragmented landscape: consequences for defining a conservation strategy of the relict Laperrine's olive.

In the present central Saharan conditions, the Laperrine's olive regeneration has never been observed and its populations are locally threatened. The production of plants originating from seeds was proposed as a multiplication strategy. In order to determine the impact of sexual reproduction, seeds issued from ten mothers (sampled from four locations in the Hoggar, Algeria) were genotyped using microsatellites. Compared to the initial population, a significant lost of allelic richness was revealed, indicating that our seed sampling was not representative of the local gene diversity. Paternity analyses allowed measurement of the effective pollen-mediated gene flow within patches. Preferential mating between some genotypes was revealed. A trend for a higher multipaternity on seeds collected on trees from relatively large patches was also observed. Lastly, seedlings issued from trees of small patches displayed low growth performance. The implications of our observations in the development of an efficient conservation strategy by seeds are discussed.

High genetic diversity and clonal growth in relict populations of Olea europaea subsp. laperrinei (Oleaceae) from Hoggar, Algeria.

BACKGROUND AND AIMS: The Laperrine's olive (Olea europaea subsp. laperrinei) is an endemic tree from Saharan massifs. Its populations have substantially regressed since the Pleistocene and are presently distributed in a fragmented habitat. Long-term persistence of this taxon is uncertain and programmes of preservation have to be urgently implemented. To define a conservation strategy, the genetic diversity and breeding system of this tree have to be investigated. METHODS: One hundred and eleven ramets were prospected in the laperrinei populations from the Tamanrasset region, southern Algeria. Genetic polymorphism was revealed at nuclear and chloroplast DNA (cpDNA) microsatellite loci allowing a comparative assessment of the genetic diversity of laperrinei and Mediterranean populations based on bi-parental and maternal markers. Additionally, nuclear microsatellite markers enabled the genotypes to be identified unambiguously. KEY RESULTS: Based on nuclear microsatellite data, the total diversity was high (Ht=0.61) in laperrinei populations and similar to that observed in western Mediterranean populations. A substantial cpDNA diversity (Ht=0.19) was also observed. Genetically identical ramets originated from the same stump (which can cover >80 m2) were identified in each population. Sixteen per cent of genets exhibited more than one ramet. In addition, several cases of somatic mutations were unambiguously revealed in distinct ramets stemming from the same stump. CONCLUSIONS: These data show that highly isolated and small laperrinei populations are able to maintain a high genetic diversity. This supports the existence of relict trees persisting for a very long time (probably since the last humid transition, 3000 years ago). It is proposed that the very long persistence associated with an asexual multiplication of highly adapted trees could be a strategy of survival in extreme conditions avoiding a mutational meltdown due to reproduction in reduced populations.