A single polyploidization event at the origin of the tetraploid genome of Coffea arabica is responsible for the extremely low genetic variation in wild and cultivated germplasm

Simone Scalabrin,Timothy Schilling,Mario Cerutti,Manuela Rosanna Ruosi,Gloria Pellegrino,Amin Al Hakimi,Gabriele Magris,Frederica Cattonaro ,Christophe Montagnon,Lorenzo Del Terra,William Solano,Seth C Murray ,Lucile Toniutti,Davide Scaglione,Michèle Morgante ,Gabriele Di Gaspero,Alberto Pallavicini,Giorgio Valle,Nicola Vitulo,Patricia E Klein,Sara Pinosio,F S Liverani ,Michele Vidotto,Nolan Bentley,Luciano Navarini,Irena Jurman,Federica Magni,G Graziosi ,Benoît Bertrand

doi:10.1038/s41598-020-61216-7

Abstract

The genome of the allotetraploid species Coffea arabica L. was sequenced to assemble independently the two component subgenomes (putatively deriving from C. canephora and C. eugenioides) and to perform a genome-wide analysis of the genetic diversity in cultivated coffee germplasm and in wild populations growing in the center of origin of the species. We assembled a total length of 1.536 Gbp, 444 Mb and 527 Mb of which were assigned to the canephora and eugenioides subgenomes, respectively, and predicted 46,562 gene models, 21,254 and 22,888 of which were assigned to the canephora and to the eugeniodes subgenome, respectively. Through a genome-wide SNP genotyping of 736 C. arabica accessions, we analyzed the genetic diversity in the species and its relationship with geographic distribution and historical records. We observed a weak population structure due to low-frequency derived alleles and highly negative values of Taijma’s D, suggesting a recent and severe bottleneck, most likely resulting from a single event of polyploidization, not only for the cultivated germplasm but also for the entire species. This conclusion is strongly supported by forward simulations of mutation accumulation. However, PCA revealed a cline of genetic diversity reflecting a west-to-east geographical distribution from the center of origin in East Africa to the Arabian Peninsula. The extremely low levels of variation observed in the species, as a consequence of the polyploidization event, make the exploitation of diversity within the species for breeding purposes less interesting than in most crop species and stress the need for introgression of new variability from the diploid progenitors.

Highlights

The genome of the allotetraploid species Coffea arabica L. was sequenced to assemble independently the two component subgenomes and to perform a genome-wide analysis of the genetic diversity in cultivated coffee germplasm and in wild populations growing in the center of origin of the species
We generated 38 Gbp of short reads from a C. eugenioides accession, corresponding to a coverage of approximately 54X (Table S1), while raw reads from a C. canephora doubled-haploid accession DH200-9411 corresponding to a 66X coverage were downloaded from the NCBI Sequence Read Archive (SRA)
We found in C. arabica the lowest level of genetic diversity reported so far in crop species (Table S4), only comparable to levels observed for bread wheat, another recent allopolyploid species, and an exceedingly large fraction of private alleles, both to individual accessions as well as to the species in comparison to the progenitor species

Summary

Introduction

The genome of the allotetraploid species Coffea arabica L. was sequenced to assemble independently the two component subgenomes (putatively deriving from C. canephora and C. eugenioides) and to perform a genome-wide analysis of the genetic diversity in cultivated coffee germplasm and in wild populations growing in the center of origin of the species. In the early 20th century, East Africa (today Burundi, Rwanda, DR Congo, Kenya, Tanzania and Uganda) started coffee cultivation and introduced seeds from Yemen, Bourbon, Typica and Indian varieties and very few Ethiopian landraces, which leaked from Ethiopia in the pockets of travelers (Geisha and Rume Sudan for instance). This strategy resulted into the first public draft genome of C. arabica L. that enabled us to undertake the first GBS approach for polymorphism detection on C. arabica accessions and its parental species This allowed us to (i) confirm the geographical structure of the genetic diversity of C. arabica which originated after a single event of polyplodization that gave rise to the species and was partly shaped by early movements of planting material, (ii) detect sources of diversity for coffee breeding and (iii) understand the relatedness between the canephora subgenome of C. arabica and the modern diploid C. canephora, some of which are used for the production of Robusta coffee beans

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Conclusion