Chromosome-scale assembly uncovers genomic compartmentation of Fusarium oxysporum f. sp. albedinis, the causal agent of Bayoud disease in date palm

Slimane Khayi; Andrew D Armitage; Fatima Gaboun; Issam Meftah-Kadmiri; Rachid Lahlali; Mohamed Fokar; Rachid Mentag

doi:10.3389/fmicb.2023.1268051

Chromosome-scale assembly uncovers genomic compartmentation of Fusarium oxysporum f. sp. albedinis, the causal agent of Bayoud disease in date palm

Front Microbiol. 2023 Oct 11:14:1268051. doi: 10.3389/fmicb.2023.1268051. eCollection 2023.

Authors

Slimane Khayi¹, Andrew D Armitage², Fatima Gaboun¹, Issam Meftah-Kadmiri^{3

4}, Rachid Lahlali^{5

6}, Mohamed Fokar⁷, Rachid Mentag¹

Affiliations

¹ Biotechnology Research Unit, Regional Center of Agricultural Research of Rabat, National Institute of Agricultural Research, Rabat, Morocco.
² Natural Resources Institute, University of Greenwich, Chatham Maritime, Greenwich, United Kingdom.
³ Plant and Microbial Biotechnology Center, Moroccan Foundation of Advanced Science Innovation and Research MAScIR, Ben Guerir, Morocco.
⁴ Plant and Soil Microbiome Sub-Program, AgroBioSciences, Mohammed VI Polytechnic University (UM6P), Ben Guerir, Morocco.
⁵ Phytopathology Unit, Department of Plant Protection, Ecole Nationale D'Agriculture de Meknes, Meknès, Morocco.
⁶ Plant Pathology Laboratory, AgroBioSciences, College of Sustainable Agriculture and Environmental Sciences, Mohammed VI Polytechnic University, Ben Guerir, Morocco.
⁷ Center for Biotechnology and Genomics, Texas Tech University, Lubbock, TX, United States.

Abstract

Date palm (Phoenixdactylifera) is the most significant crop across North Africa and the Middle East. However, the crop faces a severe threat from Bayoud disease caused by the fungal pathogen Fusarium oxysporum f. sp. albedinis (FOA). FOA is a soil-borne fungus that infects the roots and vascular system of date palms, leading to widespread destruction of date palm plantations in North Africa over the last century. This is considered the most devastating pathogen of oasis agriculture in North Africa and responsible for loss of 13 million trees in Algeria and Morocco alone. In this study, we present a chromosome-scale high-quality genome assembly of the virulent isolate Foa 44, which provides valuable insights into understanding the genetic basis of Bayoud disease. The genome assembly consists of 11 chromosomes and 40 unplaced contigs, totalling 65,971,825 base pairs in size. It exhibits a GC ratio of 47.77% and a TE (transposable element) content of 17.30%. Through prediction and annotation, we identified 20,416 protein-coding genes. By combining gene and repeat densities analysis with alignment to Fusarium oxysporum f. sp. lycopersici (FOL) 4287 isolate genome sequence, we determined the core and lineage-specific compartments in Foa 44, shedding light on the genome structure of this pathogen. Furthermore, a phylogenomic analysis based on the 3,292 BUSCOs core genome revealed a distinct clade of FOA isolates within the Fusarium oxysporum species complex (FOSC). Notably, the genealogies of the five identified Secreted In Xylem (SIX) genes (1, 6, 9, 11 and 14) in FOA displayed a polyphyletic pattern, suggesting a horizontal inheritance of these effectors. These findings provide a valuable genomics toolbox for further research aimed at combatting the serious biotic constraints posed by FOA to date palm. This will pave the way for a deeper understanding of Bayoud disease and facilitate the development of effective diagnostic tools and control measures.

Keywords: Phoenix dactylifera; accessory chromosome; effector; genome; lineage specific; pandemic; phylogenomics.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work benefited from support of the Midterm Research Program (2020 to 2024) of INRA-Morocco. AA was supported through Expanding Excellence in England funding awarded to the Natural Resources Institute from UKRI and through the UK North Africa Technical Assistance Facility by arrangement with the British Embassy Rabat.