Chromosome-scale assembly reveals asymmetric paleo-subgenome evolution and targets for the acceleration of fungal resistance breeding in the nut crop, pecan.

ABSTRACT

Pecan (Carya illinoinensis) is a tree nut crop of worldwide economic importance that is rich in health-promoting factors. However, pecan production and nut quality are greatly challenged by environmental stresses such as the outbreak of severe fungal diseases. Here, we report a high-quality, chromosome-scale genome assembly of the controlled-cross pecan cultivar 'Pawnee' constructed by integrating Nanopore sequencing and Hi-C technologies. Phylogenetic and evolutionary analyses reveal two whole-genome duplication (WGD) events and two paleo-subgenomes in pecan and walnut. Time estimates suggest that the recent WGD event and considerable genome rearrangements in pecan and walnut account for expansions in genome size and chromosome number after the divergence from bayberry. The two paleo-subgenomes differ in size and protein-coding gene sets. They exhibit uneven ancient gene loss, asymmetrical distribution of transposable elements (especially LTR/Copia and LTR/Gypsy), and expansions in transcription factor families (such as the extreme pecan-specific expansion in the far-red impaired response 1 family), which are likely to reflect the long evolutionary history of species in the Juglandaceae. A whole-genome scan of resequencing data from 86 pecan scab-associated core accessions identified 47 chromosome regions containing 185 putative candidate genes. Significant changes were detected in the expression of candidate genes associated with the chitin response pathway under chitin treatment in the scab-resistant and scab-susceptible cultivars 'Excell' and 'Pawnee'. These findings enable us to identify key genes that may be important susceptibility factors for fungal diseases in pecan. The high-quality sequences are valuable resources for pecan breeders and will provide a foundation for the production and quality improvement of tree nut crops.