The recent evolutionary rescue of a staple crop depended on over half a century of global germplasm exchange

Authors: MULETA, KEBEDE - Kansas State University; FELDERHOFF, TERRY - Kansas State University; WINANS, NOAH - Kansas State University; WALSTEAD, RACHEL - Hudsonalpha Institute For Biotechnology; CHARLES, JEAN - Quisqueya University; Armstrong, John; MAMIDI, SUJAN - Hudsonalpha Institute For Biotechnology; PLOTT, CHRIS - Hudsonalpha Institute For Biotechnology; VOGEL, JOHN - Lawrence Berkeley National Laboratory; LEMAUX, PEGGY - University Of California Berkeley; MOCKLER, TODD - Danforth Plant Science Center; GRIMWOOD, JANE - Hudsonalpha Institute For Biotechnology; SCHMUTZ, JEREMY - Hudsonalpha Institute For Biotechnology; PRESSOIR, GAEL - Quisqueya University; MORRIS, GEOFFREY - Colorad0 State University

Submitted to: Science Advances
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/22/2021
Publication Date: 2/9/2022
Citation: Muleta, K.T., Felderhoff, T., Winans, N., Walstead, R., Charles, J.R., Armstrong, J.S., Mamidi, S., Plott, C., Vogel, J.P., Lemaux, P.G., Mockler, T., Grimwood, J., Schmutz, J., Pressoir, G., Morris, G.P. 2022. The recent evolutionary rescue of a staple crop depended on over half a century of global germplasm exchange. Science Advances. 8. Article eabj4633.

Interpretive Summary: Rapid environmental change can lead to extinction of populations, or evolutionary rescue via genetic adaptation. In the past several years, smallholder and commercial cultivation of sorghum (Sorghum bicolor), a global cereal and forage crop, has been threatened by a global outbreak of an aggressive new biotype of sugarcane aphid (SCA; Melanaphis sacchari). Here we characterized genomic signatures of adaptation to SCA in a Haitian sorghum breeding population, which had been recently founded from admixed global germplasm, extensively intercrossed, and subjected to intense selection under SCA infestation. We conducted evolutionary population genomics analyses of 296 post-selection Haitian lines compared to 767 global accessions at 159,683 single nucleotide polymorphisms. Despite intense selection, the Haitian population retains high nucleotide diversity (p) through much of the genome due to its diverse founders and the intercrossing strategy. A genome-wide fixation (FST) scan suggests that adaptation to SCA in the Haitian population is conferred by a selective sweep for a globally rare East African allele of RMES1. De novo genome sequencing of a key African founder of the Haitian population revealed putative causative variants for SCA resistance. Convenient low-cost markers were developed from the RMES1 selective sweep and successfully predicted resistance in independent U.S. × African breeding lines and eight U.S. commercial and public breeding programs, demonstrating the global relevance of the findings. Together, the findings highlight the potential of evolutionary genomics to develop adaptive trait breeding technology and the importance of global germplasm exchange to facilitate evolutionary rescue.

Technical Abstract: Rapid environmental change can lead to population extinction or evolutionary rescue. The global staple crop sorghum (Sorghum bicolor) has recently been threatened by a global outbreak of an aggressive new biotype of sugarcane aphid (SCA; Melanaphis sacchari). We characterized genomic signatures of adaptation in a Haitian breeding population that had rapidly adapted to SCA infestation, conducting evolutionary population genomics analyses on 296 Haitian lines versus 767 global accessions. Genome scans and geographic analyses suggest that SCA adaptation has been conferred by a globally rare East African allele of RMES1, which spread to breeding programs in Africa, Asia, and the Americas. De novo genome sequencing revealed potential causative variants at RMES1. Markers developed from the RMES1 sweep predicted resistance in eight independent commercial and public breeding programs. These findings demonstrate the value of evolutionary genomics to develop adaptive trait technology and highlight the benefits of global germplasm exchange to facilitate evolutionary rescue.