Historical introgressions from a wild relative of modern cassava improved important traits and may be under balancing selection

Authors: WOLFE, MARNIN - Cornell University; BAUCHET, GUILLAUME - Boyce Thompson Institute; CHAN, ARIEL - Cornell University; LOZANO, ROBERTO - Cornell University; RAMU, PUNNA - Cornell University; EGESI, CHIEDOZIE - Cornell University; KAWUKI, ROBERT - National Root Crops Research Institute (NRCRI); KULAKOW, PETER - International Institute Of Tropical Agriculture (IITA); RABBI, ISMAIL - International Institute Of Tropical Agriculture (IITA); Jannink, Jean-Luc

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/15/2019
Publication Date: 12/1/2019
Citation: Wolfe, M.D., Bauchet, G.J., Chan, A.W., Lozano, R., Ramu, P., Egesi, C., Kawuki, R., Kulakow, P., Rabbi, I., Jannink, J. 2019. Historical introgressions from a wild relative of modern cassava improved important traits and may be under balancing selection. Genetics. 213(4):1237-1253. https://doi.org/10.1534/genetics.119.302757.
DOI: https://doi.org/10.1534/genetics.119.302757

Interpretive Summary: Crossing in genes from wild relatives has often been adaptive in plant breeding. However, the significance of historical crosses in modern breeding is often not clear. Cassava (Manihot esculenta) is among the most important staple foods in the world, sustaining hundreds of millions of people in the tropics, especially in sub-Saharan Africa. Widespread genotyping makes cassava a model for clonally propagated root and tuber crops in the developing world, and provides an opportunity to study the modern benefits and consequences of historical crosses with wild relatives. We detected large genome segments from Manihot glaziovii in a collection of 2,742 modern cassava landraces and elite germplasm. These segments came from 1930s era breeding to combat disease epidemics. African landraces and improved varieties had, on average, 3.8% (max 13.6%) ancestry of M. glaziovii. This ancestry accounted for a significant (mean 20%, max 56%) portion of the genetic variation of tested traits. M. glaziovii ancestry on the distal 10 Mb of chr. 1 increased dry matter and root number. On chr. 4, ancestry in a 20 Mb region improved harvest index and brown streak disease tolerance. We observed the M. glaziovii segment on chr. 1 double in frequency over three cycles of selection, but that later stage trials selectively excluded homozygotes from consideration as varieties. This observation indicates a heterozygous advantage of introgressions. We also found that maintaining large recombination-suppressed introgressions in the heterozygous state allowed the accumulation of deleterious mutations. We conclude that targeted recombination of introgressions would increase the efficiency of cassava breeding by allowing simultaneous fixation of beneficial alleles and purging of genetic load.

Technical Abstract: Introgression of alleles from wild relatives has often been adaptive in plant breeding. However, the significance of historical hybridization events in modern breeding is often not clear. Cassava (Manihot esculenta) is among the most important staple foods in the world, sustaining hundreds of millions of people in the tropics, especially in sub-Saharan Africa. Widespread genotyping makes cassava a model for clonally propagated root and tuber crops in the developing world, and provides an opportunity to study the modern benefits and consequences of historical introgression. We detected large introgressed Manihot glaziovii genome-segments in a collection of 2742 modern cassava landraces and elite germplasm, the legacy of a 1930s era breeding to combat disease epidemics. African landraces and improved varieties were, on average, 3.8% (max 13.6%) introgressed. Introgressions accounted for a significant (mean 20%, max 56%) portion of the heritability of tested traits. M. glaziovii alleles on the distal 10 Mb of chr. 1 increased dry matter and root number. On chr. 4, introgressions in a 20 Mb region improved harvest index and brown streak disease tolerance. We observed the introgression frequency on chr. 1 double over three cycles of selection, and that later stage trials selectively excluded homozygotes from consideration as varieties. This indicates a heterozygous advantage of introgressions. However, we also found that maintaining large recombination-suppressed introgressions in the heterozygous state allowed the accumulation of deleterious mutations. We conclude that targeted recombination of introgressions would increase the efficiency of cassava breeding by allowing simultaneous fixation of beneficial alleles and purging of genetic load.