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Domestication Reshaped the Genetic Basis of Inbreeding Depression in a Maize Landrace Compared to its Wild Relative, Teosinte

View ORCID ProfileL.F. Samayoa, View ORCID ProfileB.A. Olukolu, C.J. Yang, View ORCID ProfileQ. Chen, View ORCID ProfileMarkus G. Stetter, View ORCID ProfileAlessandra M. York, View ORCID ProfileJose de Jesus Sanchez-Gonzalez, Jeffrey C. Glaubitz, View ORCID ProfilePeter J. Bradbury, View ORCID ProfileMaria Cinta Romay, Qi Sun, View ORCID ProfileJinliang Yang, View ORCID ProfileJeffrey Ross-Ibarra, View ORCID ProfileEdward S. Buckler, View ORCID ProfileJ.F. Doebley, View ORCID ProfileJ.B. Holland
doi: https://doi.org/10.1101/2021.09.01.458502
L.F. Samayoa
*Department of Crop and Soil Sciences, North Carolina State University, Raleigh, NC 27695 USA
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B.A. Olukolu
†Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, Tennessee 37996 USA
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C.J. Yang
‡Laboratory of Genetics, University of Wisconsin – Madison, Madison, WI 53706 USA
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Q. Chen
‡Laboratory of Genetics, University of Wisconsin – Madison, Madison, WI 53706 USA
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Markus G. Stetter
§Institute for Plant Sciences and Center of Excellence on Plant Sciences, University of Cologne, Cologne 50674 Germany
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Alessandra M. York
‡Laboratory of Genetics, University of Wisconsin – Madison, Madison, WI 53706 USA
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Jose de Jesus Sanchez-Gonzalez
**Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Jalisco CP45110, Mexico
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Jeffrey C. Glaubitz
††Institute of Biotechnology, Cornell University, Ithaca, NY 14853 USA
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Peter J. Bradbury
‡‡US Department of Agriculture–Agricultural Research Service, Cornell University, Ithaca, NY 14853 USA
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Maria Cinta Romay
††Institute of Biotechnology, Cornell University, Ithaca, NY 14853 USA
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Qi Sun
††Institute of Biotechnology, Cornell University, Ithaca, NY 14853 USA
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Jinliang Yang
§§Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE 68583 USA
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Jeffrey Ross-Ibarra
***Department of Evolution and Ecology, Center for Population Biology, and Genome Center, University of California, Davis, CA 95616 USA
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Edward S. Buckler
‡‡US Department of Agriculture–Agricultural Research Service, Cornell University, Ithaca, NY 14853 USA
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J.F. Doebley
‡Laboratory of Genetics, University of Wisconsin – Madison, Madison, WI 53706 USA
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J.B. Holland
*Department of Crop and Soil Sciences, North Carolina State University, Raleigh, NC 27695 USA
†††United States Department of Agriculture – Agriculture Research Service, Raleigh, NC 27695 USA
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  • For correspondence: james_holland@ncsu.edu
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Abstract

Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. The extent to which the genetic load of mutations contributing to inbreeding depression is due to rare large-effect variation versus potentially more common variants with very small individual effects is unknown and may be affected by population history. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits, congruent with the greater segregating genetic load predicted from sequence data in the maize population. For many traits - and more commonly in maize - genetic variation among selffertilized families was less than expected based on additive and dominance variance estimated in outcrossed families, suggesting that a negative covariance between additive and homozygous dominance effects limits the variation available to selection under partial inbreeding. We identified quantitative trait loci (QTL) representing large-effect rare variants carried by only a single parent, which were more important in teosinte than maize. Teosinte also carried more putative juvenile-acting lethal variants identified by segregation distortion. These results suggest a mixture of mostly polygenic, smalleffect recessive variation underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following to the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against large effect variants, but polygenic load is harder to purge and segregating mutational burden increased in maize compared to teosinte.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license.
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Posted September 02, 2021.
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Domestication Reshaped the Genetic Basis of Inbreeding Depression in a Maize Landrace Compared to its Wild Relative, Teosinte
L.F. Samayoa, B.A. Olukolu, C.J. Yang, Q. Chen, Markus G. Stetter, Alessandra M. York, Jose de Jesus Sanchez-Gonzalez, Jeffrey C. Glaubitz, Peter J. Bradbury, Maria Cinta Romay, Qi Sun, Jinliang Yang, Jeffrey Ross-Ibarra, Edward S. Buckler, J.F. Doebley, J.B. Holland
bioRxiv 2021.09.01.458502; doi: https://doi.org/10.1101/2021.09.01.458502
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Domestication Reshaped the Genetic Basis of Inbreeding Depression in a Maize Landrace Compared to its Wild Relative, Teosinte
L.F. Samayoa, B.A. Olukolu, C.J. Yang, Q. Chen, Markus G. Stetter, Alessandra M. York, Jose de Jesus Sanchez-Gonzalez, Jeffrey C. Glaubitz, Peter J. Bradbury, Maria Cinta Romay, Qi Sun, Jinliang Yang, Jeffrey Ross-Ibarra, Edward S. Buckler, J.F. Doebley, J.B. Holland
bioRxiv 2021.09.01.458502; doi: https://doi.org/10.1101/2021.09.01.458502

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