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Title: Deleterious Mutation Burden and Its Association with Complex Traits in Sorghum (Sorghum bicolor)

Abstract

Sorghum (Sorghum bicolor L.) is a major food cereal for millions of people worldwide. The sorghum genome, like other species, accumulates deleterious mutations, likely impacting its fitness. The lack of recombination, drift, and the coupling with favorable loci impede the removal of deleterious mutations from the genome by selection. To study how deleterious variants impact phenotypes, we identified putative deleterious mutations among ~5.5 M segregating variants of 229 diverse biomass sorghum lines. We provide the whole-genome estimate of the deleterious burden in sorghum, showing that ~33% of nonsynonymous substitutions are putatively deleterious. The pattern of mutation burden varies appreciably among racial groups. Across racial groups, the mutation burden correlated negatively with biomass, plant height, specific leaf area (SLA), and tissue starch content (TSC), suggesting that deleterious burden decreases trait fitness. Putatively deleterious variants explain roughly one-half of the genetic variance. However, there is only moderate improvement in total heritable variance explained for biomass (7.6%) and plant height (average of 3.1% across all stages). There is no advantage in total heritable variance for SLA and TSC. The contribution of putatively deleterious variants to phenotypic diversity therefore appears to be dependent on the genetic architecture of traits. Overall, these results suggest thatmore » incorporating putatively deleterious variants into genomic models slightly improves prediction accuracy because of extensive linkage. Knowledge of deleterious variants could be leveraged for sorghum breeding through either genome editing and/or conventional breeding that focuses on the selection of progeny with fewer deleterious alleles.« less

Authors:
ORCiD logo [1];  [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [2]; ORCiD logo [4]; ORCiD logo [1]; ORCiD logo [5]; ORCiD logo [4]; ORCiD logo [2]; ORCiD logo [6]; ORCiD logo [1]
  1. Cornell Univ., Ithaca, NY (United States). Inst. for Genomic Diversity
  2. Cornell Univ., Ithaca, NY (United States). Plant Breeding and Genetics Section. School of Integrative Plant Science
  3. Univ. of Illinois, Urbana, IL (United States). Dept. of Plant Biology
  4. Univ. of Illinois, Urbana, IL (United States). Dept. of Plant Biology. Dept. of Crop Sciences. Inst. for Genomic Biology
  5. Univ. of California, Davis, CA (United States). Section of Agricultural Plant Biology. Dept. of Plant Sciences
  6. Cornell Univ., Ithaca, NY (United States). Inst. for Genomic Diversity. Plant Breeding and Genetics Section. School of Integrative Plant Science; USDA Agricultural Research Service, Ithaca, NY (United States)
Publication Date:
Research Org.:
Univ. of Illinois at Urbana-Champaign, IL (United States)
Sponsoring Org.:
USDOE Advanced Research Projects Agency - Energy (ARPA-E)
OSTI Identifier:
1510283
Grant/Contract Number:  
AR0000598; AR0000661
Resource Type:
Accepted Manuscript
Journal Name:
Genetics
Additional Journal Information:
Journal Volume: 211; Journal Issue: 3; Journal ID: ISSN 0016-6731
Publisher:
Genetics Society of America
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; deleterious mutations; genetic load; genome-wide predictions; mutation burden; sorghum

Citation Formats

Valluru, Ravi, Gazave, Elodie E., Fernandes, Samuel B., Ferguson, John N., Lozano, Roberto, Hirannaiah, Pradeep, Zuo, Tao, Brown, Patrick J., Leakey, Andrew D. B., Gore, Michael A., Buckler, Edward S., and Bandillo, Nonoy. Deleterious Mutation Burden and Its Association with Complex Traits in Sorghum (Sorghum bicolor). United States: N. p., 2019. Web. doi:10.1534/genetics.118.301742.
Valluru, Ravi, Gazave, Elodie E., Fernandes, Samuel B., Ferguson, John N., Lozano, Roberto, Hirannaiah, Pradeep, Zuo, Tao, Brown, Patrick J., Leakey, Andrew D. B., Gore, Michael A., Buckler, Edward S., & Bandillo, Nonoy. Deleterious Mutation Burden and Its Association with Complex Traits in Sorghum (Sorghum bicolor). United States. https://doi.org/10.1534/genetics.118.301742
Valluru, Ravi, Gazave, Elodie E., Fernandes, Samuel B., Ferguson, John N., Lozano, Roberto, Hirannaiah, Pradeep, Zuo, Tao, Brown, Patrick J., Leakey, Andrew D. B., Gore, Michael A., Buckler, Edward S., and Bandillo, Nonoy. Fri . "Deleterious Mutation Burden and Its Association with Complex Traits in Sorghum (Sorghum bicolor)". United States. https://doi.org/10.1534/genetics.118.301742. https://www.osti.gov/servlets/purl/1510283.
@article{osti_1510283,
title = {Deleterious Mutation Burden and Its Association with Complex Traits in Sorghum (Sorghum bicolor)},
author = {Valluru, Ravi and Gazave, Elodie E. and Fernandes, Samuel B. and Ferguson, John N. and Lozano, Roberto and Hirannaiah, Pradeep and Zuo, Tao and Brown, Patrick J. and Leakey, Andrew D. B. and Gore, Michael A. and Buckler, Edward S. and Bandillo, Nonoy},
abstractNote = {Sorghum (Sorghum bicolor L.) is a major food cereal for millions of people worldwide. The sorghum genome, like other species, accumulates deleterious mutations, likely impacting its fitness. The lack of recombination, drift, and the coupling with favorable loci impede the removal of deleterious mutations from the genome by selection. To study how deleterious variants impact phenotypes, we identified putative deleterious mutations among ~5.5 M segregating variants of 229 diverse biomass sorghum lines. We provide the whole-genome estimate of the deleterious burden in sorghum, showing that ~33% of nonsynonymous substitutions are putatively deleterious. The pattern of mutation burden varies appreciably among racial groups. Across racial groups, the mutation burden correlated negatively with biomass, plant height, specific leaf area (SLA), and tissue starch content (TSC), suggesting that deleterious burden decreases trait fitness. Putatively deleterious variants explain roughly one-half of the genetic variance. However, there is only moderate improvement in total heritable variance explained for biomass (7.6%) and plant height (average of 3.1% across all stages). There is no advantage in total heritable variance for SLA and TSC. The contribution of putatively deleterious variants to phenotypic diversity therefore appears to be dependent on the genetic architecture of traits. Overall, these results suggest that incorporating putatively deleterious variants into genomic models slightly improves prediction accuracy because of extensive linkage. Knowledge of deleterious variants could be leveraged for sorghum breeding through either genome editing and/or conventional breeding that focuses on the selection of progeny with fewer deleterious alleles.},
doi = {10.1534/genetics.118.301742},
journal = {Genetics},
number = 3,
volume = 211,
place = {United States},
year = {2019},
month = {3}
}

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