Genomics of sorghum local adaptation to a parasitic plant

Bellis, Emily S.; Kelly, Elizabeth A.; Lorts, Claire M.; Gao, Huirong; DeLeo, Victoria L.; Rouhan, Germinal; Budden, Andrew; Bhaskara, Govinal B.; Hu, Zhenbin; Muscarella, Robert; Timko, Michael P.; Nebie, Baloua; Runo, Steven M.; Chilcoat, N. Doane; Juenger, Thomas E.; Morris, Geoffrey P.; dePamphilis, Claude W.; Lasky, Jesse R.

doi:10.1073/pnas.1908707117

Title: Genomics of sorghum local adaptation to a parasitic plant

Journal Article · Tue Feb 25 00:00:00 EST 2020 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1908707117· OSTI ID:1799035

^[1]; Kelly, Elizabeth A. ^[2]; Lorts, Claire M. ^[2]; Gao, Huirong ^[3]; DeLeo, Victoria L. ^[2];

^[4]; Budden, Andrew ^[5];

^[6]; Hu, Zhenbin ^[7];

^[8]; Timko, Michael P. ^[9]; Nebie, Baloua ^[10]; Runo, Steven M. ^[11]; Chilcoat, N. Doane ^[12]; Juenger, Thomas E. ^[13]; Morris, Geoffrey P. ^[7]; dePamphilis, Claude W. ^[2]; Lasky, Jesse R. ^[2]

Pennsylvania State Univ., University Park, PA (United States); Arkansas State Univ., Jonesboro, AR (United States)
Pennsylvania State Univ., University Park, PA (United States)
Applied Science and Technology, Corteva Agriscience, Johnston, IA (United States).
Sorbonne Univ., Paris (France). École Pratique des Hautes Études
Royal Botanic Gardens (United Kingdom)
Univ. of Texas, Austin, TX (United States)
Kansas State Univ., Manhattan, KS (United States)
Uppsala Univ. (Sweden)
Univ. of Virginia, Charlottesville, VA (United States). Dept. of Biology
West and Central Africa Regional Program, International Crops Research Institute for the Semi-Arid Tropics (Mali)
Kenyatta Univ., Nairobi (Kenya). Dept. of Biochemistry and Biotechnology
Corteva Agriscience, Johnston, IA (United States)
Univ. of Texas at Austin, Austin, TX (United States). Dept. of Integrative Biology

Host–parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

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Research Organization:: Donald Danforth Plant Science Center, St. Louis, MO (United States)

Sponsoring Organization:: USDOE Advanced Research Projects Agency - Energy (ARPA-E)

Grant/Contract Number:: AR0000594

OSTI ID:: 1799035

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, Issue 8; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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