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Genomics of sorghum local adaptation to a parasitic plant.

ABSTRACT: 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.

SUBMITTER: Bellis ES

PROVIDER: S-EPMC7049153 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Genomics of sorghum local adaptation to a parasitic plant.

Bellis Emily S ES Kelly Elizabeth A EA Lorts Claire M CM Gao Huirong H DeLeo Victoria L VL Rouhan Germinal G Budden Andrew A Bhaskara Govinal B GB Hu Zhenbin Z Muscarella Robert R Timko Michael P MP Nebie Baloua B Runo Steven M SM Chilcoat N Doane ND Juenger Thomas E TE Morris Geoffrey P GP dePamphilis Claude W CW Lasky Jesse R JR

Proceedings of the National Academy of Sciences of the United States of America 20200211 8

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 <i>Sorghum bicolor</i> (L.) Moench and its association with the parasitic weed <i>Striga hermonthica</i> (Delile) Benth., a major constraint to food security in Africa. We ...[more]

PMID: 32047036

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Project description:Wolbachia and Cardinium are among the most important and widespread of all endosymbionts, occurring in nematodes and more than half of insect and arachnid species, sometimes as coinfections. These symbionts are of significant interest as potential biocontrol agents due to their abilities to cause major effects on host biology and reproduction through cytoplasmic incompatibility, sex ratio distortion, or obligate mutualism. The ecological and metabolic effects of coinfections are not well understood. This study examined a Wolbachia-Cardinium coinfection in the plant-parasitic nematode (PPN), Pratylenchus penetrans, producing the first detailed study of such a coinfection using fluorescence in situ hybridization (FISH), polymerase chain reaction (PCR), and comparative genomic analysis. Results from FISH and single-nematode PCR showed 123/127 individuals in a focal population carried Cardinium (denoted strain cPpe), and 48% were coinfected with Wolbachia strain wPpe. Both endosymbionts showed dispersed tissue distribution with highest densities in the anterior intestinal walls and gonads. Phylogenomic analyses confirmed an early place of cPpe and long distance from a sister strain in another PPN, Heterodera glycines, supporting a long history of both Cardinium and Wolbachia in PPNs. The genome of cPpe was 1.36 Mbp with 35.8% GC content, 1,131 predicted genes, 41% having no known function, and missing biotin and lipoate synthetic capacity and a plasmid present in other strains, despite having a slightly larger genome compared to other sequenced Cardinium. The larger genome revealed expansions of gene families likely involved in host-cellular interactions. More than 2% of the genes of cPpe and wPpe were identified as candidate horizontally transferred genes, with some of these from eukaryotes, including nematodes. A model of the possible Wolbachia-Cardinium interaction is proposed with possible complementation in function for pathways such as methionine and fatty acid biosynthesis and biotin transport.

Project description:BackgroundMicrosporidian Nosema bombycis has received much attention because the pébrine disease of domesticated silkworms results in great economic losses in the silkworm industry. So far, no effective treatment could be found for pébrine. Compared to other known Nosema parasites, N. bombycis can unusually parasitize a broad range of hosts. To gain some insights into the underlying genetic mechanism of pathological ability and host range expansion in this parasite, a comparative genomic approach is conducted. The genome of two Nosema parasites, N. bombycis and N. antheraeae (an obligatory parasite to undomesticated silkworms Antheraea pernyi), were sequenced and compared with their distantly related species, N. ceranae (an obligatory parasite to honey bees).ResultsOur comparative genomics analysis show that the N. bombycis genome has greatly expanded due to the following three molecular mechanisms: 1) the proliferation of host-derived transposable elements, 2) the acquisition of many horizontally transferred genes from bacteria, and 3) the production of abundnant gene duplications. To our knowledge, duplicated genes derived not only from small-scale events (e.g., tandem duplications) but also from large-scale events (e.g., segmental duplications) have never been seen so abundant in any reported microsporidia genomes. Our relative dating analysis further indicated that these duplication events have arisen recently over very short evolutionary time. Furthermore, several duplicated genes involving in the cytotoxic metabolic pathway were found to undergo positive selection, suggestive of the role of duplicated genes on the adaptive evolution of pathogenic ability.ConclusionsGenome expansion is rarely considered as the evolutionary outcome acting on those highly reduced and compact parasitic microsporidian genomes. This study, for the first time, demonstrates that the parasitic genomes can expand, instead of shrink, through several common molecular mechanisms such as gene duplication, horizontal gene transfer, and transposable element expansion. We also showed that the duplicated genes can serve as raw materials for evolutionary innovations possibly contributing to the increase of pathologenic ability. Based on our research, we propose that duplicated genes of N. bombycis should be treated as primary targets for treatment designs against pébrine. The genome data and annotation information of N. bombycis and N.antheraeae were submitted to GenBank (Accession numbers ACJZ01000001 -ACJZ01003558).

Dataset Information

Genomics of sorghum local adaptation to a parasitic plant.

Publications

Genomics of sorghum local adaptation to a parasitic plant.

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