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.

24Host-parasite coevolution can maintain high levels of genetic diversity in traits involved 25 in species interactions. In many systems, host traits exploited by parasites are 26 constrained by use in other functions, leading to complex selective pressures across 27 space and time. Here, we study genome-wide variation in the staple crop Sorghum 28 bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica 29 (Delile) Benth., a major constraint to food security in many African countries. We 30 hypothesize that sorghum landraces are subject to geographic selection mosaics within 31 parasite-prone areas and selection against resistance where S. hermonthica is never 32 found. Supporting this hypothesis, multiple independent loss-of-function alleles at 33 sorghum LOW GERMINATION STIMULANT 1 (LGS1), a locus known to impact 34 resistance, are broadly distributed among African landraces and geographically 35 associated with S. hermonthica occurrence, suggesting a role in local adaptation to 36 parasite pressure. However, the low frequency of these alleles within S. hermonthica-37 prone regions and their absence elsewhere indicates potential trade-offs restricting their 38 distribution. LGS1 impacts stereochemistry of strigolactones, hormones controlling 39 plant architecture, belowground signaling with other organisms, and abiotic stress 40 tolerance. Supporting trade-offs, transcriptome profiling of nutrient-stressed roots 41 revealed differential regulation of several strigolactone biosynthesis and signaling genes 42 in LGS1-deficient sorghum compared to a susceptible line. Signatures of balancing 43 selection surrounding LGS1 and candidates from analysis of genome-wide associations 44 with parasite distribution support long-term maintenance of diversity in parasite 45 resistance genes. Our study of host resistance evolution across smallholder 46 agroecosystems provides a valuable contrast to both industrial farming systems and 47 natural communities. 48 49 KEYWORDS: species distribution modeling, environmental niche modeling, genotype-50 environment association analysis, Red Queen 51 52 SIGNIFICANCE STATEMENT: 53 3 Understanding co-evolution in crop-parasite systems is critical to management of 54 myriad pests and pathogens confronting modern agriculture. In contrast to wild plant 55 communities, parasites in agricultural ecosystems are usually expected to gain the 56 upper hand in co-evolutionary 'arms races' due to limited genetic diversity of host crops 57 in cultivation. Here, we develop a framework for studying associations between genome 58 diversity in global landraces (traditional varieties) of the staple crop sorghum with the 59 distribution of the devastating parasitic weed Striga hermonthica. We find long-term 60 maintenance of diversity in genes related to parasite resistance, highlighting an 61 important role of host adaptation for co-evolutionary dynamics in smallholder 62 agroecosystems. 63 64 INTRODUCTION:

Intraspecific trait variation is caused by genetic and plastic responses to environment. This intraspecific diversity is captured in immense natural history collections, giving us a window into trait variation across continents and through centuries of environmental shifts. Here we tested if hypotheses based on life history and the leaf economics spectrum explain intraspecific trait changes across global spatiotemporal environmental gradients. We measured phenotypes on a 216‐year time series of Arabidopsis thaliana accessions from across its native range and applied spatially varying coefficient models to quantify region‐specific trends in trait coordination and trait responses to climate gradients. All traits exhibited significant change across space or through time. For example, δ15N decreased over time across much of the range and leaf C:N increased, consistent with predictions based on anthropogenic changes in land use and atmosphere. Plants were collected later in the growing season in more recent years in many regions, possibly because populations shifted toward more spring germination and summer flowering as opposed to fall germination and spring flowering. When climate variables were considered, collection dates were earlier in warmer years, while summer rainfall had opposing associations with collection date depending on regions. There was only a modest correlation among traits, indicating a lack of a single life history/physiology axis. Nevertheless, leaf C:N was low for summer‐ versus spring‐collected plants, consistent with a life history–physiology axis from slow‐growing winter annuals to fast‐growing spring/summer annuals. Regional heterogeneity in phenotype trends indicates complex responses to spatiotemporal environmental gradients potentially due to geographic genetic variation and climate interactions with other aspects of environment. Our study demonstrates how natural history collections can be used to broadly characterize trait responses to environment, revealing heterogeneity in response to anthropogenic change.

Intraspecific trait variation is caused by genetic and plastic responses to environment. This intraspecific diversity is captured in immense natural history collections, giving us a window into trait variation across continents and through centuries of environmental shifts. Here we tested if hypotheses based on life history and the leaf economics spectrum explain intraspecific trait changes across global spatiotemporal environmental gradients. We measured phenotypes on a 216‐year time series of Arabidopsis thaliana accessions from across its native range and applied spatially varying coefficient models to quantify region‐specific trends in trait coordination and trait responses to climate gradients. All traits exhibited significant change across space or through time. For example, δ15N decreased over time across much of the range and leaf C:N increased, consistent with predictions based on anthropogenic changes in land use and atmosphere. Plants were collected later in the growing season in more recent years in many regions, possibly because populations shifted toward more spring germination and summer flowering as opposed to fall germination and spring flowering. When climate variables were considered, collection dates were earlier in warmer years, while summer rainfall had opposing associations with collection date depending on regions. There was only a modest correlation among traits, indicating a lack of a single life history/physiology axis. Nevertheless, leaf C:N was low for summer‐ versus spring‐collected plants, consistent with a life history–physiology axis from slow‐growing winter annuals to fast‐growing spring/summer annuals. Regional heterogeneity in phenotype trends indicates complex responses to spatiotemporal environmental gradients potentially due to geographic genetic variation and climate interactions with other aspects of environment. Our study demonstrates how natural history collections can be used to broadly characterize trait responses to environment, revealing heterogeneity in response to anthropogenic change.

BackgroundThe presence of non-coding introns is a characteristic feature of most eukaryotic genes. While the size of the introns, number of introns per gene and the number of intron-containing genes can vary greatly between sequenced eukaryotic genomes, the structure of a gene with reference to intron presence and positions is typically conserved in closely related species. Unexpectedly, the ABCB1 (ATP-Binding Cassette Subfamily B Member 1) gene which encodes a P-glycoprotein and underlies dwarfing traits in maize (br2), sorghum (dw3) and pearl millet (d2) displayed considerable variation in intron composition.ResultsAn analysis of the ABCB1 gene structure in 80 angiosperms revealed that the number of introns ranged from one to nine. All introns in ABCB1 underwent either a one-time loss (single loss in one lineage/species) or multiple independent losses (parallel loss in two or more lineages/species) with the majority of losses occurring within the grass family. In contrast, the structure of the closest homolog to ABCB1, ABCB19, remained constant in the majority of angiosperms analyzed. Using known phylogenetic relationships within the grasses, we determined the ancestral branch-points where the losses occurred. Intron 7, the longest intron, was lost in only a single species, Mimulus guttatus, following duplication of ABCB1. Semiquantitative PCR showed that the M. guttatus ABCB1 gene copy without intron 7 had significantly lower transcript levels than the gene copy with intron 7. We further demonstrated that intron 7 carried two motifs that were highly conserved across the monocot-dicot divide.ConclusionsThe ABCB1 gene structure is highly dynamic, while the structure of ABCB19 remained largely conserved through evolution. Precise removal of introns, preferential removal of smaller introns and presence of at least 2 bp of microhomology flanking most introns indicated that intron loss may have predominantly occurred through non-homologous end-joining (NHEJ) repair of double strand breaks. Lack of microhomology in the exon upstream of lost phase I introns was likely due to release of the selective constraint on the penultimate base (3rd base in codon) of the terminal codon by the splicing machinery. In addition to size, the presence of regulatory motifs will make introns recalcitrant to loss.Electronic supplementary materialThe online version of this article (10.1186/s12862-017-1077-x) contains supplementary material, which is available to authorized users.