28Rice (Oryza sativa) is one of the world's most important food crops. We reconstruct 29
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:
BackgroundCoral reef ecosystems are declining in response to global climate change and anthropogenic impacts. Yet patterns of standing genetic variation within cnidarian species, a major determinant of adaptive potential, are virtually unknown at genome-scale resolution. We explore patterns of genome-wide polymorphism and identify candidate loci under selection in the sea anemone Aiptasia, an important laboratory model system for studying the symbiosis between corals and dinoflagellate algae of the genus Symbiodinium.ResultsLow coverage genome sequencing revealed large genetic distances among globally widespread lineages, novel candidate targets of selection, and considerably higher heterozygosity than previously reported for Aiptasia. More than 670,000 single nucleotide polymorphisms were identified among 10 Aiptasia individuals including two pairs of genetic clones. Evolutionary relationships based on genome-wide polymorphism supported the current paradigm of a genetically distinct population from the US South Atlantic that harbors diverse Symbiodinium clades. However, anemones from the US South Atlantic demonstrated a striking lack of shared derived polymorphism. Heterozygosity was an important feature shaping nucleotide diversity patterns: at any given SNP site, more than a third of individuals genotyped were heterozygotes, and heterozygosity within individual genomes ranged from 0.37–0.58 %. Analysis of nonsynonymous and synonymous sites suggested that highly heterozygous regions are evolving under relaxed purifying selection compared to the rest of the Aiptasia genome. Genes previously identified as having elevated evolutionary rates in Aiptasia compared to other cnidarians were found in our study to be under strong purifying selection within Aiptasia. Candidate targets of selection, including lectins and genes involved in Rho GTPase signalling, were identified based on unusual signatures of nucleotide diversity, Tajima’s D, and heterozygosity compared to genome-wide averages.ConclusionsThis study represents the first genome-wide analysis of Tajima’s D in a cnidarian. Our results shed light on patterns of intraspecific genome-wide polymorphism in a model for studies of coral-algae symbiosis and present genetic targets for future research on evolutionary and cellular processes in early-diverging metazoans.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2488-6) contains supplementary material, which is available to authorized users.
Transposable elements (TEs) represent a major portion of most eukaryotic genomes, yet little is known about their mutation rates or how their activity is shaped by other evolutionary forces. Here, we compare short- and long-term patterns of genome-wide mutation accumulation (MA) of TEs among 9 genotypes from three populations of Daphnia magna from across a latitudinal gradient. While the overall proportion of the genome comprised of TEs is highly similar among genotypes from Finland, Germany, and Israel, populations are distinguishable based on patterns of insertion site polymorphism. Our direct rate estimates indicate TE movement is highly variable (net rates ranging from -11.98 to 12.79 x 10−5 per copy per generation among genotypes), differing both among populations and TE families. Although gains outnumber losses when selection is minimized, both types of events appear to be highly deleterious based on their low frequency in control lines where propagation is not limited to random, single-progeny descent. With rate estimates 4 orders of magnitude higher than base substitutions, TEs clearly represent a highly mutagenic force in the genome. Quantifying patterns of intra- and interspecific variation in TE mobility with and without selection provides insight into a powerful mechanism generating genetic variation in the genome.
Rising ocean temperatures disrupt the symbiosis between corals and their microalgae, accelerating global decline of coral reef ecosystems. Because of the difficulty of performing laboratory experiments with corals, the sea anemone Aiptasia has emerged as an important model system for molecular studies of coral bleaching and symbiosis. Here, we investigate natural variation in bleaching responses among different genetic lineages of Aiptasia. Both heat- and cold-induced paths to symbiosis breakdown were analyzed. Significant genetic variation in response to acute heat stress was observed, with severe bleaching of two Aiptasia strains from Hawaii but minimal bleaching of strains from the U.S. South Atlantic, including the strain used to generate the Aiptasia reference genome. Both strains from Hawaii hosted Symbiodinium type B1, whereas strains from the U.S. South Atlantic hosted type A4 or B2. In contrast to the results from exposures to acute heat stress, negligible variation was observed in response to a pulsed cold shock despite moderate bleaching across all strains. These results support our hypothesis that bleaching responses to distinct stressors are independent. Our findings emphasize the role of stress regime when predicting adaptive responses of symbiotic cnidarians to changing climates, because genetic variation may exist for some forms of stress-induced bleaching but not others.
Host-specific interactions can maintain genetic and phenotypic diversity in parasites that attack multiple host species. Host diversity, in turn, may promote parasite diversity by selection for genetic divergence or plastic responses to host type. The parasitic weed purple witchweed [Striga hermonthica (Delile) Benth.] causes devastating crop losses in sub-Saharan Africa and is capable of infesting a wide range of grass hosts. Despite some evidence for host adaptation and host-by-Striga genotype interactions, little is known about intraspecific Striga genomic diversity. Here we present a study of transcriptomic diversity in populations of S. hermonthica growing on different hosts (maize [Zea mays L.] vs. grain sorghum [Sorghum bicolor (L.) Moench]). We examined gene expression variation and differences in allelic frequency in expressed genes of aboveground tissues from populations in western Nigeria parasitizing each host. Despite low levels of host-based genome-wide differentiation, we identified a set of parasite transcripts specifically associated with each host. Parasite genes in several different functional categories implicated as important in host–parasite interactions differed in expression level and allele on different hosts, including genes involved in nutrient transport, defense and pathogenesis, and plant hormone response. Overall, we provide a set of candidate transcripts that demonstrate host-specific interactions in vegetative tissues of the emerged parasite S. hermonthica. Our study shows how signals of host-specific processes can be detected aboveground, expanding the focus of host–parasite interactions beyond the haustorial connection.
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