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Sawers, R. J. H.

Publications and source records attributed to Sawers, R. J. H..

13 recordsLinked to original sources

The MexMAGIC population reveals the genetic architecture of clinal trait variation in Mexican native maize

Defining the genetic basis of local adaptation is fundamental to evolutionary biology and crop improvement. Theory predicts that when selective pressures track differences in the environment, a cline will be established. Such clines might be exploited to uncover adaptive variation by association of alleles with environmental stressors. However, monotonic phenotypic change over a cline is not necessarily mirrored by adaptive genetic variants. Furthermore, population structure can complicate the interpretation of genotype-environment association. To test the assumptions of genotype-environment association in a crop species, we developed a multi-parent advanced generation inter-cross (MAGIC) population using eight Mexican native maize varieties sourced from distinct agroecological zones. We mapped two clinal traits (tassel branching and flowering time) differing in genetic architecture. Variation in tassel branch number was dominated by a single QTL with allele effects that aligned well with a negative elevational cline. In contrast, we mapped 11 flowering time QTL with allele effects that were not consistently correlated with any one source environmental factor and distinct loci donated by highland and lowland early maturing varieties. Our observations support the theoretical result that genotype-environment association will be strongest under simple genetic architecture, although identification of adaptive alleles may still be confounded by population structure. Plain Language: Nine thousand years of careful selection and cultivation by indigenous farmers has generated a rich diversity of native Mexican maize (corn) varieties, grown from sea level to high mountains, and from jungle to semidesert. By crossing native varieties adapted to different locations, we can uncover important genetic variants conferring tolerance to environmental stressors.

genetics↗

Strigolactone effects on Sorghum bicolor ecophysiology and symbioses

Strigolactones are ecologically, developmentally, and physiologically important hormones, but much remains unknown about their evolution and role in non-model species. Sorghum is a globally important C4 cereal and exhibits natural variation in root-exuded strigolactones. Differences in sorghum strigolactone stereochemistry are associated with resistance to parasitic plants, but with evidence for potential trade-offs. We studied sorghum mutants of loci in the strigolactone biosynthetic pathway, CAROTENOID CLEAVAGE DIOXYGENASE 8 (SbCCD8b) and LOW GERMINATION STIMULANT 1 (LGS1), previously shown to be Striga resistant by stimulating little germination of the parasite. SbCCD8b CRISPR-Cas9 deletions changed the accumulation of low abundance metabolites, reduced net carbon assimilation rate, altered root architecture and anatomy, and diminished the establishment and benefit of mycorrhizal symbionts. For Striga-resistant LGS1 CRISPR-Cas9 deletions, differentially expressed genes were enriched with promoter motifs for stress response and growth pathways, net carbon assimilation rate was reduced, and the colonization of mycorrhizal symbionts was delayed. We additionally restored functional LGS1 into the RTx430 genetic background, which normally has the lgs1-2 natural deletion allele. While root exudates from LGS1 insertion mutants rescued Striga susceptibility, we did not see consistent rescue of other traits impacted in LGS1 loss-of-function mutants. We hypothesize that epistasis with a neighboring strigolactone synthesis gene, which is rarely lost without concomitant loss of LGS1, may alter the phenotypic effects of LGS1 variation. Our study gives context to potential trade-offs associated with host resistance to parasitic plants and, more broadly, builds on the contribution of strigolactones in shaping sorghum physiological processes, growth, and development.

plant biology↗

Metabolic modeling reveals synergistic growth benefits of engineering maize symbiosis with rhizobia and arbuscular mycorrhizal fungi

Engineering a novel N2-fixing rhizobia symbiosis in cereal crops is a strategy being pursued to improve agricultural sustainability. However, if such a symbiosis were introduced, it would have to be economically viable in the context of existing nutrient acquisition strategies, including the existing symbiosis with arbuscular mycorrhizal fungi (AMF) that the vast majority of plants already engage in. This raises the question of how the metabolic costs and benefits from these separate symbioses that have partially overlapping functions might impact nutrient status and subsequent plant growth. To address this, we developed metabolic models describing how the relative growth rate of Zea mays is impacted by the AMF Rhizophagus irregularis and a hypothetical N2-fixing symbiosis with Bradyrhizobium diazoefficiens both in isolation and in tandem. To validate the AMF component of our model, we conducted field evaluation of mutant AMF-incompatible maize hybrids and found that the empirically measured AMF-mediated growth benefit agreed well with our models predictions. Our model of the rhizobium symbiosis predicted that the lower N content of cereal crops makes the relative growth rate cost associated with acquiring nitrogen from N2-fixing rhizobia smaller than in legumes. Finally, our model also predicted positive synergies between rhizobia and AMF under nutrient-limited conditions but negative synergies under nutrient, particularly phosphorus, replete conditions. These findings indicate that these bioengineering strategies could improve cereal crop yields and may achieve greater gains in tandem, but soil nutrient status of target sites as well as the nitrogen requirements of specific varieties should be considered.

systems biology↗

Heritable maize microbiomes contribute to local adaptation and host stress resilience

Beneficial interactions with microorganisms are pivotal for crop performance and resilience. However, it remains unclear how heritable the microbiome is with respect to the host plant genotype and to what extent host genetic mechanisms can modulate plant-microbe interactions in the face of environmental stress. Here, we surveyed the root and rhizosphere microbiome of 129 accessions of locally adapted Zea mays, sourced from diverse habitats and grown under control and different stress conditions. We quantified treatment and host genotype effects on the microbiome. Plant genotype and source environment were predictive of microbiome composition. Genome wide association analysis identified host genetic variants linked to both rhizosphere microbiome composition and source environment. We identified transposon insertions in a candidate gene linked to both the abundance of a keystone microbe Massilia and source total soil nitrogen, finding mutant plants to show a reduction in lateral root density. We conclude that locally adapted maize varieties exert patterns of genetic control on their root and rhizosphere microbiomes that follow variation in their home environments, consistent with a role in tolerance to prevailing stress.

genetics↗

The pho1;2a'-m1.1 allele of Phosphate1 conditions mis-regulation of the phosphorus starvation response in maize (Zea mays ssp. mays L.)

PHO1 proteins play a central role in plant inorganic phosphorus translocation and sensing. The maize (Zea mays ssp. mays) genome encodes two co-orthologs of the Arabidopsis PHO1 gene, designated ZmPho1;2a and ZmPho1;2b. Here, we report the characterization of the transposon-footprint allele Zmpho1;2a-m1.1, which we refer to hereafter as pho1;2a. The pho1;2a allele is a stable derivative formed by excision of an Activator element from the ZmPho1;2a gene. The pho1;2a allele contains an 8 bp insertion at the point of excision that disrupts the reading frame and is predicted to generate a premature translational stop. We show that the pho1;2a allele is linked to a dosage-dependent reduction in transcript accumulation and a mild reduction in seedling growth that is enhanced under nutrient deficient conditions. Characterization of the shoot and root transcriptomes of seedlings segregating the pho1;2a mutation under different nutrient conditions revealed pho1;2a to have a dominant effect on patterns of transcript accumulation. Gene set enrichment analysis of the transcripts mis-regulated in pho1;2a mutants suggests that Pho1;2a functions in the fine-tuning of the transcriptional phosphate starvation response. We discuss our results with reference to possible genetic redundancy among maize Pho1 genes and in the context of reports linking functional variation in Pho1;2a to agronomically important traits.

plant biology↗

Strengthened mutualistic adaptation between teosinte and its rhizosphere biota in cold climates

O_LIWhile abiotic environments consistently shape local adaptation, the strength of local adaptation to biotic interactions may vary more. One theory, COCO (CO-evolutionary Outcomes across Conditionality), predicts it may be strongest where species experience greater stress, because stress increases fitness impacts of species interactions. For example, in plant interactions with rhizosphere biota, positive outcomes increase with stress from low soil fertility, drought and cold. C_LIO_LITo investigate the influence of abiotic stress gradients on adaptation between plants and rhizosphere biota, we used a greenhouse common garden experiment recombining teosinte, Zea mays ssp. mexicana (wild relative of maize), and rhizosphere biota, collected across a stress gradient (elevational variation in temperature, precipitation, and nutrients). C_LIO_LIWe found stronger local adaptation between teosinte and rhizosphere biota from colder, more stressful sites, as expected by COCO. However, biota from less stressful, warmer sites provided greater average benefits across teosinte populations. Links between plant traits and 20-element profiles of plant leaves explained fitness variation, persisted in the field, were influenced by both plants and biota, and largely reflected patterns of local adaptation. C_LIO_LIIn sum, we uncovered greater local adaptation to biotic interactions in colder sites, and that both plants and rhizosphere biota affect the expression of plant phenotypes. C_LI

evolutionary biology↗

Demonstration of local adaptation of maize landraces by reciprocal transplantation

Populations are locally adapted when they exhibit higher fitness than foreign populations in their native habitat. Maize landrace adaptations to highland and lowland conditions are of interest to researchers and breeders. To determine the prevalence and strength of local adaptation in maize landraces, we performed a reciprocal transplant experiment across an elevational gradient in Mexico. We grew 120 landraces, grouped into four populations (Mexican Highland, Mexican Lowland, South American Highland, South American Lowland), in Mexican highland and lowland common gardens and collected phenotypes relevant to fitness, as well as reported highland-adaptive traits such as anthocyanin pigmentation and macrohair density. 67k DArTseq markers were generated from field specimens to allow comparison between phenotypic patterns and population genetic structure. We found phenotypic patterns consistent with local adaptation, though these patterns differ between the Mexican and South American populations. While population genetic structure largely recapitulates drift during post-domestication dispersal, landrace phenotypes reflect adaptations to native elevation. Quantitative trait QST was greater than neutral FST for many traits, signaling divergent directional selection between pairs of populations. All populations exhibited higher fitness metric values when grown at their native elevation, and Mexican landraces had higher fitness than South American landraces when grown in our Mexican sites. Highland populations expressed generally higher anthocyanin pigmentation than lowland populations, and more so in the highland site than in the lowland site. Macrohair density was largely non-plastic, and Mexican landraces and highland landraces were generally more pilose. Analysis of{delta} 13C indicated that lowland populations may have lower WUE. Each population demonstrated garden-specific correlations between highland trait expression and fitness, with stronger positive correlations in the highland site. These results give substance to the long-held presumption of local adaptation of New World maize landraces to elevation and other environmental variables across North and South America.

evolutionary biology↗

Low nitrogen availability inhibits the phosphorus starvation response in maize (Zea mays ssp. mays L.)

BackgroundNitrogen (N) and phosphorus (P) are macronutrients essential for crop growth and productivity. In cultivated fields, N and P levels are rarely sufficient, contributing to the yield gap between realized and potential production. Fertilizer application increases nutrient availability, but not all farmers have access to fertilizers, nor are current rates of application sustainable or environmentally desirable. Transcriptomic studies of cereal crops have revealed dramatic responses to either low N or low P single stress treatments. In the field, however, levels of both N and P may be suboptimal. The interaction between N and P starvation responses remains to be fully characterized. ResultsWe characterized growth and root and leaf transcriptomes of young maize plants under nutrient replete, low N, low P or combined low NP conditions. We identified 1,555 genes to respond to our nutrient treatments, in one or both tissues. A large group of genes, including many classical P starvation response genes, were regulated antagonistically between low N and P conditions. An additional experiment over a range of N availability indicated that a mild reduction in N levels was sufficient to repress the low P induction of P starvation genes. Although expression of P transporter genes was repressed under low N or low NP, we confirmed earlier reports of P hyper accumulation under N limitation. ConclusionsTranscriptional responses to low N or P were distinct, with few genes responding in a similar way to the two single stress treatments. In combined NP stress, the low N response dominated, and the P starvation response was largely suppressed. A reduction in N availability was sufficient to repress the induction of P starvation associated genes. We conclude that activation of the transcriptional response to P starvation in maize is contingent on sufficient N availability.

plant biology↗

The genetic architecture of host response suggests a trade-off between mycorrhizal and non-mycorrhizal performance in field-grown maize

Arbuscular mycorrhizal fungi (AMF) are ubiquitous in cultivated soils, forming symbiotic relationships with the roots of major crop species. Although studies in controlled conditions have demonstrated the potential of the symbiosis to enhance host plant nutrition and alleviate environmental stress, practical difficulties make it hard to estimate the actual benefit in cultivated fields, not least because of the lack of availability of suitable AMF-free controls. Furthermore, the response can vary depending on the plant variety in a manner which is not fully understood. Here, we implemented a novel strategy based on the selective incorporation of AMF-resistance into a genetic mapping population to evaluate maize response in the field. We found AMF to account for about one third of the grain production in a rain-fed medium input field, as well as to impact the relative performance of plant varieties. Characterization of the genetic architecture of host response allowed us to distinguish mycorrhizal benefit from dependence and indicated a trade-off between mycorrhizal and non-mycorrhizal performance, both at the level of individual QTL and genomewide. This approach is applicable to other crop species, permits further mechanistic analysis and is scalable to full yield trials.

plant biology↗

Inoculation with the mycorrhizal fungus Rhizophagus irregulars increases nutrient uptake in maize (Zea mays) through hyphal foraging and promotion of root growth

Plant root systems play an essential role in nutrient and water acquisition. In resource-limited soils, modification of root system architecture is an important strategy to optimize plant performance. Most terrestrial plants also form symbiotic associations with arbuscular mycorrhizal fungi to maximize nutrient uptake. In addition to direct delivery of nutrients, arbuscular mycorrhizal fungi benefit the plant host by promoting root growth. Here, we aimed to quantify the impact of arbuscular mycorrhizal symbiosis on root growth and nutrient uptake in maize. Inoculated plants showed an increase in both biomass and the total content of twenty quantified elements. In addition, image analysis showed mycorrhizal plants to have denser, more branched root systems. For most of the quantified elements, the increase in content in mycorrhizal plants was proportional to root and overall plant growth. However, the increase in boron, calcium, magnesium, phosphorus, sulfur and strontium was greater than predicted by root system size alone, indicating fungal delivery to be supplementing root uptake.

plant biology↗

Adaptive phenotypic divergence in teosinte differs across biotic contexts

Climate is a powerful force shaping adaptation within species, often creating dramatic phenotypic clines. Yet adaptation to climate does not occur in a vacuum: species interactions filter the fitness consequences of both climatic and phenotypic variation. In other words, the translation of genotype to phenotype may be altered by biotic context, influencing the variation upon which climatic selection can act. We investigate the role of such interactions in changing the phenotypes on which selection acts using ten populations of an annual grass species (teosinte: Zea mays ssp. mexicana) sourced from along an elevational gradient, along with rhizosphere biota sourced from three of those populations. We grow teosinte families in a half-sibling design in separate biota treatments to first test whether the divergence we see among traits in teosinte populations exceeds what we would expect from genetic drift and then whether the source of rhizosphere biota affects the expression of divergent traits. We also assay the influence of these three rhizosphere biotas on contemporary additive genetic variation in teosinte traits across populations. We find that expression of most measured traits in teosinte is altered by rhizosphere biota, as well as the degree of variance and covariance among traits involved in root mass and flowering time. As a number of these traits are also found to underlie adaptive divergence across habitats, our data suggest that biota influence the expression of traits underlying local adaptation. Together, our results suggest that changes in trait expression and covariance elicited by interactor communities in root mass and flowering time may have played a historical role in local adaption of teosinte to environments, and that they would play a contemporary role in responses to changing selection pressures.

evolutionary biology↗

Allele specific expression analysis identifies regulatory variation associated with stress-related genes in the Mexican highland maize landrace Palomero Toluqueno

BackgroundGene regulatory variation has been proposed to play an important role in the adaptation of plants to environmental stress. In the central highlands of Mexico, farmer selection has generated a unique group of maize landraces adapted the challenges of the highland niche. In this study, gene expression in Mexican highland maize and a reference maize breeding line were compared to identify evidence of regulatory variation in stress-related genes. It was hypothesised that local adaptation in Mexican highland maize would be associated with a transcriptional signature observable even under benign conditions.\n\nMethodsAllele specific expression analysis was performed using the seedling-leaf transcriptome of an F1 individual generated from the cross between the highland adapted Mexican landrace Palomero Toluqueno and the reference line B73, grown under benign conditions. Results were compared with a published dataset describing the transcriptional response of B73 seedlings to cold, heat, salt and UV treatments.\n\nResultsA total of 2386 genes were identified to show allele specific expression. Of these, 277 showed an expression difference between Palomero Toluqueno and B73 alleles that mirrored the response of B73 cold, heat, salt and/or UV treatments, and, as such, were considered to display a constitutive stress response. Constitutive stress response candidates included genes associated with plant hormone signaling and a number of transcription factors. Construction of a gene co-expression network revealed further signaling and stress-related genes to be among the potential targets of the transcription factors candidates.\n\nDiscussionConstitutive activation of responses may represent the best strategy when stresses are severe but predictable. Expression differences observed here between PT and B73 alleles indicate the presence of cis-acting regulatory variation linked to stress-related genes in PT. Considered alongside gene annotation and population data, allele specific expression analysis of plants grown under benign conditions provides an attractive strategy to identify functional variation potentially linked to local adaptation.

plant biology↗

Identification of the maize Mediator CDK8 module, and Dissociation insertional mutagenesis of ZmMed12a

Mediator is a conserved transcriptional co-activator that links transcription factors bound at enhancer elements to RNA Polymerase II. Mediator-RNA Polymerase II interactions can be sterically hindered by the Cyclin Dependent Kinase 8 (CDK8) module, a submodule of Mediator that acts to repress transcription in response to discrete cellular and environmental cues. The CDK8 module is conserved in all eukaryotes and consists of 4 proteins: CDK8, CYCLIN C (CYCC), MED12, and MED13. In this study, we have characterized the CDK8 module of Mediator in maize. The maize genome contains single copy genes for Cdk8, CycC, and Med13, and two genes for Med12. Analysis of expression data for the CDK8 module demonstrated that all five genes are broadly expressed in maize tissues, with ZmMed12a, ZmMed12b, and ZmMed13 exhibiting similar expression patterns. We performed a Dissociation (Ds) insertional mutagenesis, recovering two independent insertions in the ZmMed12a gene. One of these Ds insertions results in a truncation of the ZmMed12a transcript. Our molecular characterization of the maize CDK8 module, as well as transposon tagging of ZmMed12a, establish the basis for molecular and functional studies of these important transcriptional regulators in Zea mays.

plant biology↗