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Sawers, R.

Publications and source records attributed to Sawers, R..

6 recordsLinked to original sources

The teosinte mexicana chromosomal inversion Inv4m modulates maize flowering time, plant height, and growth regulation gene networks

Chromosomal inversions facilitate local adaptation by maintaining co-adapted allele complexes as a single inherited unit, but the genes driving their phenotypic effects are rarely identified. Inv4m is an inversion from the highland teosinte Zea mays ssp. mexicana that is nearly fixed at 2500 masl in Mexican traditional varieties but absent in temperate maize. While association studies link Inv4m to flowering time, its key adaptive trait, the mechanisms connecting it to this phenotype remain unknown. Here, we generate near isogenic lines by introgressing the highland Michoacan 21 (Mi21) Inv4m haplotype into temperate B73 through eight backcross generations. We assemble the Inv4m-Mi21 NIL genome and, aligning to three Zea reference genomes, provide the first precise delimitation of Inv4m, a 15.2 Mb region with breakpoints overlapping knob repeat arrays. In field trials across Pennsylvania and North Carolina, Inv4m consistently accelerated flowering, whereas its plant height effect reversed sign between regions, a genotype by environment interaction consistent with environment-dependent fitness. Using RNA-seq, we identify 465 differentially expressed genes, the strongest from a cluster of JUMONJI histone demethylases (JMJ). Comparing five Zea genomes, the B73 reference carries a lineage-specific tandem expansion of five JMJ paralogs while highland genotypes carrying Inv4m retain a single ancestral copy, a difference that accounts for most of the clusters differential expression. We then show Inv4m disrupts growth related coexpression modules, with the JMJ cluster losing connectivity, and traced a trans regulatory network linking it to cell proliferation genes including pcna2 and sec6. In summary, we identify candidate genes and networks underlying Inv4ms effects and propose that part of this inversions adaptive value may reside in a dosage-sensitive regulator whose action propagates through a downstream network of genes that are involved in growth and flowering and are important for highland adaptation. Recombination suppression may thus protect a co-adapted regulatory architecture rather than independent alleles alone. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=194 HEIGHT=200 SRC="FIGDIR/small/732082v1_ufig1.gif" ALT="Figure 1"> View larger version (106K): org.highwire.dtl.DTLVardef@85400org.highwire.dtl.DTLVardef@c2f820org.highwire.dtl.DTLVardef@301c0aorg.highwire.dtl.DTLVardef@80e715_HPS_FORMAT_FIGEXP M_FIG C_FIG

Plant Biology↗

Uncoupling the Effects of Highland Maize Chromosomal Inversion Inv4m from Leaf Phosphorus Deficiency Responses

Local adaptation of a species involves the selection of adaptive alleles that confer a fitness advantage in their local environment. Inversions prevent recombination between the standard and inverted heterozygous hybrids. Inversions can play a crucial role in local adaptation by locking together a set of co-adapted alleles, acting as supergenes. Inv4m is a 13 Mb inversion in maize prevalent in highland maize and highland wild relatives from Mexico. Maize from the highlands of the Trans-Mexican volcanic belt has been shown to be well-adapted to volcanic, acidic soils with low phosphorus availability. Inv4m carries several genes involved in P acquisition and utilization. We therefore tested the hypothesis that Inv4m contributes to maize adaptation to these environments through enhanced phosphorus acquisition or utilization. Alternatively, Inv4m possible adaptive value may operate through constitutive developmental effects independent of nutrient stress responses. To test this hypothesis, we introgressed a highland maize variety from the highlands of Michoacan, Mexico, carrying Inv4m into the temperate line B73 and developed Near-Introgression Lines (NILs) carrying Inv4m. We then grew NILs carrying the inversion and controls without it in soils with different phosphorus levels and evaluated the fitness effects of the inversion, as well as changes in gene expression using RNA-Seq. Our results show that P starvation elicits highly conserved transcriptomic, lipidomic, and ionomic responses, independently of the Inv4m inversion genotype. Therefore, phosphorus deficiency does not seem to be driving the adaptive value of Inv4m. Additionally, we observed a phosphorus modulated transcriptional gradient from the collar leaf downward, characterized by a decrease in the expression of photosynthesis genes and an increase in the expression of senescence-associated genes, corresponding to the positional onset and initial stages of sequential leaf senescence. Although the magnitude of the phosphorus response increased with leaf age, we did not observe significant interactions with Inv4m. Our multi-omics analysis of the maize phosphorus starvation response identified and characterized two coordinately regulated molecular programs, light harvesting shutdown and accelerated senescence, whose deployment depends on leaf developmental stage, with older leaves below the collar integrating nutrient limitation into the natural progression toward senescence.

plant biology↗

Evidence that variation in root anatomy contributes to local adaptation in Mexican native maize

Mexican native maize (Zea mays ssp. mays) is adapted to a wide range of climatic and edaphic conditions. Here, we focus specifically on the potential role of root anatomical variation in this adaptation. In light of the investment required to characterize root anatomy, we present a machine learning approach using environmental descriptors to project trait variation from a relatively small training panel onto a larger panel of genotyped and georeferenced Mexican maize accessions. The resulting models defined potential biologically relevant clines across a complex environment and were used subsequently in genotype-environment association. We found evidence of systematic variation in maize root anatomy across Mexico, notably a prevalence of trait combinations favoring a reduction in axial conductance in cooler, drier highland areas. We discuss our results in the context of previously described water-banking strategies and present candidate genes that are associated with both root anatomical and environmental variation. Our strategy is a refinement of standard environmental genome wide association analysis that is applicable whenever a training set of georeferenced phenotypic data is available.

plant biology↗

Allele-specific expression reveals multiple paths to highland adaptation in maize

Maize is a staple food of smallholder farmers living in highland regions up to 4,000 meters above sea level worldwide. Mexican and South American highlands are two major highland maize growing regions, and population genetic data suggests the maizes adaptation to these regions occurred largely independently, providing a case study for parallel evolution. To better understand the mechanistic basis of highland adaptation, we crossed maize landraces from 108 highland and lowland sites of Mexico and South America with the inbred line B73 to produce F1 hybrids and grew them in both highland and lowland sites in Mexico. We identified thousands of genes with divergent expression between highland and lowland populations. Hundreds of these genes show patterns of convergent evolution between Mexico and South America. To dissect the genetic architecture of the divergent gene expression, we developed a novel allele-specific expression analysis pipeline to detect genes with divergent functional cis-regulatory variation between highland and lowland populations. We identified hundreds of genes with divergent cis-regulation between highland and lowland landrace alleles, with 20 in common between regions, further suggesting convergence in the genes underlying highland adaptation. Further analyses suggest multiple mechanisms contribute to this convergence. Our findings reveal a complex genetic architecture of cis-regulatory alleles underlying adaptation to highlands in maize. Although the vast majority of evolutionary changes associated with highland adaptation were region-specific, our findings highlight an important role for convergence at the gene expression and gene regulation levels as well.

evolutionary biology↗

Gene regulatory effects of a large chromosomal inversion in highland maize

Chromosomal inversions play an important role in local adaptation. Inversions can capture multiple locally adaptive functional variants in a linked block by repressing recombination. However, this recombination suppression makes it difficult to identify the genetic mechanisms that underlie an inversions role in adaption. In this study, we explore how large-scale transcriptomic data can be used to dissect the functional importance of a 13 Mb inversion locus (Inv4m) found almost exclusively in highland populations of maize (Zea mays ssp. mays). Inv4m introgressed into highland maize from the wild relative Zea mays ssp. mexicana, also present in the highlands of Mexico, and is thought to be important for the adaptation of these populations to cultivation in highland environments. First, using a large publicly available association mapping panel, we confirmed that Inv4m is associated with locally adaptive agronomic phenotypes, but only in highland fields. Second, we created two families segregating for standard and inverted haplotypess of Inv4m in a isogenic B73 background, and measured gene expression variation association with Inv4m across 9 tissues in two experimental conditions. With these data, we quantified both the global transcriptomic effects of the highland Inv4m haplotype, and the local cis-regulatory variation present within the locus. We found diverse physiological effects of Inv4m, and speculate that the genetic basis of its effects on adaptive traits is distributed across many separate functional variants. Author SummaryChromosomal inversions are an important type of genomic structural variant. However, mapping causal alleles within their boundaries is difficult because inversions suppress recombination between homologous chromosomes. This means that inversions, regardless of their size, are inherited as a unit. We leveraged the high-dimensional phenotype of gene expression as a tool to study the genetics of a large chromosomal inversion found in highland maize populations in Mexico - Inv4m. We grew plants carrying multiple versions of Inv4m in a common genetic background, and quantified the transcriptional reprogramming induced by alternative alleles at the locus. Inv4m has been shown in previous studies to have a large effect on flowering, but we show that the functional variation within Inv4m affects many developmental and physiological processes. Author ContributionsT. Crow, R. Rellan-Alvarez, R. Sawers and D. Runcie conceived and designed the experiment. M. Aguilar-Rangel, J. Rodr[g]uez, R. Rellan-Alvarez and R. Sawers generated the segregating families. T. Crow, J. Ta, S. Nojoomi, M. Aguilar-Rangel, J. Rodr[g]uez D. Gates, D. Runcie performed the experiment. T. Crow, D. Gates, D. Runcie analyzed the data. T. Crow, D. Runcie wrote the original manuscript, and R. Rellan-Alvarez and R. Sawers provided review and editing.

genomics↗

Coordinated Changes In The Accumulation Of Metal Ions In Maize (Zea mays ssp. mays L.) In Response To Inoculation With The Arbuscular Mycorrhizal Fungus Funneliformis mosseae

Arbuscular mycorrhizal symbiosis is an ancient interaction between plants and fungi of the phylum Glomeromycota. In exchange for photosynthetically fixed carbon, the fungus provides the plant host with greater access to soil nutrients via an extensive network of root-external hyphae. Here, to determine the impact of the symbiosis on the host ionome, the concentration of nineteen elements was determined in the roots and leaves of a panel of thirty maize varieties, grown under phosphorus limiting conditions, with, or without, inoculation with the fungus Funneliformis mosseae. Although the most recognized benefit of the symbiosis to the host plant is greater access to soil phosphorus, the concentration of a number of other elements responded significantly to inoculation across the panel as a whole. In addition, variety-specific effects indicated the importance of plant genotype to the response. Clusters of elements were identified that varied in a coordinated manner across genotypes, and that were maintained between non-inoculated and inoculated plants.\n\nAbbreviations

plant biology↗