bioRxiv Science⌕ Search

Biology subjects

Perez-Limon, S.

Publications and source records attributed to Perez-Limon, S..

9 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↗

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↗

The genetic architecture of leaf vein density traits and its importance for photosynthesis in maize

O_LILeaf venation density has significantly increased during plant evolution. Higher densities are observed in angiosperms compared to early land plants, and among angiosperms, recently diverged C4 species have the highest values. This has allowed leaves to increase water conductance, transpiration and possibly photosynthesis. Despite its importance, the genetic architecture of this trait is not well characterized and its relationship with photosynthesis has not been clearly established. C_LIO_LIUsing native Mexican varieties of maize adapted to a wide range of environmental conditions, we show that vein density is variable and plastic. We leverage this variation to perform correlation analyses with photosynthetic rates and to map genetic regions associated with vein patterning traits using a MAGIC population. C_LIO_LIOur results show that higher vein densities are correlated with higher photosynthetic rates, but only for small intermediate veins. Varieties adapted to drier environments can substantially increase vein density in response to heat, suggesting a role in water use efficiency. We further detected 12 QTLs associated with vein patterning and identified candidate genes related to small intermediate vein development. C_LIO_LIThese findings have implications for understanding vein architecture evolution, particularly that of C4 plants, which have significantly higher photosynthetic efficiency and productivity under warm and dry conditions. C_LI

plant biology↗

In silico analysis of the evolution of root phenotypes during maize domestication in Neolithic soils of Tehuacan

Roots are essential for plant adaptation to changing environments, yet the role of roots in crop domestication remains unclear. This study examines the evolution of root phenotypes from teosinte to maize, a transition resulting in reduced nodal root number (NRN), multiseriate cortical sclerenchyma (MCS), and increased seminal root number (SRN). We reconstructed the root phenotypes of maize and teosinte, as well as the environments of the Tehuacan Valley over the last 18,000 years using a combination of ancient DNA, paleobotany, and functional-structural modeling. Our models reveal that increasing Holocene atmospheric CO2 concentrations favored the appearance of reduced NRN and MCS between 12000 to 8000 years before present (yBP), promoting deeper root systems. The advent of irrigation by 6000 yBP switched nitrogen distribution from topsoil to subsoil domains, a change which increased the utility of reduced NRN and MCS. Comparison of allelic frequencies among ancient samples ranging from 5500 to 500 yBP suggest that increased SRN may have appeared around 3500 yBP, coinciding with a period of increased human population, agricultural intensification, and soil degradation. Our results suggest that root phenotypes that enhance plant performance under nitrogen stress were important for maize adaptation to changing agricultural practices in the Tehuacan Valley. ClassificationPhysiology & Development

plant biology↗

Mycorrhizal status impacts the genetic architecture of mineral accumulation in field grown maize (Zea mays ssp. mays L.)

Arbuscular mycorrhizal fungi (AMF) establish symbioses with major crop species, providing their hosts with greater access to mineral nutrients and promoting tolerance to heavy metal toxicity. There is considerable interest in AMF as biofertilizers and for their potential in breeding for greater nutrient efficiency and stress tolerance. However, it remains a challenge to estimate the nutritional benefits of AMF in the field, in part due to a lack of suitable AMF-free controls. Here we evaluated the impact of AMF on the concentration of 20 elements in the leaves and grain of field grown maize using a custom genetic mapping population in which half of the families carry the AMF-incompatibility mutation castor. By comparing AMF-compatible and AMF-incompatible families, we confirmed the benefits of AMF in increasing the concentration of essential mineral nutrients (e.g., P, Zn, and Cu) and reducing the concentration of toxic elements (e.g., Cd and As) in a medium-input subtropical field. We characterised the genetic architecture of element concentration using quantitative trait mapping and identified loci that were specific to AMF-compatible or AMF-incompatible families, consistent with their respective involvement in mycorrhizal or direct nutrient uptake. Patterns of element covariance changed depending on AMF status and could be used to predict variation in mycorrhizal colonisation. We comment on the potential of AMF to drive genotype-specific differences in the host ionome across fields and to impact the alignment of biofortification breeding targets. Our results highlight the benefits of AMF in improving plant access to micronutrients while protecting from heavy metals, and indicate the potential benefits of considering AMF in biofortification programs.

plant biology↗

A B73 x Palomero Toluqueo mapping population reveals local adaptation in Mexican highland maize

Generations of farmer selection have produced a unique collection of traditional maize varieties adapted to the environmental challenges of the central Mexican highlands. In addition to agronomic and cultural value, Mexican highland maize represents a good system for the study of local adaptation and acquisition of adaptive phenotypes under cultivation. In this study, we characterized a recombinant inbred line population derived from the cross of the B73 reference line and the Mexican highland maize variety Palomero Toluqueno. Evaluation over multiple years in lowland and highland field sites in Mexico identified genomic regions linked to yield components and putatively adaptive morphological traits. A region on chromosome 7 associated with ear weight showed antagonistic allelic effects in lowland and highland fields, suggesting a trade-off consistent with local adaptation. We identified several alleles of highland origin associated with characteristic highland traits, including reduced tassel branching, increased stem pigmentation and the presence of stem macrohairs. The oligogenic architecture of characteristic morphological traits supports their role in adaptation, suggesting they have arisen from consistent directional selection acting at distinct points across the genome. We discuss these results in the context of the origin of phenotypic novelty during selection, commenting on the role of de novo mutation and the acquisition of adaptive variation by gene flow from endemic wild relatives.

plant biology↗

Teosinte introgression modulates phosphatidylcholine levels and induces early maize flowering time

Native Americans domesticated maize (Zea mays ssp. mays) from lowland teosinte parviglumis (Zea mays ssp.parviglumis) in the warm Mexican southwest and brought it to the highlands of Mexico and South America where it was exposed to lower temperatures that imposed strong selection on flowering time. Phospholipids are important metabolites in plant responses to low-temperature and phosphorus availability, and have been suggested to influence flowering time. Here, we combined linkage mapping with genome scans to identify High PhosphatidylCholine 1 (HPC1), a gene that encodes a phospholipase A1 enzyme, as a major driver of phospholipid variation in highland maize. Common garden experiments demonstrated strong genotype-by-environment interactions associated with variation at HPC1, with the highland HPC1 allele leading to higher fitness in highlands, possibly by hastening flowering. The highland maize HPC1 variant resulted in impaired function of the encoded protein due to a polymorphism in a highly conserved sequence. A meta-analysis across HPC1 orthologs indicated a strong association between the identity of the amino acid at this position and optimal growth in prokaryotes. Mutagenesis of HPC1 via genome editing validated its role in regulating phospholipid metabolism. Finally, we showed that the highland HPC1 allele entered cultivated maize by introgression from the wild highland teosinte Zea mays ssp. mexicana and has been maintained in maize breeding lines from the Northern US, Canada and Europe. Thus, HPC1 introgressed from teosinte mexicana underlies a large metabolic QTL that modulates phosphatidylcholine levels and has an adaptive effect at least in part via induction of early flowering time.

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↗