bioRxiv Science⌕ Search

Biology subjects

Lopez-Valdivia, I.

Publications and source records attributed to Lopez-Valdivia, I..

8 recordsLinked to original sources

Root phenotypic plasticity improves yield stability when directed toward an adaptive integrated phenotype

Root phenotypic plasticity is often proposed to improve crop performance under stress, yet it remains unclear how much plasticity is beneficial and whether adaptive responses require changes across many traits or adjustments in few specific traits. Using public data of 6,500 field-grown maize and barley plants, this study examined the extent and distribution of root plasticity, and when it is associated with yield stability. We quantified root plasticity across nine anatomical and architectural traits using complementary statistical models and applied a feature-discovery framework to identify the drought-associated optimal integrated phenotypes and determine whether plasticity toward these phenotypes improved yield stability. More plasticity did not mean greater yield stability. Neither the number of plastic traits nor the magnitude of plastic responses predicted yield stability. Rather, we identified species-specific high-yielding, stable integrated phenotypes defined by distinct trait configurations. Critically, genotypes whose plastic responses moved their root phenotype toward these targets achieved greater yield stability, whereas movement away from them was associated with lower stability. Root plasticity is adaptive when it shifts root phenotypes towards an optimal integrated phenotype. These findings show that the value of plasticity depends on the trajectory of phenotypic change rather than its magnitude alone.

plant biology↗

Digging for meaningful connections: associations between root phenotypes and rhizosphere microbial diversity in maize

Drought threatens food security globally. Adaptive root phenotypes and microbiomes can improve maize (Zea mays L.) water uptake and tolerance to drought. However, synergisms between root phenotypes and microbiomes remain underexplored. We aimed to investigate the association between varying root phenotypes and rhizosphere microbiomes under field-scale drought. We grew 22 maize inbred lines in the field under optimal water availability and drought imposed by excluding rain with rainout shelters. We quantified grain yield and measured root architectural and anatomical phenotypes on root crown and cross-section images obtained by laser ablation tomography, respectively. We characterized rhizosphere prokaryotic and fungal communities with DNA metabarcoding of ribosomal markers. Rhizosphere microbial diversity predominantly associated with root anatomy rather than root architecture. Cortical parenchyma wall width explained 13.1% of the variance of the prokaryotic {beta}-diversity and correlated with grain yield under control conditions. Under the same conditions, number of cortical cell files and metaxylem vessels explained 1.4-2.1% of the variance of prokaryotic and fungal {beta}-diversities. No effect of the root phenotypes was observed under drought. We found 248 significant correlations between microbial taxa abundances and root anatomical phenotypes, especially cortex-related phenotypes such as number of cell files and living cortical area. Overall, a greater number of correlations was found under control conditions. We identified root phenotypes explaining a small but significant percentage of the variance of the microbial {beta}-diversity, mostly under optimal water availability. We showed that especially root anatomy is associated with rhizosphere microbial diversity in field-grown maize.

systems biology↗

A thermal time framework drives coordinated below- and above-ground development in temperate cereal crops

O_LICereal architecture is underpinned by the coordinated development of modular phytomer units. While above-ground phenology is well characterized by metrics such as the phyllochron, an equivalent framework for root system development is lacking. Because each phytomer node initiates both leaves and adventitious roots, root and shoot development are inherently linked. C_LIO_LIHere, we quantified this coordination in wheat, barley, and rye across contrasting temperature regimes and validated the results under field conditions. We introduce the rhizochron, defined as the thermal time (growing degree-days, {degrees}C d) period between the emergence of nodal roots on successive stem nodes, and the root appearance interval, describing the emergence rate of individual root axes. Root development followed a highly conserved thermal sequence synchronized with shoot phenology. C_LIO_LIAcross species and environments, the rhizochron averaged 146.1{degrees}C d, closely matching the phyllochron (126.6{degrees}C d). We also identified a consistent thermal offset, with nodal roots emerging approximately 185.3{degrees}C d after the corresponding leaf on the same phytomer node. The root appearance interval averaged 45.3{degrees}C d, reflecting continuous root deployment across active nodes. C_LIO_LIBy integrating root phenology into a node-based framework, the rhizochron provides a predictive tool for crop modeling, trait-based breeding, and more target phenotyping aimed at improving resource acquisition and climate resilience. C_LI

plant biology↗

Ploidy alters root anatomy and shapes the evolution of wheat polyploids

Polyploidization played a crucial role in crop domestication and modern agriculture. While increased cell size in polyploids is known to enhance plant biomass and vigor, its impact on soil exploration remains poorly understood. Using wheat as a model, we identify a ploidy-induced belowground domestication syndrome, characterized by (a) increased root cortical cell size reducing root respiration, nitrogen content, and phosphorus content; (b) enlarged metaxylem vessels, increasing axial hydraulic conductance; and (c) blunter root tips, limiting penetration ability in compacted soils. Our empirical and in silico experiments show that reduced root respiration and reduced cellular nutrient content in wheat polyploids improved nutrient use and acquisition efficiency under suboptimal nitrogen and phosphorus availability. These adaptations would have been advantageous in nutrient-depleted agroecosystems of the Pre-Pottery Neolithic B (PPNB) Fertile Crescent, where continuous cultivation depleted soil fertility over time. Functional-structural modeling indicates that larger cortical cells in wheat polyploids increase vacuolar occupancy, reducing root metabolic costs. Enhanced axial hydraulic conducta nce may have improved water transport, an advantage in irrigated PPNB agroecosystems. However, polyploids have blunter root tips, which reduces their penetration ability in compacted soils, making them less suited for native soils with greater mechanical impedance. We propose that root anatomical changes driven by ploidy played an important role in adaptations of wheat domesticates to PPNB agriculture. One-Sentence SummaryPolyploidy induced changes in root anatomy may have improved adaptation of wheat to Neolithic agroecosystems.

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↗

Exploring yield stability and the fitness landscape of maize landrace root phenotypes in silico

Integrated root phenotypes contribute to environmental adaptation and yield stability. We used the functional-structural plant/soil model OpenSimRoot_v2 to reconstruct the root phenotypes and environments of eight maize landraces to understand the phenotypic and environmental factors associated with broad adaptation. We found that accessions from low phosphorus regions have root phenotypes with shallow growth angles and greater nodal root numbers, allowing them to adapt to their native environments by improved topsoil foraging. We used machine learning algorithms to detect the most important phenotypes responsible for adaptation to multiple environments. The most important phene states responsible for stability across environments are large cortical cell size and reduced diameter of roots in nodes 5 and 6. When we dissected the components of root diameter, we observed that large cortical cell size improved growth by 28%, 23 % and 114%, while reduced cortical cell file number alone improved shoot growth by 137%, 66% and 216%, under drought, nitrogen and phosphorus stress, respectively. Functional-structural analysis of 96 maize landraces from the Americas, previously phenotyped in mesocosms in the greenhouse, suggested that parsimonious anatomical phenotypes, which reduce the metabolic cost of soil exploration, are the main phenotypes associated with adaptation to multiple environments, while root architectural traits were related to adaptation to specific environments. Our results indicate that integrated phenotypes with root anatomical phenes that reduce the metabolic cost of soil exploration will increase tolerance to stress across multiple environments and therefore improve yield stability, regardless of their root architecture.

plant biology↗

Cortical parenchyma wall width (CPW) regulates root metabolic cost and maize performance under suboptimal water availability

We describe how increased root cortical parenchyma wall width (CPW) can improve tolerance to drought stress in maize by reducing the metabolic costs of soil exploration. Significant variation (1.0 to 5.0 {micro}m) for CPW was observed within maize germplasm. The functional-structural model RootSlice predicts that increasing CPW from 2 to 4 {micro}m is associated with ca. 15% reduction in root cortical cytoplasmic volume, respiration rate, and nitrogen content. Analysis of genotypes with contrasting CPW grown with and without water stress in the field confirms that increased CPW is correlated with ca. 32 to 42% decrease in root respiration. Under water stress in the field, increased CPW is correlated with 125% increased stomatal conductance, 325% increased leaf CO2 assimilation rate, 73 to 78% increased shoot biomass, and 92 to 108% increased grain yield. CPW was correlated with leaf mesophyll midrib parenchyma wall width, indicating pleiotropy. GWAS analysis identified candidate genes underlying CPW. OpenSimRoot modeling predicts that a reduction in root respiration due to increased CPW would also benefit maize growth under suboptimal nitrogen, which requires empirical testing. We propose CPW as a new phene that has utility under edaphic stress meriting further investigation. Significance StatementSuboptimal water availability is a primary constraint for global crop production that is intensifying due to climate change. The metabolic cost of soil exploration is a critical factor in plant performance under suboptimal water availability. This study highlights how increased root cortical parenchyma wall width (CPW) reduces root metabolic cost and improves crop adaptation to water deficit. Modeling results also indicate that increased CPW would be beneficial under suboptimal nitrogen availability. Therefore, CPW is a promising target for breeding crops with improved water and nitrogen use efficiency.

plant biology↗

Domestication and lowland adaptation of coastal preceramic maize from Paredones, Peru

Archaeological cobs from Paredones and Huaca Prieta (Peru) are phenotypically indistinguishable from modern maize. This contrasts with the earliest Mexican macro-specimens from Guila Naquitz and San Marcos, which are phenotypically intermediate even though they date more recently in time. These observations suggest at least two alternative scenarios, one in which maize was domesticated earlier than previously thought in the lowland Mesoamerica, followed by rapid lowland dispersal to Peru, and another in which maize was independently domesticated in South America and subsequently lost, as current evidence supports a single origin for all modern maize. To gain insights into the origins of ancient Peruvian maize, we sequenced DNA from three Paredones specimens dating 6775 to 5000 calibrated years before present (BP) and conducted comparative analyses with two teosinte subspecies (Zea mays ssp. mexicana and parviglumis) and extant maize, including highland and lowland landraces from Mesoamerica and South America. We show that Paredones maize originated from the same domestication event as Mexican maize and was domesticated by 6775 BP, implying rapid dispersal followed by improvement. Paredones maize show minimal levels of gene flow from mexicana, smaller than those observed in teosinte parviglumis. It also harbors significantly fewer alleles previously found to be adaptive to highlands, but not of alleles adaptive to lowlands, supporting a lowland migration route. Our overall results imply that Paredones maize originated in Mesoamerica, arrived in Peru without mexicana introgression through a rapid lowland migration route, and underwent improvements in both Mesoamerica and South America. Significance StatementThe coastal Peruvian preceramic sites of Paredones and Huaca Prieta provide the earliest known maize macro-remains. Found more than 3,800 km away from the maize center of origin and presenting a phenotypically modern cob constitution relative to their antiquity, these specimens represent a paradox for understanding maize evolution and dispersal. We show that Paredones maize originated in Mesoamerica, like all known maize, and arrived in South America without introgression from the teosinte mexicana. Since modern maize has substantial contributions from mexicana, it raises the question of when mexicana introgression spread to South America. Paredones maize preferentially shares adaptive allelic diversity with lowland Mesoamerican samples, suggesting a migration route probably associated with a coastal corridor previously identified with archeological findings.

plant biology↗