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Growth is required for perception of water availability to pattern root branches in plants.

ABSTRACT: Water availability is a potent regulator of plant development and induces root branching through a process termed hydropatterning. Hydropatterning enables roots to position lateral branches toward regions of high water availability, such as wet soil or agar media, while preventing their emergence where water is less available, such as in air. The mechanism by which roots perceive the spatial distribution of water during hydropatterning is unknown. Using primary roots of Zea mays (maize) we reveal that developmental competence for hydropatterning is limited to the growth zone of the root tip. Past work has shown that growth generates gradients in water potential across an organ when asymmetries exist in the distribution of available water. Using mathematical modeling, we predict that substantial growth-sustained water potential gradients are also generated in the hydropatterning competent zone and that such biophysical cues inform the patterning of lateral roots. Using diverse chemical and environmental treatments we experimentally demonstrate that growth is necessary for normal hydropatterning of lateral roots. Transcriptomic characterization of the local response of tissues to a moist surface or air revealed extensive regulation of signaling and physiological pathways, some of which we show are growth-dependent. Our work supports a "sense-by-growth" mechanism governing hydropatterning, by which water availability cues are rendered interpretable through growth-sustained water movement.

SUBMITTER: Robbins NE

PROVIDER: S-EPMC5789911 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Growth is required for perception of water availability to pattern root branches in plants.

Robbins Neil E NE Dinneny José R JR

Proceedings of the National Academy of Sciences of the United States of America 20180109 4

Water availability is a potent regulator of plant development and induces root branching through a process termed hydropatterning. Hydropatterning enables roots to position lateral branches toward regions of high water availability, such as wet soil or agar media, while preventing their emergence where water is less available, such as in air. The mechanism by which roots perceive the spatial distribution of water during hydropatterning is unknown. Using primary roots of <i>Zea mays</i> (maize) w ...[more]

PMID: 29317538

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Project description:BackgroundDeeper roots help plants take up available resources in deep soil ensuring better growth and higher yields under conditions of drought. A large-scale semi-field root phenotyping facility was developed to allow a water availability gradient and detect potential interaction of genotype by water availability gradient. Genotyped winter wheat lines were grown as rows in four beds of this facility, where indirect genetic effects from neighbors could be important to trait variation. The objective was to explore the possibility of genomic prediction for grain-related traits and deep root traits collected via images taken in a minirhizotron tube under each row of winter wheat measured.ResultsThe analysis comprised four grain-related traits: grain yield, thousand-kernel weight, protein concentration, and total nitrogen content measured on each half row that were harvested separately. Two root traits, total root length between 1.2 and 2 m depth and root length in four intervals on each tube were also analyzed. Two sets of models with or without the effects of neighbors from both sides of each row were applied. No interaction between genotypes and changing water availability were detected for any trait. Estimated genomic heritabilities ranged from 0.263 to 0.680 for grain-related traits and from 0.030 to 0.055 for root traits. The coefficients of genetic variation were similar for grain-related and root traits. The prediction accuracy of breeding values ranged from 0.440 to 0.598 for grain-related traits and from 0.264 to 0.334 for root traits. Including neighbor effects in the model generally increased the estimated genomic heritabilities and accuracy of predicted breeding values for grain yield and nitrogen content.ConclusionsSimilar relative amounts of additive genetic variance were found for both yield traits and root traits but no interaction between genotypes and water availability were detected. It is possible to obtain accurate genomic prediction of breeding values for grain-related traits and reasonably accurate predicted breeding values for deep root traits using records from the semi-field facility. Including neighbor effects increased the estimated additive genetic variance of grain-related traits and accuracy of predicting breeding values. High prediction accuracy can be obtained although heritability is low.

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Growth is required for perception of water availability to pattern root branches in plants.

Publications

Growth is required for perception of water availability to pattern root branches in plants.

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