Root-zone hypoxia reduces growth of the tropical forage grass Urochloa humidicola in high-nutrient but not low-nutrient conditions

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Abstract

BACKGROUND AND AIMS: The perennial C4 grass Urochloa humidicola is widely planted on infertile acidic and waterlogging-prone soils of tropical America. Waterlogging results in soil anoxia, and O2 deficiency can reduce nutrient uptake by roots. Interestingly, both nutrient deficiencies and soil waterlogging can enhance root cortical cell senescence, and the increased gas-filled porosity facilitates internal aeration of roots. We tested the influence of nutrient supply and root-zone O2 on root traits, leaf nutrient concentrations and growth of U. humidicola. METHODS: Plants were grown in pots in a completely randomized design under aerated or stagnant deoxygenated hydroponic conditions and six nutrient regimes, with low to high concentrations of all essential elements, for 28 d in a controlled-temperature greenhouse. The standard acid solution (SAS) used was previously designed based on infertile acidic soils of the tropical America savannas, and step increases in the concentration of SAS were used in aerated or deoxygenated 0.1 % agar solution, which mimics changes in gas composition in waterlogged soils. Measurements included shoot and root growth, root porosity, root anatomy, radial O2 loss, and leaf tissue nutrient concentrations. KEY RESULTS: Shoot dry mass was reduced for plants in stagnant compared with aerated conditions at high, but not at low, levels of mineral nutrition. In low-nutrition stagnant solution, roots were shorter, of greater porosity and had smaller radial thickness of the stele. Suberized lamellae and lignified sclerenchyma, as well as a strong barrier to radial O2 loss, were documented for roots from all treatments. Leaf nutrient concentrations of K, Mg and Ca (but not N, P and S) were higher in aerated than in stagnant conditions. CONCLUSIONS: Under low-nutrient conditions, plant growth in stagnant solution was equal to that in aerated solution, whereas under higher-nutrient regimes growth increased but dry mass in stagnant solution was less than in aerated solution. Slow growth in low-nutrient conditions limited any further response to the low O2 treatment, and greater porosity and smaller stele size in roots would enhance internal O2 movement within roots in the nutrient-limited stagnant conditions. A constitutive barrier to radial O2 loss and aerenchyma facilitates O2 movement to the tips of roots, which presumably contributes to maintaining nutrient uptake and the tolerance of U. humidicola to low O2 in the root-zone.

Original languageEnglish
Pages (from-to)1019-1032
Number of pages14
JournalAnnals of Botany
Volume124
Issue number6
DOIs
Publication statusPublished - 27 Nov 2019

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Urochloa humidicola
forage grasses
hypoxia
rhizosphere
nutrients
porosity
flooded conditions
stele
nutrient content
nutrient uptake
gases
leaves
sclerenchyma
soil
shoots
tropical soils
acids
nutrient deficiencies
plant nutrition
aeration

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@article{2144180af38e47fe82bc7aba6b7a9fe3,
title = "Root-zone hypoxia reduces growth of the tropical forage grass Urochloa humidicola in high-nutrient but not low-nutrient conditions",
abstract = "BACKGROUND AND AIMS: The perennial C4 grass Urochloa humidicola is widely planted on infertile acidic and waterlogging-prone soils of tropical America. Waterlogging results in soil anoxia, and O2 deficiency can reduce nutrient uptake by roots. Interestingly, both nutrient deficiencies and soil waterlogging can enhance root cortical cell senescence, and the increased gas-filled porosity facilitates internal aeration of roots. We tested the influence of nutrient supply and root-zone O2 on root traits, leaf nutrient concentrations and growth of U. humidicola. METHODS: Plants were grown in pots in a completely randomized design under aerated or stagnant deoxygenated hydroponic conditions and six nutrient regimes, with low to high concentrations of all essential elements, for 28 d in a controlled-temperature greenhouse. The standard acid solution (SAS) used was previously designed based on infertile acidic soils of the tropical America savannas, and step increases in the concentration of SAS were used in aerated or deoxygenated 0.1 {\%} agar solution, which mimics changes in gas composition in waterlogged soils. Measurements included shoot and root growth, root porosity, root anatomy, radial O2 loss, and leaf tissue nutrient concentrations. KEY RESULTS: Shoot dry mass was reduced for plants in stagnant compared with aerated conditions at high, but not at low, levels of mineral nutrition. In low-nutrition stagnant solution, roots were shorter, of greater porosity and had smaller radial thickness of the stele. Suberized lamellae and lignified sclerenchyma, as well as a strong barrier to radial O2 loss, were documented for roots from all treatments. Leaf nutrient concentrations of K, Mg and Ca (but not N, P and S) were higher in aerated than in stagnant conditions. CONCLUSIONS: Under low-nutrient conditions, plant growth in stagnant solution was equal to that in aerated solution, whereas under higher-nutrient regimes growth increased but dry mass in stagnant solution was less than in aerated solution. Slow growth in low-nutrient conditions limited any further response to the low O2 treatment, and greater porosity and smaller stele size in roots would enhance internal O2 movement within roots in the nutrient-limited stagnant conditions. A constitutive barrier to radial O2 loss and aerenchyma facilitates O2 movement to the tips of roots, which presumably contributes to maintaining nutrient uptake and the tolerance of U. humidicola to low O2 in the root-zone.",
keywords = "Urochloa humidicola, leaf tissue nutrient concentrations, mineral nutrition, root anatomy, root porosity, root radial oxygen loss, root:shoot ratio, Tropical forage grass, waterlogging tolerance",
author = "Jim{\'e}nez, {Juan de la Cruz} and Lukasz Kotula and Veneklaas, {Erik J.} and Colmer, {Timothy D.}",
year = "2019",
month = "11",
day = "27",
doi = "10.1093/aob/mcz071",
language = "English",
volume = "124",
pages = "1019--1032",
journal = "Annals of Botany",
issn = "0305-7364",
publisher = "OXFORD UNIV PRESS UNITED KINGDOM",
number = "6",

}

TY - JOUR

T1 - Root-zone hypoxia reduces growth of the tropical forage grass Urochloa humidicola in high-nutrient but not low-nutrient conditions

AU - Jiménez, Juan de la Cruz

AU - Kotula, Lukasz

AU - Veneklaas, Erik J.

AU - Colmer, Timothy D.

PY - 2019/11/27

Y1 - 2019/11/27

N2 - BACKGROUND AND AIMS: The perennial C4 grass Urochloa humidicola is widely planted on infertile acidic and waterlogging-prone soils of tropical America. Waterlogging results in soil anoxia, and O2 deficiency can reduce nutrient uptake by roots. Interestingly, both nutrient deficiencies and soil waterlogging can enhance root cortical cell senescence, and the increased gas-filled porosity facilitates internal aeration of roots. We tested the influence of nutrient supply and root-zone O2 on root traits, leaf nutrient concentrations and growth of U. humidicola. METHODS: Plants were grown in pots in a completely randomized design under aerated or stagnant deoxygenated hydroponic conditions and six nutrient regimes, with low to high concentrations of all essential elements, for 28 d in a controlled-temperature greenhouse. The standard acid solution (SAS) used was previously designed based on infertile acidic soils of the tropical America savannas, and step increases in the concentration of SAS were used in aerated or deoxygenated 0.1 % agar solution, which mimics changes in gas composition in waterlogged soils. Measurements included shoot and root growth, root porosity, root anatomy, radial O2 loss, and leaf tissue nutrient concentrations. KEY RESULTS: Shoot dry mass was reduced for plants in stagnant compared with aerated conditions at high, but not at low, levels of mineral nutrition. In low-nutrition stagnant solution, roots were shorter, of greater porosity and had smaller radial thickness of the stele. Suberized lamellae and lignified sclerenchyma, as well as a strong barrier to radial O2 loss, were documented for roots from all treatments. Leaf nutrient concentrations of K, Mg and Ca (but not N, P and S) were higher in aerated than in stagnant conditions. CONCLUSIONS: Under low-nutrient conditions, plant growth in stagnant solution was equal to that in aerated solution, whereas under higher-nutrient regimes growth increased but dry mass in stagnant solution was less than in aerated solution. Slow growth in low-nutrient conditions limited any further response to the low O2 treatment, and greater porosity and smaller stele size in roots would enhance internal O2 movement within roots in the nutrient-limited stagnant conditions. A constitutive barrier to radial O2 loss and aerenchyma facilitates O2 movement to the tips of roots, which presumably contributes to maintaining nutrient uptake and the tolerance of U. humidicola to low O2 in the root-zone.

AB - BACKGROUND AND AIMS: The perennial C4 grass Urochloa humidicola is widely planted on infertile acidic and waterlogging-prone soils of tropical America. Waterlogging results in soil anoxia, and O2 deficiency can reduce nutrient uptake by roots. Interestingly, both nutrient deficiencies and soil waterlogging can enhance root cortical cell senescence, and the increased gas-filled porosity facilitates internal aeration of roots. We tested the influence of nutrient supply and root-zone O2 on root traits, leaf nutrient concentrations and growth of U. humidicola. METHODS: Plants were grown in pots in a completely randomized design under aerated or stagnant deoxygenated hydroponic conditions and six nutrient regimes, with low to high concentrations of all essential elements, for 28 d in a controlled-temperature greenhouse. The standard acid solution (SAS) used was previously designed based on infertile acidic soils of the tropical America savannas, and step increases in the concentration of SAS were used in aerated or deoxygenated 0.1 % agar solution, which mimics changes in gas composition in waterlogged soils. Measurements included shoot and root growth, root porosity, root anatomy, radial O2 loss, and leaf tissue nutrient concentrations. KEY RESULTS: Shoot dry mass was reduced for plants in stagnant compared with aerated conditions at high, but not at low, levels of mineral nutrition. In low-nutrition stagnant solution, roots were shorter, of greater porosity and had smaller radial thickness of the stele. Suberized lamellae and lignified sclerenchyma, as well as a strong barrier to radial O2 loss, were documented for roots from all treatments. Leaf nutrient concentrations of K, Mg and Ca (but not N, P and S) were higher in aerated than in stagnant conditions. CONCLUSIONS: Under low-nutrient conditions, plant growth in stagnant solution was equal to that in aerated solution, whereas under higher-nutrient regimes growth increased but dry mass in stagnant solution was less than in aerated solution. Slow growth in low-nutrient conditions limited any further response to the low O2 treatment, and greater porosity and smaller stele size in roots would enhance internal O2 movement within roots in the nutrient-limited stagnant conditions. A constitutive barrier to radial O2 loss and aerenchyma facilitates O2 movement to the tips of roots, which presumably contributes to maintaining nutrient uptake and the tolerance of U. humidicola to low O2 in the root-zone.

KW - Urochloa humidicola

KW - leaf tissue nutrient concentrations

KW - mineral nutrition

KW - root anatomy

KW - root porosity

KW - root radial oxygen loss

KW - root:shoot ratio

KW - Tropical forage grass

KW - waterlogging tolerance

UR - http://www.scopus.com/inward/record.url?scp=85075805477&partnerID=8YFLogxK

U2 - 10.1093/aob/mcz071

DO - 10.1093/aob/mcz071

M3 - Article

VL - 124

SP - 1019

EP - 1032

JO - Annals of Botany

JF - Annals of Botany

SN - 0305-7364

IS - 6

ER -