Root length is proxy for high-throughput screening of waterlogging tolerance in Urochloa spp. grasses
Juan de la Cruz Jiménez
A F , Juan A. Cardoso B , Lukasz Kotula A , Erik J. Veneklaas A C D , Ole Pedersen A E and Timothy D. Colmer A D
+ Author Affiliations
- Author Affiliations
A UWA School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B International Center for Tropical Agriculture (CIAT), Km 17 Recta Cali – Palmira, Colombia.
C UWA School of Biological Sciences, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
D The Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
E Department of Biology, University of Copenhagen, Universitetsparken 4, 3rd floor, 2100 Copenhagen, Denmark.
F Corresponding author. Email: juan.jimenezserna@research.uwa.edu.au
Functional Plant Biology - https://doi.org/10.1071/FP20200
Submitted: 9 July 2020 Accepted: 10 November 2020 Published online: 8 December 2020
Abstract
C4 perennial Urochloa spp. grasses are widely planted in extensive areas in the tropics. These areas are continuously facing waterlogging events, which limits plant growth and production. However, no commercial cultivar combining excellent waterlogging tolerance with superior biomass production and nutritional quality is available. The objective of this study was to identify root traits that can be used for selecting waterlogging tolerant species of Urochloa. Root respiration, root morphological, architectural and anatomical traits were evaluated in eight contrasting Urochloa spp. genotypes grown under aerated or deoxygenated stagnant solutions. Moreover, modelling of internal aeration was used to relate differences in root traits and root growth in waterlogged soils. Increased aerenchyma formation in roots, reduced stele area and development of a fully suberised exodermis are characteristics improving internal aeration of roots and therefore determining waterlogging tolerance in these C4 forage grasses. Waterlogging-tolerant genotypes had steeper root angles and greater root lengths than the waterlogging-sensitive genotypes. In stagnant conditions, waterlogging-tolerant genotypes had a greater proportion of aerenchyma and reduced stele area in root cross-sections, had deeper roots, steeper root angle and larger root biomass, which in turn, allowed for greater shoot biomass. Total root length had the strongest positive influence on shoot dry mass and can therefore be used as proxy for selecting waterlogging tolerant Urochloa genotypes.
Keywords: abiotic stress, lignin, radial oxygen loss, root anatomy, root angle, root internal aeration, root length modelling, root respiration, suberin, tropical grasses, Urochloa spp., waterlogging.
References
Abiko T, Kotula L, Shiono K, Malik AI, Colmer TD, Nakazono M (2012) Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). Plant, Cell & Environment 35, 1618–1630.| Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays).Crossref | GoogleScholarGoogle Scholar |
Aguilar EA, Turner DW, Gibbs DJ, Armstrong W, Sivasithamparam K (2003) Oxygen distribution and movement, respiration and nutrient loading in banana roots (Musa spp. L.) subjected to aerated and oxygen-depleted environments. Plant and Soil 253, 91–102.
| Oxygen distribution and movement, respiration and nutrient loading in banana roots (Musa spp. L.) subjected to aerated and oxygen-depleted environments.Crossref | GoogleScholarGoogle Scholar |
Ali ML, Luetchens J, Nascimento J, Shaver TM, Kruger GR, Lorenz AJ (2015) Genetic variation in seminal and nodal root association with grain yield of maize under conditions. Plant and Soil 397, 213–225.
| Genetic variation in seminal and nodal root association with grain yield of maize under conditions.Crossref | GoogleScholarGoogle Scholar |
Anzooman M, Christopher J, Dang YP, Taylor J, Menzies NW, Kopittke PM (2019) Chemical and physical influence of sodic soils on the coleoptile length and root growth angle of wheat genotypes. Annals of Botany 124, 1043–1052.
| Chemical and physical influence of sodic soils on the coleoptile length and root growth angle of wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 31175829PubMed |
Armstrong W (1979). Aeration in higher plants. In ‘Advances in botanical research’. (Ed. HW Woolhouse) pp. 225–332. (Academic Press: London, UK)
Armstrong W, Beckett PM (1987) Internal aeration and the development of stelar anoxia in submerged roots: multi-shelled mathematical model combining axial diffusion of oxygen in the cortex with radial losses to the stele, the wall layers and the rhizosphere. New Phytologist 105, 221–245.
| Internal aeration and the development of stelar anoxia in submerged roots: multi-shelled mathematical model combining axial diffusion of oxygen in the cortex with radial losses to the stele, the wall layers and the rhizosphere.Crossref | GoogleScholarGoogle Scholar |
Armstrong W, Drew MC (2002). Root growth and metabolism under oxygen deficiency. In ‘Plant roots: the hidden half’, 3rd edn. (Eds Y Waisel, A Eshel, U Kafkafi) pp. 729–761. (Marcel Dekker: New York, USA)
Armstrong W, Webb T (1985) A critical oxygen pressure for root extension in rice. Journal of Experimental Botany 36, 1573–1582.
| A critical oxygen pressure for root extension in rice.Crossref | GoogleScholarGoogle Scholar |
Armstrong W, Healy MT, Lythe S (1983) Oxygen diffusion in pea II. Oxygen concentrations in the primary pea root apex as affected by growth, the production of laterals and radial oxygen loss. New Phytologist 94, 549–559.
| Oxygen diffusion in pea II. Oxygen concentrations in the primary pea root apex as affected by growth, the production of laterals and radial oxygen loss.Crossref | GoogleScholarGoogle Scholar |
Armstrong W, Justin SHFW, Beckett PM, Lythe S (1991) Root adaptation to soil waterlogging. Aquatic Botany 39, 57–73.
| Root adaptation to soil waterlogging.Crossref | GoogleScholarGoogle Scholar |
Brundrett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with sudan red 7B or fluorol yellow 088 in polyethylene glycol-glycerol. Biotechnic & Histochemistry 66, 111–116.
| Efficient lipid staining in plant material with sudan red 7B or fluorol yellow 088 in polyethylene glycol-glycerol.Crossref | GoogleScholarGoogle Scholar |
Cardoso JA, Rincón J, Jiménez JC, Noguera D, Rao IM (2013) Morpho-anatomical adaptations to waterlogging by germplasm accessions in a tropical forage grass. AoB PLANTS 5, plt047
| Morpho-anatomical adaptations to waterlogging by germplasm accessions in a tropical forage grass.Crossref | GoogleScholarGoogle Scholar |
Cardoso JA, Jiménez JC, Rao IM (2014) Waterlogging induced changes in root architecture of germplasm accessions of the tropical forage grass Brachiaria humidicola. AoB PLANTS 6, plu017
| Waterlogging induced changes in root architecture of germplasm accessions of the tropical forage grass Brachiaria humidicola.Crossref | GoogleScholarGoogle Scholar | 24876299PubMed |
Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. Journal of Experimental Botany 62, 39–57.
| Ion transport in seminal and adventitious roots of cereals during O2 deficiency.Crossref | GoogleScholarGoogle Scholar | 20847100PubMed |
Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665–681.
| Flooding tolerance: suites of plant traits in variable environments.Crossref | GoogleScholarGoogle Scholar | 32688679PubMed |
De Simone O, Haase K, Müller E, Junk WJ, Hartmann K, Schreiber L, Schmidt W (2003) Apoplasmic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species. Plant Physiology 132, 206–217.
| Apoplasmic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species.Crossref | GoogleScholarGoogle Scholar | 12746526PubMed |
Dias-Filho MB, Carvalho CJR (2000) Physiological and morphological responses of Brachiaria spp. to flooding. Pesquisa Agropecuária Brasileira 35, 1959–1966.
| Physiological and morphological responses of Brachiaria spp. to flooding.Crossref | GoogleScholarGoogle Scholar |
Gibberd MR, Gray JD, Cocks PS, Colmer TD (2001) Waterlogging tolerance among a diverse range of Trifolium accessions is related to root porosity, lateral root formation and ‘aerotropic rooting’. Annals of Botany 88, 579–589.
| Waterlogging tolerance among a diverse range of Trifolium accessions is related to root porosity, lateral root formation and ‘aerotropic rooting’.Crossref | GoogleScholarGoogle Scholar |
Gibbs J, Turner DW, Armstrong W, Darwent MJ, Greenway H (1998) Response to oxygen deficiency in primary maize roots. I. Development of oxygen deficiency in the stele reduces radial solute transport to the xylem. Australian Journal of Plant Physiology 25, 745–758.
Gronewald JW, Hanson JB (1982) Adenine nucleotide content of corn roots as affected by injury and subsequent washing. Plant Physiology 69, 1252–1256.
| Adenine nucleotide content of corn roots as affected by injury and subsequent washing.Crossref | GoogleScholarGoogle Scholar | 16662381PubMed |
Haque ME, Oyanagi A, Kawaguchi K (2012) Aerenchyma formation in the seminal roots of Japanese wheat cultivars in relation to growth under waterlogged conditions. Plant Production Science 15, 164–173.
| Aerenchyma formation in the seminal roots of Japanese wheat cultivars in relation to growth under waterlogged conditions.Crossref | GoogleScholarGoogle Scholar |
Hirabayashi Y, Mahendran R, Koirala S, Konoshima L, Yamazaki D, Watanabe S, Kim H, Kanae S (2013) Global flood risk under climate change. Nature Climate Change 3, 816–821.
| Global flood risk under climate change.Crossref | GoogleScholarGoogle Scholar |
Jiménez JdlC, Cardoso JA, Arango-Londoño D, Fischer G, Rao I (2015a) Influence of soil fertility on waterlogging tolerance of two Brachiaria grasses. Agronomia Colombiana 33, 20–28.
| Influence of soil fertility on waterlogging tolerance of two Brachiaria grasses.Crossref | GoogleScholarGoogle Scholar |
Jiménez JdlC, Cardoso JA, Dominguez M, Fischer G, Rao I (2015b) Morpho-anatomical traits of root and non-enzymatic antioxidant system of leaf tissue contribute to waterlogging tolerance in Brachiaria grasses. Grassland Science 61, 243–252.
| Morpho-anatomical traits of root and non-enzymatic antioxidant system of leaf tissue contribute to waterlogging tolerance in Brachiaria grasses.Crossref | GoogleScholarGoogle Scholar |
Jiménez JdlC, Kotula L, Veneklaas EJ, Colmer TD (2019) Root-zone hypoxia reduces growth of the tropical forage grass Urochloa humidicola in high-nutrient but not low-nutrient conditions. Annals of Botany 124, 1019–1032.
| Root-zone hypoxia reduces growth of the tropical forage grass Urochloa humidicola in high-nutrient but not low-nutrient conditions.Crossref | GoogleScholarGoogle Scholar |
Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytologist 106, 465–495.
| The anatomical characteristics of roots and plant response to soil flooding.Crossref | GoogleScholarGoogle Scholar |
Kato Y, Abe J, Kamoshita A, Yamagishi J (2006) Genotypic variation in root growth angle in rice (Oryza sativa L.) and its association with deep root development in upland fields with different water regimes. Plant and Soil 287, 117–129.
| Genotypic variation in root growth angle in rice (Oryza sativa L.) and its association with deep root development in upland fields with different water regimes.Crossref | GoogleScholarGoogle Scholar |
Kirk GJD (2003) Rice root properties for internal aeration and efficient nutrient acquisition in submerged soil. New Phytologist 159, 185–194.
| Rice root properties for internal aeration and efficient nutrient acquisition in submerged soil.Crossref | GoogleScholarGoogle Scholar |
Kotula L, Ranathunge K, Schreiber L, Steudle E (2009) Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. Journal of Experimental Botany 60, 2155–2167.
| Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution.Crossref | GoogleScholarGoogle Scholar | 19443620PubMed |
Kotula L, Clode PL, Striker GG, Pedersen O, Läuchli A, Shabala S, Colmer TD (2015) Oxygen deficiency and salinity affect cell-specific ion concentrations in adventitious roots of barley (Hordeum vulgare). New Phytologist 208, 1114–1125.
| Oxygen deficiency and salinity affect cell-specific ion concentrations in adventitious roots of barley (Hordeum vulgare).Crossref | GoogleScholarGoogle Scholar | 26094736PubMed |
Kotula L, Schreiber L, Colmer TD, Nakazono M (2017) Anatomical and biochemical characterisation of a barrier to radial O2 loss in adventitious roots of two contrasting Hordeum marinum accessions. Functional Plant Biology 44, 845–857.
| Anatomical and biochemical characterisation of a barrier to radial O2 loss in adventitious roots of two contrasting Hordeum marinum accessions.Crossref | GoogleScholarGoogle Scholar | 32480613PubMed |
Kutscha NP, Gray JR (1972) The suitability of certain stains for studying lignification in balsam fir, Abies balsamea (L.) Mill. LifeSciences and Agriculture Experiment Station Technical Bulletin 53, 1–70.
Lux A, Morita S, Abe J, Ito K (2005) An improved method for clearing and staining free-hand sections and whole-mount samples. Annals of Botany 96, 989–996.
| An improved method for clearing and staining free-hand sections and whole-mount samples.Crossref | GoogleScholarGoogle Scholar | 16192293PubMed |
Mendiburu F (2014). Agricolae: statistical procedures for agricultural research. R package. Version 1.1–8. Available at http://CRAN.R-project.org/package=agricolae [Verified 18 November 2020]
Miles JW, Do Valle CB, Rao IM, Euclides VPB (2004) ‘Brachiariagrasses.’ Warm Season (C4) Grasses, Agronomy Monograph no. 45. (American Society of Agronomy, Crop Science Society of America, Soil Science Society of America: Madison, WI, USA)
Oyanagi A (1994) Gravitropic response growth angle and vertical distribution of roots of wheat (Triticum aestivum L.). Plant and Soil 165, 323–326.
| Gravitropic response growth angle and vertical distribution of roots of wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Pedersen O, Colmer TD, Sand-Jensen K (2013) Underwater photosynthesis of submerged plants – recent advances and methods. Frontiers in Plant Science 4,
| Underwater photosynthesis of submerged plants – recent advances and methods.Crossref | GoogleScholarGoogle Scholar | 23734154PubMed |
Pedersen O, Sauter M, Colmer TD, Nakazono M (2020) Regulation of root adaptive anatomical and morphological traits during low soil oxygen. New Phytologist
| Regulation of root adaptive anatomical and morphological traits during low soil oxygen.Crossref | GoogleScholarGoogle Scholar | 33222170PubMed |
Ramalingam P, Kamoshita A, Deshmukh V, Yaginuma S, Uga Y (2017) Association between root growth angle and root length density of a near-isogenic line of IR64 rice with DEEPER ROOTING 1 under different levels of soil compaction. Plant Production Science 20, 162–175.
| Association between root growth angle and root length density of a near-isogenic line of IR64 rice with DEEPER ROOTING 1 under different levels of soil compaction.Crossref | GoogleScholarGoogle Scholar |
Rao I, Miles J, Wenzl P, Louw-Gaume A, Cardoso JA, Ricaurte J, Polania J, Rincón J, Hoyos V, Frossard E, Wagatsuma T, Horst W (2011). Mechanisms of adaptation of brachiariagrasses to abiotic stress factors in the tropics. In ‘Proceedings of the 3rd international symposium on forage breeding, Bonito, Brazil’.
Shiono K, Yamauchi T, Yamazaki S, Mohanty B, Malik AI, Nagamura Y, Nishizawa NK, Tsutsumi N, Colmer TD, Nakazono M (2014) Microarray analysis of laser-microdissected tissues indicates the biosynthesis of suberin in the outer part of roots during formation of a barrier to radial oxygen loss in rice (Oryza sativa). Journal of Experimental Botany 65, 4795–4806.
| Microarray analysis of laser-microdissected tissues indicates the biosynthesis of suberin in the outer part of roots during formation of a barrier to radial oxygen loss in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 24913626PubMed |
Sorrell BK, Mendelssohn IA, Mckee KL, Woods RA (2000) Ecophysiology of wetland plant roots: a modelling comparison of aeration in relation to species distribution. Annals of Botany 86, 675–685.
| Ecophysiology of wetland plant roots: a modelling comparison of aeration in relation to species distribution.Crossref | GoogleScholarGoogle Scholar |
Striker GG, Insausti P, Grimoldi AA, Vega AS (2007) Trade-off between root porosity and mechanical strength in species with different types of aerenchyma. Plant, Cell & Environment 30, 580–589.
| Trade-off between root porosity and mechanical strength in species with different types of aerenchyma.Crossref | GoogleScholarGoogle Scholar |
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics 45, 1097–1102.
| Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions.Crossref | GoogleScholarGoogle Scholar | 23913002PubMed |
Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SV, Rebetzke GJ, Kirkegaard JA, Christopher J, Watt M (2012) Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. Journal of Experimental Botany 63, 3485–3498.
| Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops.Crossref | GoogleScholarGoogle Scholar | 22553286PubMed |
Wenzl P, Mancilla LI, Mayer JE, Albert R, Rao IM (2003) Simulating infertile acid soils with nutrient solutions: the effects on Brachiaria species. Soil Science Society of America Journal 67, 1457–1469.
| Simulating infertile acid soils with nutrient solutions: the effects on Brachiaria species.Crossref | GoogleScholarGoogle Scholar |
Wiengweera A, Greenway H (2004) Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation. Journal of Experimental Botany 55, 2121–2129.
| Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation.Crossref | GoogleScholarGoogle Scholar | 15310817PubMed |
Wiengweera A, Greenway H, Thomson CJ (1997) The use of agar nutrient solution to simulate lack of convection in waterlogged soils. Annals of Botany 80, 115–123.
| The use of agar nutrient solution to simulate lack of convection in waterlogged soils.Crossref | GoogleScholarGoogle Scholar |
Yamauchi T, Abe F, Tsutsumi N, Nakazono M (2019a) Root cortex provides a venue for gas-space formation and is essential for plant adaptation to waterlogging. Frontiers in Plant Science 10, 259
| Root cortex provides a venue for gas-space formation and is essential for plant adaptation to waterlogging.Crossref | GoogleScholarGoogle Scholar | 31024577PubMed |
Yamauchi T, Tanaka A, Inahashi H, Nishizawa NK, Tsutsumi N, Inukai Y, Nakazono M (2019b) Fine control of aerenchyma and lateral root development through AUX/IAA- and ARF-dependent auxin signalling. Proceedings of the National Academy of Sciences of the United States of America 116, 20770–20775.
| Fine control of aerenchyma and lateral root development through AUX/IAA- and ARF-dependent auxin signalling.Crossref | GoogleScholarGoogle Scholar | 31548376PubMed |
